Documenti di Didattica
Documenti di Professioni
Documenti di Cultura
.'
I
I
I
,,
.'
Third Edition
. . . . : ... . :'.:
,
,"
'." ",
'.
",
.'
'.
'
..
...
..
...
Third Edition
Bryce Kendrick
..
,
,,
,
Foclls Publishing
R. Pull ins Company
Newburyport MA 01950
USA
IV - E)'"
. ~F_deP""""'bUCO
~lellOTECA CENTRAL I C1DADE UNIVERS~ARIA
CEP 50.670-901 Recife pernarnbocO - Brasil
Reg. n- 9957 -2AI1112OO6
m ula: THE RFTH KINGOOM
10
I,
V03101l 81BQ
800'3 d~n
/if
Table of Contents
Preface ............ ... ..................... ..... _................. _........ ............................... .... ... VII
Acknowkdgments ....................................................................................... viii
Introduction ................................... _............. _................................................. xi
l.
2.
3_
4.
5.
6.
7.
8.
9.
10.
II.
12.
13.
14.
15.
16.
17.
18.
19_
20.
21.
22.
23.
24.
~ UFP;:CCB
~B I BL IOTECA
Preface
"Fungi probably rival flowering pl:lnts in their species diversity, and outweigh the
animal kingdom. Whilst wield ing great destrocti~'e power as agents of disease and decay,
they drive the global carbon cycle, sustain our forests and grasslands via mycorrhizal
associations. and clothe. as lichens, what wou ld otherwise be bare parts of the plane!.
Their developmentally versatile body forms provide immense scope for industrial exploitation as well as experimentally acce ss ible systems for studying fundamental biological
issue,. Yet most people's appreciation offungi stops at mushrooms. mouldy food and fairy
tales.
"Challenged by such ignorance. mycologists need to overcome some deeply rooted
prejudices. On the one hand. the variety. edibility and toxicity of fungal froit bodies has
always been a sOurce of fascination v>'hieh can be relied on to deliver new recroir.s to the
cause of mycology. but if that fascination becomes an obsession. the cause is lost.
hOn the othe r hand, mytologists working on disease tontrol. taxonomy or some
indl.lstria! pllXess often find it difficult to communicate the wider interest of what they are
doing. Because of the vicious cycle of neglect. their task is lUade harder by the need to use
technical' terms: piant scientists tan assl.lme that their audience knows what leaves, roots
and stems are: mycologists always have to explain what hyphae and mycelium are.
50 there are IWO images of the mycologist: one of the eccentric amateur, the other
of the remote profeSSional working on esou::ric problems. Both are damaging."
So writes ProfeSlior Alan Rayncr, one of mycology's mOSt aniculate spoke..~pcrsons,
and it is impQSsiblc to disagree with him. Perhaps this book can do something to produte
a more b~!anced understanding and appreciation of fungi among university students and
intelligent lay persons. Interest is the best st imul3nt to learning, and at least some of the
slOrics in this book will surely tickle even the most jaded p:date. since the fungal lifestyle
is so bi~arre, Ihe faCtS so strange. Science fiction writers. look no funher. Plots lie within .
So far. we ha,c described about 100.000 fungi. yet we estimate these to represe nt
less than onctcnth of the Earth's mycota. Part of this book. then. is a telebTiltion of
biodiversity: jusl think. there arc over len thousand spe-cies of mushrooms alone. Tragically. the world is gf'ddually losing its biological richness. As a resull of human activities.
speties ofliving orgJnisms, fungi among them. are being driven irretrievably imo c~tinc
tion every day. We need you. the readers of this book. to help stop those losses. There rue
many kinds of environmental action: may J urge you to become personally involvcd in
some of them. Our grandchildren wiUlhank us, but only if we succeed.
viii '
PREFACE
The CD-ROM which should be used in parallel with this book con tains many
images of fungi, but Twould like you to look OUt for pictures of fungi that I have found in
my own garden, or on the beach below my house. I have emphasized these to show you
that ifyoti keep your eyes open, you too should be able to find just as many fungi in your
own surroundings.
Acknowledgments
Mycology has now become so multifaceted, and each of itS many aspectS so spe
daliw:!, that il is increasingly difficult for one person to write a troly comprehensive text.
This book and CD-ROM may well prove that point, though I did nOI prepare them unaided. I am grateful to Joan Bennett (Tulane University), Bernie Glick (University of
Waterloo), and Jim Anderson (University of Toronto), fOf their input to earlier versions of
the genelics chapter, and recently to Brenda Wingfield (University of Pretoria) who made
vital contributions to the molecular aspects of the chapter as it appears in the third edition
and on the CDROM, I thank Shannon Berch of the BC Provincial Forest Service for
giving me access to her fine pbolomicroscOpe, which has provided a number of liIe
photomicrographs to be found on the CDROM.
Donald Barr (Biosystematics Research Institute. Ottawa) made sure the original
chapter on fungi with flagellate cells was up-to date, and supplied several original ill ustrations. George Barron (University of Guelph) supplied interesting new infonnation for
the revision of the chapter on fungi exploiting microscopic animals, and pennission 10
use his excellent photomicrographs. Alan Watson (Macdonald College of McGill Universi ty) sem me new material on biological control of weeds by fungi: John Rippon (Universit)" of Chicago) provided many helpful comments on medical mycology. Dr. Zheng Ru
yong (Academia Sinica, Beijing) gave me invaluable advice about the Erysiphales.l am
grateful to Dr. Henry Descals for a detailed and most helpful critique, which was valuable
in the preparation of the second edition.
I also thank the following professors who used the book in their courses, and provided me wilh useful feedback: Margaret Barr. George Barron. Lynn Margulis. Peler
Neumann, G.B. Ouellette, R.D. Reeleder. John Rippon, Suzanne Schwab, Don Thomas.
Mikoe Tansey reviewed the second edition and many of his suggestions were incorporated
in its second prinling. For the egregious errors and misinterpretations that undoubtedly
remain in thc third edition and the CD-ROM version, I accepl sole responSibility.
PREFACE ix
pencil sketches. line drawings, photographs, colour transparencies. microscope preparations and macroscopic specimens-is dc:c:ply appredated. Some drawi ngs were kindly
provided by Frank DiCosmo, a former graduate student of mine who is now a professor at
the University of Toronto. and Ms. Gracia Murase. my able and versatile technician.
executed a number of drawings and diagrams. She also helped in other ways--compiling
the glossary and the index. making drawings and calligraphing titles. retyping lost files,
doing paste-ups of plates, proofreading and editing. numbering and labelling-and I am
indebted to her for her help, without which the publication of the second edition would
have been much delayed. In 1984-5 I composed the original manuscript on an Apple ll+
Microcom puter, using the Easywriter word processing program (which camouflaged my
almost total lack of typing sltil!). In 1985. the camera-ready copy was produced by a
Muitiwriter IV daisywheel printer using multistrik.c: carbon ribbons. The text for the second edition was prepared in 1991 on a new-generation PC: an MS-DOS clone wi th an
Intel 386 microprocessor runni ng at 25 MHz. using WordPerfect 5.1. The text and the
HTML version of the third edition h(lVe been pm together on 350 MHz and 600 MH z PCs
running WordPerfect 8 and Front Page 98 and 2000. The hundreds of colour illuslr3tions
on the web and CD-ROM versions of the book ha~"e been either scanned by an HP Scanjet
4C flatbed scanner with a transparency adapter. or taken with a Ricoh RDC-S300 2.3
megapixel digital camera. The image files were trdfisfonned and resampled with Web
Graphics Optimizer 4.0. The video sequences on the CD-ROM were imported from my
own Hi8 videotapes by a Matrox Marvel G400-TV video card and Avid Cinema software.
The over 1,100 illustrations have been derived from a variety of sou rces. My own
collection of teaching transparencies and digital images provided the majori ty. but many
othe r mycologists have given me images over the years for teaching purposes. I am
P'lJ1.icu!arly indebted to George Barron, my erstwhile colleague at the University of Guelph.
for many fme images (and for almost all of those associated with chapter 15). Credit has
been given in many places. but sometimes I have had an image for so long thaI I have lost
track of its source. I must ask forgiveness of those whose contributions are not acknowledged. and I will be more than happy to add further attribut ions to future versions of the
CD-ROM.
I retired in 1994 to my dream waterfront home on Vancouver Island. J had no ide a
that 1998, 1999 and 2000 would be filled with the activity of producing web and CDROM editions of my book. and the third edition oflhe printed version. The lure of the new
technologies was too strong. and I succumbed to their possibilities. I hope those who use
the book and CD-ROM in tandem will feel that these efforts have been worthwhile. and
that at least some of those possibilities have been realized.
Bryce Kendrick
Sidney-by-the-Sea
British Columbia, Canada, V8 l IM8
September 2000
bryce@mvcQ\og,s;om
www.mycolog.com
UF FECCB
BIB LIOTECA
Introduction
lmagiflC the picnic of your dreams. You and your loved one float across II flower-filled
meadow, coming to rest under the shade of a giant white pine. There you spread out the
magic ingredients-the champagne(ofwine. or beer, if you prefer), the fresh crusty bread,
the p~te au truffe, the creamy camembert (or brie or roquefort) cheese. You may add other
ingredients -
str:ues, 3nd thc'i1.lcohol thcy contain is a fungal metabolite highly prized by those who
need an occasional escape from rcality Even those who prefer (0 kecp reality at ann's
length with psilocybin or L.S. D. usually know thaI these psycholropic substances are also
fungal melllbolitcs.
Bread owes its lightness and texture to the ' raising' activities of a fungus. The
mouth-watering fl avour of your pate is enhanced by the presence of pieces of black
trume, a subterranean fungus from Europe. The cheeses are ripened and given their unique
texture and ta51e by specific moulds.
But fungi, like people, ha"e a darker side. On closer inspection, the flowers in the
meadow may be found to be suffering from II host of fUllg~1 diseases - leaf spots, wilts,
mildews, blights lind more -and the pine tree may have problems with root rOl, heart rot,
blister rus.t and needle cast, all caused by fungi. Some oflhe food in your picnic may have
been insidiously infiltrated by fungi. Those ripe. juicy peaches ),ou brought along for
dessert may reveal rapidly spreading brown arcus. You must trust thaI the bread wasn't
made from wheat containing vomilOxin, or if it's rye bread, that no ergot, with its mllll!IUde of alkaloids and hallucinogens, was in the grain. Even your blue cheese and yoor
peanut butler could possibly contain myCOlo;o.:ins,
Homeowners know this other face, too. Has your wooden fence or your deck become rOlten and needed rebuilding? Has yOllr prile elm (fCc died, or your chestnut been
defoliated by leaf blight? Are your roses besmirched by black ~POI. ),our lilacs by powdery mildew, you r hollyhocks by IIlst? Do YOUf tOmatoes suffer from early blight, your
potatoes from late blight, your ~rapes from downy mildew, your strawberries from grey
mould? Are your JX'acbes attacked by leaf curl or soft rot, your apples by scab? Does
damping-off cause your seedlings to keel over? Does food go mouldy, tuming green. pink
or brown, or growing whiskers, even in the refrigerator? And is there aereeping black stain
around the door of that appliance? Have you ever had athlete's fOOl, or jock itch, or
ringwonn of the scalp? All of these, too, are the results of fungal activity.
But there's still another side 10 the fungi. 'The blister rust on your pine tree may itself
be allacked and controlled by anomer fungus, as may the powdery mildew on the grass.
Specialized fungi can control infestations of insects in your garden. A fungal metabolite
is used world-wide to control many bacterial infections (including gonorrhea), while
another can cure some of the fungal diseases that afflict people from time to time. Organ
transplants now have much improved chances of succes.s because of a fungal metabolite
that safely prevents the body from rejecting the new organ, and this same substance seems
to StOp the development of some kinds of diabetes - the nrst actual cure ever discovered
for this disease.
These are a few of the reasons why you should know something about fung i. I hope
that by the end of this book, which I have tried to prepare as a tasry mycological smorgasbord. you will be able to add other reasons of your own.
Kingdoms, Classification
and Biodiversity
Kingdoms -
As you read the text that follows, you rnay come across words that are new 10 you.
Mos t of them will be in the glossary. If even the definitions given there leave you scratching your head, r suggest you find and rcad a first year University Biology tc)(thook before
going much further.
You may not know it, but you are about to become a member of an elitc: group.
Although many people are aware that there are millions of different kinds (s pecies) of
living organisms on'Earth today (although OI.IT own species is doing its beSllOdrivc: many
of them into e;~tinction). surprisingly few people are aware thaI these organisms are now
di vided up among no fewer than se\"en Kingdoms. Before I can effectively develop the
theme of this book [must explain these major panel'Tl5. and those of some of the almost
one hundred distinctive evolutionary pathways known as Phyla (botanists sometimes
call them Di,isions) which make up those Kingdoms.
The really basic division among life fonns is between the simpler Prokar yotes and
the more complex Euka ryo t e.~. Look at the diagram below (after Patterson & Sogin
1992): it shows {he way in whicll we thin k the Kingdoms evolved. It is based on molecular
evidence: base sequences from ribosomal RL'fA.
The earliest foons of life, which appeared about 3,500 million years ago. were
prokaryotC5. We tend to define them by their relative morphological simplicity. and by
the absence of many features found in more modem cells. Although thei r modem descendants have a single ch romosome. this is no! found inside a nu cleus. and thei r cytoplasm
contains no mi IOcho nd r i3 or plastids (cytoplasmic orga nelles). These organisms make
up the baseline Kingdoms Arch:leb:lcteria and Eubactcria.
The prokaryotes had the world to themselves for 1.500 million years (the y did.
however, invent photosYflt hesis during that time). Not until about 2 billion years ago did
life take the next giant step. the evolution of the eukaryotic cell. Many biologists now
believe that th is arose as a result of the mutually beneficial symbiotic uni on of several
different kinds of prokaryote within anothe r host-prokaryote. (I) Mitochondria spo:cialize
in the oxidation of 3-carbon organic acids (the Krebs cycle). providing an immediately
availahle energy supply in the form of ATP. (2) P lastids may contain photosynthetic
pigments and enzymes (chloroplasts). or may store food. Many of us are convi nced that
2 CHAPTER ONE
;0
o
>-
0:
;2
_ ,PROTOZOA
,-
=>
w ,/ "
,
,,
,
,,
,,,
,
,
,, ,
,,
,,
,
,,
,,
,,
,,
,,
,,
1,,
,
1 , 1,
,,
I, ,,I
,,
,
",
~ , .- --, ,,-
,<
,
,,,
,,
,,
,,
,,
,,
,,,
,
'.
,,
,,
,,
,,
g
~
""o
:.:
0:
"-
'"
.,'
.'.- "
'
,,
mitOChondria. p!astids and eyen (3) nage lla were once r"'' e-living prokaryOkS. which
were e ngulfed and co-opted during the evolution of the eukaryotie cdl to ~come specialized and efficie nt components of the ncw. more sophisticated syStem.
EUlcaryotic cells also have their DNA organ ized into a number of discre tc chromosomes, which are found inside a nucleus which is surrounded by a membrane. Cell divi_
sion in eukaryote5 involves a complex process called mitosis. The nuclcar membrane
breaks down. a mitotic spind le of microtubules develops, and the chromosomes are
duplicated. Then the daughter chromosomes separate and are pulled to opposite poles by
the contracting spindle fibres. Each set of chromosomes then becomes enclosed by a ncw
nuclear membrane. and the cell finally divides into two.
Prokaryotic cclls have only a single. usually circular chromosome. and do not
undergo mitosis. They usually divide by a much si mpler process called bin3ry nssion.
Mitosis, with ils very accurate duplication and sharing of the genetic material. seems to
have been a C'l'lIcial invention. Only eukaryotic cells. with their precisely regulated genetic mechanisms. apparently had the potential!() evolve into more complex, multicellular organisms in which cells are organized into different tissues and organs. All prokaryotes are still microbes.
Now look at the Kingdom diagram again. The Archaebacteria and the Eu bacteria
are prokaryotes. lbe eukaryotes encompass the Other five Kingdoms, and it is in th ese
other Kingdoms that the dazzling e\'Olutionary explosion o f new taxa has occurred. The
diagram shows five eukaryote Kingdoms: Protozoa, Chromista, Plan tae. Animalia and
Eumycot:l..
The e;ttplosion of eukaryote evol ution was made possible by. among other things. a
modified form of mitosis called me iosis or reduction division. In many organisms this
produces special sex cel!s called gametes. Each of these sex cells ha$ a single SCI of
chromosomes (w~ say that the gametes are haploid). When two gametes from compatible
parent organisms fuse. the resulting cel! (the zygote) has two sets o f chromosomes (we call
lhis condition diplo id). In plants and animals. zygotes develop into diploid, multic<;.ilular
organisms. but in most fungi the vegelative phase is always haploid. so meiosis must take
place in the zygote. Whether meiosis happens in the zygotc. or at the other end of the life
cycle, during the formation of gametes, it is responsible for the reassortment of the genetic
infonnation buill into the chromosomes.
New fcatures are constantly being added to the pool of genetic material by the
process of mutatio n. but sexuuI reproduction is the mechanism by which this pool is
recombined each generation in most eukaryotic organisms. producing an endless supply
o f variation upon which the processes of natural selection can work. This is one of the key
sec rets of eukaryote diversity.
The radiation of the twO unicellular Kingdoms (Protozoo and Ch romista) show)
how the evolution of the cukaryotic ee l! expanded life's horizons. But the full potential of
the new teamwork - J can it that, since sever.ll prokaryotes eooperate to make one functional eukaryotic eell- was not real ized until cells. as well as cen components. began to
cooperate. When organisms became multicellular. different cells could assume different .
specialized functions. This division of labour eventually led to the development of tissues and organs, and ultimately permitted the evolution of complex beings like our
selves, beings with almost infinitely expan ded capabilities (both wonderful and terrible).
Three new multicellular Kingdoms arose. exemplifying three different ways oflifc.
~Iu!ticellular organisms which could pho tosynthesize - make their own food from simple
inorganic precursors - were eaten by other multicellular organisms that lac ked this talent.
and both were recycled after death by a third group. These groups we calJ produce rs,
consumers and decomposers - the plants, the animals and the fungi. We rerognize about
4 CHAPTER Ol"l'E
9 phyla of plants, about 32 phyla of animals. and 5 phyla of fungi (2 chromistan and 3
eumycotan).
'The world being what it is, the picture is not as simple as we might like. Some of the
divergent paths of evolution have come together again, almost as they did at the birth of
the eukaryotes, and many organisms that seem unitary are, in fact, partnerships or even
consonia. Lichens, for example, always incorporate both an al ga (e ukaryotic or prokary
otic) and a fungus.
Howcan fungi fit into two Kingdoms? !be answer lies in the way we derme the tenn
fungus (plural: fungi). Fungi are eukaryotk heterotrophic, abso rpth'c organisms that
develop a rather diffusc, branched, tubular body and reproduce by means of spores.
This describes not a single ph)'logenetic liDe, but rather a way of life shared by organisms
of different evolutionary bac kgrounds. We recogni~e throm lstan fungi as well as
eumycotan fungi .
If you find this strange, consider the 'algae' for a mome nt - they include represen
tativc5 of three Kingdoms: eubacterial prok:aryoles (the blue-green cyanobacte ria),
chromiSlans (brown algae, diatoms. etc.) and plantae (green algae). Both algae and fungi
are defined functionnlly or ecologically, rather than phylogenetically.
At this point it beromes clear that this book does not, as its title implies, deal
exclusively with the fifth Kingdom, Eumycota, but also discusses some elements of Kingdom Chromista. But these latter are relatively minor players in the biosphere when compared with the huge numbers and biomasS of the Eumycota.
Biological Classification
The first part of this book deals with the classification of the fungi. You can eer'
tainly ignore chnpters 2-7, nnd mo"e quiddy to the more aecessible and, to many people,
mon: interesting ch;!pters later in the book which deal with the many ways in which fungi
imlXlct on human exiStence. Hov,-ever, I don', think I am overstating the case if I say that
unless you understand something about how the main groups of funSi differ in morphology and behaviour. you will not be able to make much sense of Ihe more 'relevant'
sections of the book. If you can develop a son of 'cognitive map' of the main classes.
recognizing them on sighl, and undcrs(~nding the unique abilities of each. you will find
the study of fungi - mycology - infinitely mon: rewarding.
Biological Nomenclature
Every species of living organism is a collection of individuals which are very
similar (genctically. if not always in appearance), and each species has a unique name
made up of twO wOrds, which may actually be from the ancient Latin lex.icon, but are far
mon: often new, ps~udo-Latin words coined for the occasion. This two-epithet name is Ihe
bi nomial. You and ( belong to the speeies Homo Sllpiens. The supcnnarket mushroom
belongs to the species Agaricus bnmnesctns. In each case the first of these two Latin
words is the gene ric name or epithet (this places the organism in a genus. a collection of
simil:lr andlor related spe<;ies). The second Latin word is the epithet applied to one particul:lf spceies of the genus. But notice thallhe name of the species always consists of
both epithets together. This is because only the two-word combination is aClUally unique
to that species. The generic epithet is shared by all Olher species in th;!! genus. The same
species epithet may also be applicd to species in other genera (for example. many Canadian spring flowers, though belonging to diffcrent genera, have the same species epithet.
canadensis. as does the national animal of Canada. the beaver), So remember that only the
IWO epithets together - the binomial - properly specify a species. Homo sapienl is the
only extant species in the genus Homo, but most genera contain more than one species.
Biodive rsity
Different strokes for different folks. For some people, place names are evocalive,
calling up vivid memories of past e.~periences. For me it is the names of organisms I have
seen that bring back those experiences. Melrvsideros exu/sa conjures up Christmas in
Auckland. New Zealand, where the red flowers of this tree adorn beaches in December.
Pro/tO. c)"IIaroide5 lakes me back to the am;u:ingly rich Fynbos plant communicy ifI South
6 CHAPTER ONE
Africa, where this Oamboyant shrub flouri shes, and has been adopted as the nati~nal
Oower. Amphiprion places me on the Barrier Reef in Australi ... where these agi le Imle
damsel fish with blue-white stripes live unscathed among lhe tenwcles of lMge sea anemo-nes. Such organisms and the communities and ec~ystems of whic~ they are P:uu. are ~e
real reasons I leave home. I hope that some of you will also come to think ufthe hlodlver"Slty
you encounter as a measure of your quality of life.
Biodiversity is one of the buzz-words of the nineties, and I for one hope that it will
continue to be a Dewsmaker in the new millennium. Biologists know from the earliest
years of their ttaining that the Eanh is blessed with an amazing number of differeD! Ihing
things. As you have just read. systematists have tried to catalogue and describe all these
riches. but with widely varying degrees of success. We know practically all the birds, and
almost all the mammals, that inhabit the eanh. But we know only a small fraction of the
ntthropods and fungi. How can I make those two statements 50 confidently? Because
although there are many omithologists and mnmmalogists scouring the globe for new
taxa, they rarely find any. At the other end of the scale, entomologists and mycologists
find new taxa every day. They have so far described approximately a million insects and
some where between 70,000 and 100,000 fungi. but it is obvious to the professionals who
work in these areas that huge numbers of both groups have not yet been descri bed. I began
my mycological career examining the sequence of fu ngi involved in the slow decomposition of Scots pine (Pin/IS s}'/Ies/ris) needles. Almost immediately I found several microscopic fungi which turned out to be new to science. and I had the privilege of deSCribing
thcse fungi (You can see some of them in chapter II of the CD-ROM). Since I movep to
Vancouver Island. off th e west coast of Canada, in 1994, I have seen many mushroo ms that
could not be identified using the e)l;isting literature. I am convinced th at many of these
fungi are actually undescribed.
How many fungi are wailing to be disCQ\ercd? D:lvid Hawksworth came up with an
ingenious ans"'cr a few years ago. Noting that Britain is among the most intensively
in\estigated areas on Eanh for plants and for fungi. he pointed out that almost all the
Oowcring plants in Britain are known. and that there are about 2,000 species. Although
the fungi of Britain are definitely not as full y known. since new ones are still being
described, abum 12.000 species have been recorded there. This gives a ratio of abuut si)l;
fungi to each plant species. Extnlpolating (perhaps rather ambitiously) from Britain to the
entire globe. Hav,-ksworth suggested that since there appear to be about 250.000 species
of Oowering planl.S in the world, there are probably sb: times as m~ny fungi - about
1.500.000 fungi, in facl. Even if this figure is an over-estim:lte. and there are onl) half a
milli on fungi, we have still described only 20% of the total. and a huge task lies before us.
But if we accept this figure as a workiny approxima tion (and no one has yet come up
with a different formula), it brings us to a realization that about two centuries of mycology
have so far succeeded in describ ing only about 6-7% of the world's rnycota - a pretly
shocking Slate of affairs. Over the years I have been involyed in describi ng probably three
hundred fungal ta.t a. and have now basically run out of steam in this area of mywlogy.
But e,en if all the mycologists alive today were to publish 100 spa:ies apiece, they would
still manlge to describe only about 300.000 taxa. So it is a multi-generatio[l.al task.
The preceding discussion assumes a steady state in whi ch no species are added, and
none subtracted. from the global total. But we know that this is not t.he else. New species
are arising con~tantly. albe it at an unknown fate. as results of the combined effects of
selection pressure and genc tic recombination. Our own specics. by sticking its fingers
into every existi ng niche and ecosystem, as well as creating new ones. is undoubtedly
providing the fungi wi th new challenges at every tum, and they are surely responding to
those challenges by sp;twning ne w taxa.
-.
Fig 1.2 Dr. 8obMurphy, with a flTe-belied toad from
Vietnam-protection for f~
But o ne of our problems in North America is that we do not have exte nsive records
of the myCOtll from the past - a base-line with which present-day comparisons can be
made. Fortunately, so me European countries, with centuries of datil collec tion to dr,lw
upon, have tx:en ab le to document the decline in num bers of mDny fu ngi. and hllVe
published what they call Red Lists, Thes.: listS highlight the increasing rarity of many
fungi. and the appa~nt disappearance of somc,
So what doc s a fire-bellied toad from North Vietnam have to do with prese rving
fungal diversity? Re3d on... Dr. Bob Murphy. Director of Ihe Royal Ontario MU$Cum's
Centre fo r Biodiversity and Conservation Biology. reports in Ihe Globl" and Mail for Jllly
12th, 1999 that he has JUS! retumed from collecting herpeti les (amphibia and reptiles) in
the North Vietnam ra inforest. His comments about his animals are worth repeating here.
"BeeaU!;e th ey're beautiful, aesthetic ally appealing. wonderful animals, you can get them
protected. If you can get them protected. you protect the forest. If you protect the forest,
you pr(){ecl everything that's there, l"S{Hci(1Uy tire fUngi (my italics), which are producing
the majority of new pharmaceuticals that are coming out:' You will find an echo of that
statement in chapter 24, in the discussion of antibi otics, immunosuppressants and other
fungal metabolites.
So ou r efforts to collect (md describe the world's myeota need to be redoubled. As
you will learn from many of the other chapters in this book, and perhaps mOSt accessibly
fromchapter24. many fungi eonfe r e normous be nefits on Mank ind_ I am nOt just referring
to tbe producers of ant ibiotics such as pe nicill in and imm unos up pressant s like
e)'elosporine. but also to the myriad species which recycle organ ic matter. especially
plant debris. and to the others that establish obligate mUlualistic symbioses with many of
ou r most imponant plants.
This awareness of our ignorance has led 10 proposals 10 compile whDt are call ed
"All-Taxa Biodh'ersily lOHmtories" Of "ATBT" for sho rt, A meeting [ 0 discuss such an
ATBI for a forested area in COSta Rica came up with a fi gu re of 520 million for the fUllgi
alone. Although the Costa Rican venture didn 't ny, it spawned a margi nall y less ambi -
lj
CHAl'TKI{UN~
tious projel:t for the Great Smoky Mountains National Park in Tennessee. Setting other
organisms aside, it has been estimated thai there are 20,000 fungi in the Park, of which
only 2,250 have so far been described, (Hey, that's more than 10%, 50 we are already ahead
of the game.) A two-year pilot project aimed al refining sampling methods and data
protocols was begun in M~h 1999. and mycologists everywhere will be watching with
in terest (or being co-opted) as this unfolds. To learn more about this project. visil the web
site hltp:J/www,disco'-erlife.org
~;
A Mixed Bag:
Protozoan 'Pseudofungi'
(the so-called "Slime Moulds" Phyla MYXOSTELlDA, DICTYOSTELIDA,
lABYRINTHULlDA, PlASMODIOPHORIDA),
Chromistan Fungi
(Phyla HYPHOCHYTRIOMYCOTA and
OOMYCO:rA),
Eumycotan Fungi (Phylum CHYTRIDIOMYCOTA)
Firsl let me elaborate a little on the definition of fungi given earlier. Fung.i..~jJelher
chromista/.l
,
cell ulose, and with in this wall the cytoplasm and nuclei live and move. protected from the
o utside world, bu t able to explore small areas of it inside their apically extending, microscopic. hyphal tunnels, and much larger areas by means of their OetaChable r~roducti\'e
units called s pores.
But before I discuss real fungi. four "outsider" phyla must be mentioned. These are
the so-called ,.
I
""
I .
\0
t
t of as fungi,
are still
with in some
curtent mycological literoturc. this is at least phy logenetically incorrect. Here's why. The
assimilative or somatic phases of three of these four groups are basically amoeboid: none
of the four ever produces hyp hae (a diagnostic feature of most true fungi), and the assimilative plasmodia have no cell walls. The names currently applied to some of these groups
an: mi~ing, in that they imply a fungal nature, so in three cases I have supplied DeW
names renect;'ng their non-fungal affiliations. I hope you will agree with me .a~r yOU
have read the thumbnail sketches below and compared them with my later descnpllons of
10 CHAPTER TWO
the waH-possessing hyphal fungi. These phyla are included in some mycology courses
because some of them (particularly My~ostelida) tend to tum up when we look for fungi.
And if mycologists, who have historically looked after them, ilbandon them, which other
group of organismic biologist~ will agree to add these organisms to their already crowded
course schedules?
id
"
--
';XX.
ge''''i nation
m,
"'''''09a
i">o'e)
Fig~ 2.1
A l\IlX ED BAG 11
.., ,~~ vidual amoebae which feed by ingesting bacteria , The reproductive phase begins when
t t ~ the amoebae begin 10 secrete cyclic adenosine mooophosphate (cAMP), a son of phewt,
0
!!lone which cau~ the anlOt:;.~ t~ be..!!lutually attracted. They stream together and form
aggregations called pseudoplasmodia or :&l!J::f (these differ from lltte plasmodia in that
L.;
each amoeba retains its cell membrane). Each slug crawls around until dry conditions
~1
prompt it to undergo differentiation, heaping itself up and eventually fOrming a Smlcture
~)
called a sorocarp...which has a slim cellulosic stalk and an expanded head comaining
spores. Dictyosteiium has been used as an experimental organism by many sciemists
because it provides a simple system for studying differentiation. (Fig. 2.2)
(. \.;
(f>,y..
..... r'
;-1,
'~ 1
It
"r;
,;
0}
'
J?-
--Co
one of the few marine flowering plant~). e s'j,t;;-dlc-shaped. naked cells of rne....co1ony-J
live and move entirely ~thil!.a networ of narrow, tubular, polysaccharide sheathS which
they themselves secrete. They release biflagellate gametes, and the zygOie divides mitotically to generate a new colony, whose cells are presumable diploid. Most orner members
oflhis group are also marine. parasitizing algae. (Fig. 2.3)
~I
\
("(" ~
Tn.
J~ ~b ~ "iE:!
~ 2
11-'; ~~ \, "/
:1:r .. 1/
s-.
J'
.
<j.V::>~
-:z;.~~~t,.0-"
~ "C~~1"'~
~ ---"'~.
-'<),<:, "'" 0
...-..
"c,-
_.
I-'"
vJ)"'1-
~=~~
\
.l.
""'-
~ UFPE.CCB
DBIBLIOTECA
12 CH APTER TWO
b=""~,J'
ofi~()S9
cabbage (Brassica oluacea). Inside, they grow into multinucleate
microscopic
primary plasmodia. These eventually develop II wall and divide internally into uninucleate se<:ondary sporangia. These germinate, releasing four secondary. biflagellate z~pores
which leave the host. These may also act a.~ gametes. fusing in pairs, but soon-infe<:t a root
again, developing within host cells into mu ltinudeate secondary plasmodia. At marority,
these can. cleave into uninucleate cysts, each containing a single spore, which can persist
in the soil for many years. ThIs parasite stimulates the cabbage roots to become grossly
swollen, a serious diseas'e' co ndi tion known as "club roo!." (Fig. 2.4)
"Real Fungi
The four groups just outlined are nOI fungi. Every other organism dealt with in this
book is II fungus.
As I mentioned in chapter I. what lILe call "fungi::.share many morphologica1..aru!
behavioural similarities in their ~milath-.e..p.base, buUb:ey.-do...not.ha.'iC. a _unifonn &!<. It now s~iiiSobvious that they have evolved from at least \WO ances;;;;"'"" . can produce cells that swim hy means of one or twO very fine
whiplike extensions
I flagell a (rather like the tails of sperms). T hree phy la Hyphochytriomycota, O om ycot:l and C hytridlomycota - fall into this category. Molecular evidence tells us that they are members of two different Kingdoms, the first two
being Chromistan in origin, the last (despite ils Oagc:Uars: phase) ElImYCQlao The other'
two main-line, largely terrestrial fungal phyla never have moiilc: cells. ami they _ the
(). Zygomycota and Dl kllryomyt:ot:1 - make up the rest of Kingdom Eumycota~thollgh
only the Dikaryomycota produce highly_diff!.rentiated, multiccJlufllf'reproductive struc\ lUccs.as you will sec.
\~
Before I introduce you to the three flagellate phyla, a few words about flagella
.C5
(singul ar: flagellum). These are very long, narrow organelles. essentially contractile ex~
g
tensions of a cell. which have the ability to beat. or make whip-like motions. Th is beating
confers roolility on the cell: flagella move the cell about in water, giving it the ability to
)9
swim up chemical gradients (that is, 10 move from a lower concenu'l.Iion of a substance
toward a higher concenlrlltion), such as those which lead toward a sexual paMer or a
\:(10
suitable host organism.
"".YJ\ .n(f
~
.:g
J.2
c{:l.' q. 1
'"+
:::,:t;f.>;/C"'
,
A MIXED BAG 13 '
The amazing thing about flage!la is that wherever we find them among e~ar)'otic
organisms, they have esse ntially the same fine Structure: along the shaft of the fl~gellum
run 9 pairs of peripheral microt\lbules and 2 central microtubu!es - the 9 + 2 "Pauem.
Each microtubule is buill from II protein called tubulin, its subunits arranged in 13 vertical staclcs (count them in Fig. 2.5) around a hollow centre.
"
Th.is picture ofa transverse section of a flagellum (which is about one-sixth [0.17J of
a micron thick) would look more or less the same whether the flagellum came from one of
the simple fungi discussed here, or from a protozoan such as Poromot!cium (which has lots
of short flagella called cilia allover the outside of the cell).
Of
from II unicellular or
colonial green alga, a sea gooseberry (a Ctenophore) whi ch bas plales of cilia that beat in
rhythm and move the whole macroscopic organism, or from the spenn (male gamete) of a
brown alga, 11 sea urchin, a moss, a (ern, or a human. You see, all eukaryOles really are
related!
-......
-- -y- .
../ - ', '
-
. ~ e<
-.
{nucl ......1:>. ) __
""'0" '1
--------
14 CHAPTER TWO
U FP" . CC~
~BIBL!OTEC~
Mil
,
Fig. 2.5 - Transverse sect ion of a typical
9.2 microtubule flagelum(diameter
about 170nanometres)
A ]\fLXED BAG . IS
You might be interested in the activities of some of the members ofmcs<: two orders
including the fungi just named. The holocarpic Olpidium brassicae does not itself caus~
much damage to plunt roots, but is the vector of some n:lsty pl:lnt viru ses. The eucarpic
Sphellomycts puncUllus and Chylridillm Illgenoria paras itize polle n grains. The poly_
centric Cladoclrylrium is saprobic, growing on decaying aquatic vegetation. At least one
chytrid is II seriouS problem for fanners: Synchylr;um endobiolicum causes wandisease of
potato. This fungus produces dark brown, cauliflower like growths on the tubers. and a
catastrophic reduction in yield. Fortun ately. although the pathogen is widespread in
Europe, and has spread to Newfoundland, resistant varieties of potato help to keep the
disease und er control. Other microscopic chytrid~ parasitize algae, and can be so numerous as to Cause epidemics which sign ificantl y. if temporarily. reduce primary production
in lakes.
HypitlX~ytrium
IKpho.;/1)"1rid:alOS)
Fig. 2.6 Litrastructll"e of f~1 zoospores: er. endoplasrric retict.Un; F, fIagel.m; G, goIgi apparatus;
K, knetosome; L. ipid; M, milOChorrlion; m, microbody; rm. mastigooeme; mt, rricrotul::Ues; N,
rncleus; NC, nuclear cap (rbosomes); nFe - l1OI"I--ti.n:tioJlal centrioles; Nu, rudooIus; R, ~;
Ro. rootlet; Rv, nroposome; SO, striated cisco
-r.:i51S ~:::l y"~JJ.!)oV)
~G=
" ...,.J- rv\.Q
.J
16 C HAPTE R TWO
B: O/pldlum
c: cr.dochytrlum
,
,0
MoflOlWpMris
Fig. 2.7 Types of thali and reproductive strucllres among the Orytriciorrrytota. A:. eucarpic thaLs
of Spiullom)ces p uncta /us lSpil:eIorn).tales) in pine polen; B: noIocarpic thallus of Olp/dium
b raukae (Chytridiales) in cell of cabbage root; C: poIycenlrk tha~us of C/adochylrium
(Chytrio::iales); D: stages of oogamous reproductkln i1 Monobll'pharis polymorpha
~"".
A i'lUXED B.\G 17
No one knows why this fungus would suddenly begin killing frogs in places as
diverse as Au stralia and P:mama. The fu ngus may have been tra!l5poncd to these places
only recently - perhaps even on the boots or equipment of re~archers studying the
d isappearance of frogs. Or the fu ngus may have been present for a long time but frogs are
now succumbing because their immune systems have been impaired by recent environ
mental changes. One obvious change is increased ultraviolet light. which is known 10
damage immune sys tems of animals. Recently, chlorinated chemicals released by hu
mans have auacked the ozone layer in the upper atmosphere. allowing 10% more UfV
light 10 reach the Earth's surface. Industrial chemicals may also be danlaging the frogs'
immune systems. Retinoids are under suspicion because they eaw;e binh defects in many
animals, including frogs and humans. Accu tane. used to treat acne. is a retinoid known to
cause binh defects in humans. U you are interested in pursuing this topic, I M1ggest you
search for more infonnation on the internet: check out the archives of Rachel, an internet
environmental magazine.
Sexual reproduction in chytrids and Spizellomycetales needs to be reexamined: it
used to be assumed that any zoospore with twO flagella, and evely resting spore. resulted
from nuclear fusion. Now we know that some biflagellate zoospores originate by incomple te differentiation of cytoplasm during zoospore formation. and that many resting spores
are just thickwalled asexual sporangia which can survive dry periods.
Order Blas todadi alcs. Here the thallus has both broad true hyphae 3nd narrow
rhizoids. Allomyas orbuSCllllls, whose life cycle is illusll":lted in Fig. 2.8. exhibits what
we call alternation o r genera tions - a rotation between haploid and diploid thalli.
Haploid Ihalli produce gametes in $pedalized gamt tangia. while diploid thalli produce
flagellate zoospores and resting sporangia. In AI/omyce.l the gametes come in two sizes,'a
condition called a nisogamy. The general principle underlying anisogamy is division of
labour: the smaller. more mobile game te (which we can now think of as male) ac tively
see ks out the larger, less mobile (female) gamete, which has sacrificed some speed in order
to carry enough food to give the next generation a good stan. In ,l,/lomyces arbflsculus.
bo th kinds of gamete arc formed on the same hapl oid thallus. The colourless female
gametangia are Ixlme at the lips of hyphal branches. with the orange male gametangia
immediately below.
Zygotes develop into diploid thalli which bear two kinds of sporangia. thin-walled
and thi ck-walled. The nucl ei of thinw a!led sporangia undergo repeated mitosis and
produce mi lospores. which in this case 3fe diploid, uniflagellate zoospores that can establish new diploid thalli. The other kind of re productive structures. resistnnt sporangia.
shown on the right side of the diagmm, are thickwalled, brown. and can survi'>e for up to
30 years. E~'entually, some environmelllal stimulus trigge rs reduction division (m.:iosis)
in these sporangia. and the resultant haploiil meiospores are liber:.lted and develop inlo
sexualthaUi . Coelomomyces is another genus of the BlastOCladiales in which some spe
cies arc obligate parasi tes of mosquito I3rvae, and attempts are being made to use them in
biological control of Ihesc in~1S (see chapter 14).
Orde r Monoblcpharldalcs. MOll oblephar;$ polymorphu (Figs. 2.6. 2.7). which is
found on twigs of bin:h, ash, elm or oak submerged in slightly alh.!!"e freshwater pools,
is the first fungus we have met that has gone all the way to complete se.,u~1 differentiation
of gametes. The male gamete is ffi()tile (a speno). but the female (an egg) is not. This style
of sexuality is called oogllmy. Sperms fonn in gametangi~ called antheridia. while eggs
develop in oogonia, which are found on the same hypha just below the antheridia.
Spenos are ofte n released before the adjacent oogonium is ripe. This mny be a
mechanism for avoiding selffertilization. and ensuring oulbreeding (calle4 hetcrolhal
!ism in fungi). After the egg has been fenitized. the resulting zygote becomes amoeboid .
,
18 CHAPTER TWO
moves 01,11 01110 the top of the oogonium. arid encysts, developing a thick wall. Meiosis
probably occurs when this resting spore gemtinates. produci ng a genn tube (another
name for a first hypha).
Ahhoogh we Cbytridiomycota vary in so many things: in the morphology of their
assimilative phase, in their pauems of selluality. and in their adoption of parasitic o r
saprobic lifestyles; most of !hem have mOlile spores (zoospores or gametes), wjlh one
flagellum al the back (posteriorly uniflagellate - the cell swims li ke a spenn), and their
eel! waUs. like those of the other, more comple ... , eumycotan fungi, are largely made of
c hitin (8 polysaccharide very sintiJar to the stuff of which insect exoskeletons ate made).
They synthesize lysine by the same pathway (see chapter 9), and the more advanced
mem~rs
"
, ~~
(ml105l>Ores)
"'pIoid
=_H
(m..,spo",)
- ...
' ,-
,
"
I,
,,
. . _e
1>1."""",,
,
1IPO,~
...
I
D: AI~ugO -
1>0" Of SO ""
A MIXED BAG 21
they Stop swimming and develop a thick wall. later, they genninate again as secondary
zoospores which. if they are lucky. will find a new substrate and deve lop into new assimilative thalli. 'This process of encystment. followed by a repetition of germination, is a
strategy that gives the spores a second chance at finding food if they aren't so lucky when
first released.
Many Saprolegnia and Achlya species form compatible anthe ridia and oogonia on
the same mycelium. which means th at they are hom othalii c. S ince the assimi lative thallus is diploid, meiosis must take place inside the gametangia. E.lch globose oogonium
contains several eggs (Fig. 2. lOA). A nu mber of antheridia may grow toward and touch a
single oogonium. penetrating its wall at pre-formed thin spots and sendi ng in fertilization tubes which deliver the male nuc lei to the eggs. Fenilization is more reliable because
neither gamete is exposed to the vagaries of a free-swirruning existence. The whole
double life cyc le is illustrated in Fig. 2.11.
The zygotes develop thick, resistant walls and obviously function as survival spores
th nt can live through Such catastrophes as the drying up of the pond or stream. Homothnllie species ha ve lost the enhanced variation provided by o utbreeding, but they still
benefit from the thick-walled resting oospores produced by the sexual cycle.
Order Peronos porales, Many members of th is order arc ob ligately parasi tic on
higher plants. In some cases they cause epidemics that dev astate imponant crops. The
build-up of these epidemics is made possible: (t) by our need to grow dense stands of
single plant species (c rops), and (2) by aerial transmission o f me rungi, which have evolved
airbome mitosporangia (Fig. 2.9 B.C) Noto that these are often wrongly called conidia:
they are analogous but not homologous to those spores (whic h are disc ussed under the
Phy lum Dikaryomycota). Dogonia are also fonned, each contai ning a single egg (Fig.
2.10 B). Sexual reproduction is usually homOlhallic (the antheridium arises from the
same thallus as the oogonium).
"
We will examine
representatives of five ge nera from three Frunilies, Pythincene
(Pyllrium, Phy /()phrhora) . P e r o no s porllccu e (Pu() n()s p ora, Plasm()para), and
Alhuginaceae (Albugo).
Damping-orT disease of seedli ngs (Pylhirlm - Pythiaceae)
Th is is a soil-bome disease, so ilS causal agents. species o f Pythillm, have no need
for airbome sporangia, since they persist saprobically in most solts, and spread by zoospores
during weI condi tions. When thesc motile cells find young pl:llllS. they cause infections
22 CHAPTER TWO
which release toxins and also produce a pectinase enzyme which dissolves the middle
lamella that glues plant cells together. Seedlings of many plants collapse rapidly when
this disease strikes at the base of their delicate shoots. Damping-off is, unhappily, familiar
to gardeners who try to get a head stan on the growing sea.>on by germinating seeds
indoors. The disease can be controlled by using heat-sterilized soil, by dusting seeds with
Benomyl (a very safe fungicide - see chapter 13), or by watering seedlings with other
fungicides such as Zineb or No-damp. The complete life cycle of Pythium is illuscraled in
Fig. 2.12.
primary
germination
zoospore
sporangL3
penelration
"'
f~rtililalion
"0'
karyogamy
~ UFPE .CCB'
OBIS LlO T C
zooSj)Oms
veside
encysted
zoosporBS
spo rangium
soma1ic
Ilyptla
germinat,on
o
oogoniu m
oospore
.. /
6 ..'. i
.{,
.~
plasmogamy
!l
24 CHAPTER n
vo
The ravages of potato blight contributed to a million deaths, and drovc millions
more toemigrate from Ireland. Ten ye;:m; after the first epidemic, the population of Ireland
had crashed from 8 million to 4 million. Contemporary pictures from the umdon Jllus
Ira/cd Nc"'s convey some of the misery caused by the recurring epidemics. Ragged and
starving peasant girls gleaned desperately in the fields for anything edible, and whole
families Were forced to leave their homcs forever. Some died. Many sailed for North
America, but 187 doubly unfortunate souls were shipwrec ked and drowned off Forillon
National Park near the tip ofth<: Gas~ Peni nsula, Quebec - in sight of the promised land.
There is a fine web site on tbe potato famine at htt p:/hass un.vassar.edul-sUaylor/
FA.MINE with many contemporary illustrations.
Until 1976 this hetcrothallie pathogen (e)[cept in its homeland, Mexico) was ase)[ual,
representing only one of the two mating types. In that dry year. many crop failure s led to
importation of potatoes that carried the other matin g type with them. It has also been
suggested that new genotypes were spread in ~d tubers. in tomato tissues. and even in
tropical storm systems. However it came about, new sexual populations have certainly
supplanted the older lI.>;ClIual str.l.in. and have led to a resurgence of the disease. which
now costs the U.s. alone about 53 billion per year in auempts al control by spraying
fungicide~, by trying to breed resi stant varieties of potato, etc.
The airborne sporangia of the potato blight fUngus are c1e:lrly an efficient shon-range
dispers:almechanism, but humans were JUSt as dearly the long-range ve<:tors of this disease. POtato blight i~ still a threat, though it can be control1ed by: (I) spraying with
fungicide at times carefully chosen by plant pathologists (nowadays with the aid of
spechtl blight-forecasting computer progril.ms), (2) destroy ing infected foliage before
har.... est. and (3) planting disease-resistant seed potatoes.
[n addition to its most infamous spct:ies, the genus Phylopluhoru contains about 60
other species. Some of them are also. as one might suspect, serious plant pathogens.
PhytopirlllOf(I sojOl! plagues soybean farmcrs in North America. Phyt()phlllOf(I megakal)"ll
attacks cacao trees in West Africa. A hybrid between P. cambivom and P.frugariae has
killed about 10% oflhe aldcr trees (Alnus spp.) in Britain and is now spreading to France.
Holland. Sweden. Gennany and Austria. Ph)"tophlhom cimwmomi is destroying Jarmh
(Eucalyptus) forest and other natural ecosystems in western Australia, cQrk oak forcsts in
Spain, and is a serious problem for grower.>of avocados. pineapples and ericaceous shrubs
elsewhere in the lIorid. No wonder this genus pml'ides work for hundreds of plant p~
Ihologis\s and mycolog ists lliorldwide.
Downy m ilde w d ise~s (Plasmapara. Penmospora - Peronosporaceae)
Thc downy mil dews include blue mould of tobacco and downy mildcw of grape.
Since thcse diseases have historic or economic import3nce. I" lItel1 you something about
them. In this group the mitospol""Jngia are no longer unspeci:l.1ized hyphal tips. but are
borne on highly differentiated. branc hed. 3crial sporangiophores. The sporangi:t don ' t
just release WOSpores but are themselves set free and blown or splashed away. The sporan
gia of PerrmQspom genninate b)' producing a hypha, though those of mOSt o ther members
of the grou p still release motile zoospores.
Downy mi1d~w of Gra pe (Plasmoparu - Peronosporoceae)
P/llsmopara ,;ricola. an oomycete native to America, causes downy mildew of
gr<lpcs. It can be found attacking wild grapes evcry summer. But because it evoh'ed along
with its Nonh American host. a biological balance has been strock, and the wild llilis
species aren't seriously damaged. When this fungus wa~ accidentally introduced to Europe in the 1870s, it was a different story. The French grape vines (Vitis villifera) had no
re~istance tothe Ilt" palhogen. and were quickly devastated. FQttunately for the oenophiles
A MI](ED BAG 25
of the world, the: concoction of Bordeaux Mixture. olleofthe world's first practical fungicides, by a university professor(yes, we profs do occasi onall y have good ideas!) saved the
day. The rather strange story behind this invention is told in chapter 13.
The life cycle of Plo.smoparo is illustrated in Fig. 2.13. Look at this set of diagrams
carduUy, and decide at which stage you think it would be moSt vulnerable to chemical
att3i: k (Here's a clue - the answer begins with 7.. . ).
I
,
-.
F!8. 2. 13 Peronosporales: He cycle of Pla smapara vitico/a.
26 CHAPTER TWO
epidemic ensued. About 30% of the OnLlrio crop. wonh $100 million, wa. lost. BI",e
mould helped 10 put the Ontario tobacco industry 011 a slippery slope, and the decline in
tob3o acreage is still contin",ing, though it is now driven by changing societal auitudes
toward smoking. Pemnospom once again became a !iCrious problem (3 coffin nail ?) for
Omario tobacco growers in 1997.
WlUl e rus t disease or crucifers (Albugo - Albtiginaceae)
This disease allack..s cabbage, radish, etc. - all members of the family Brass icaceae
_ and is caused by Albugo candida, which produces extensive white blisters on leaves
and stems. These unique blisters contain innumerable unicellular mitosporangia devel
oping in chains f;om the tips of shon. tightl y packed sporangiophore; (Fig. 2.9 D). When
the host epidermis bursts, the sporangia are wind or rainsplash dispersed to other host
plants. where each CilIl germinate 10 release eight bit1.agellate zoospores. Oogonia de
velop later. inside the host stem Of leaves, and sexual reproduction is usually heterolhal
lie, or OIItbreeding.
'1
~
'.I
.1
t o.
in species diversity. We already know about 100,000 cumycotan fungi. and it is obvious
to those of uS who work with them that these arc just the tip o f the iceberg. We esti mate
that there nre ...."Cll over a million species wa iting to be found and described. Hu ndn:ds of
new fungal taxa an: described c"cry year. For eumplc, in 1990. Rafael Cast:ll'leda and I
described 14 new genera and 40 new species of microscopic moulds from dead leaves of
Cuban rninfurest plants. This wealth of species is a measure of fungal succe ss in eYolu~
tio nary terms, just as the existence of millions of species of insec ts tells us that they. too,
are winners (though their total biomass is f:tr less than that of th e fungi), Before we look at
the eumycotan fungi in detail. it is worth enquiring into the reasons for their success,
E:trlier. I introduced the idea that 1he numbl.-r. ki nd and arrJngemenl of motility
organelles (flagella) found in the chromiSlan (Oornycota. Hyphochytriomycota) and
some eumycolan fungi (Chytridiomycota) are very basic, highly co nserved featurcs. As a
corollary of Ihis, the absence of motile eelJ~ from the life cycle of most eumycotan fun gi
must al so be considered important. Th is seems to reflect a radical shift in evolutionary
dim:tion, It shows very clearly that most true fungi are h.::lsically te rrestrial (landlubbe~). and must have been so for a long time (evcn in geological tenns). l-'Iany more
ecological Riches and substrates arc available on land than in the water. and the challeng~s of sur"\"iv~1 and di spersal are very di fferent.
fun gi are beterot(op-.We which mean s that th ey dee;nd on energy-ricb carbolL.sompounds manufactured by othe r organisms. But this doesn' t ~m to have been a
serious disadvantage. Fu ngi have e\'ol\'ed e nzymes that can digest some extremely JOugh
substr.l\es. Chitin (arthropod exoskeletons). keflltU;J (mammalian and avian skin. hair,
hom and Feathers), cellulose (most plant debris - the largest reservoir of biological
materi al) and Ilgnin (a major constituent of wood) nou rish mJny fungi. thougb we must
.keep in mind that cellulose and lignin remain com pletely unavailable to almost all animals (except with the collaboratio n of microbial sy mbionlS). The unusual ability of somc
saprobic fungi to exploit cell ulose and lignin gives them almost exclusive access to the
massi\'e quant ities of plant debris produced every year, and may well make them .the
world's number onc r~yclers. Only man-made plastics arc. perhaps unfortunately. lm-
27
28 CHAPTER TH REE
mune to tIleir aLiacks, wroch means that we, not tile fungi, must take respon~ity for
recycling these substances.
l . ~~
The fungal colony (Fi g 3.1), with its strong. watefii1Qw. chitinous hyphae, its ri chl y
branched growth pallern. the repertoire of digestive enzymes it can secrete at its everincreasing number of growing tips, and the hydrostatic pressures it can bring to bear, is
ideally suited for actively penetrating. explori ng and exploiting solid substrates in a
manner that the bacteria, chief competitors of the fungi in the recycling business, cannot
match. (flow many hyphal ti ps do you think there are in Fig. 3. 1, an illustration of a very
young colony? 1761 294? 338? 502? - the answer is 388, and this numlxr will double
every hour or two.) If a fungus is growing in liquid culture or in a solid substrate and
produci ng a spherical colony. the rate of increase is many times faster, and the finil
number is astronomical.
The non-motile microscopic spores of eumycotan fungi. which come in a dazzling
array of forms (Fig. 3.2) to fit specific functions, are often produced very quicJil,y. (in a
matter of days or e ~'en hours after the initial colonization of the substrate). and in enormous numbers. They are dispersed by wind, by water, or by animal vectors, and they can
often survive long periods. sometimes even yean, of unfavourable conditions such as
freezing , starvation or desiccation (which means drying Out, and is speUed with one ' 5'
and two 'cs). Like bacteria. fungal spores are everywhere, especially in the soil (in astro-
Fig. 3. 1 Young colony of Phycomyces arisWlg from a mitospore.l'-Iote lhefarge number of hyphal
tips.
~~
~:>
1 '/
<t~
~
->I "9
\I~ ""
nomic n umbers) and in the air we breathe (sometimes up 1010.000 in a cubic metre). If
you are curious about the ways in which we describe and name these spores, zip off 10
chapter 4 and find out.
Fungi have learned 10 cope with environmental extremes. They can grow at temperatures as low as _5Celsius and as high as 6OCelsius. They include the most xerotolerant
organisms known: some moulds will grow at the amazingly low wate r activity of 0.65
(most plants wilt permanently at a water activity of 0.98). Other IT\Qulds grow in oxygen
eoncentrations as low as 0.2% (air contains 20% oxygen). Cenain fungi can grow under
extremely add cond itions (pH I): others can tolerate alkalinity up to pH 9. These topics
are covered in more detail in chapters 9 (Fungal Physiology) and 20 (Food Spoilage by
Fungi and its Prevention).
- t 'f
As I have already noted. the s3probic funal are recydcq parex.cellenc.e. but they are
; !) also among the world's greatest opportunists, and don't restrict their attentions to natIJ-
1'-Ii i
,J;.
~ ~
fabric. paper and paint, or almost any other kind of organic matter. Some of their metabol ~( lites (m ycolo:\:i ns) are extremely dangerous - even carcinogenic - if they Contaminate
.'~ ~ ~ ~ (ch apter 2 1 - M ycotoxins in Food and Feed). And parasitic fungi cauS!: the majority
%: '
-
<".
raUy occurring dead wood and leaves. Wherever there is a Imce of moisture, their omnipresent spores will germinate. and the hyphae arising from them will allac!; food and
~i~ '"
i
~ t~ c-
00 .
))
! \. r:
i:;
X'YJ \
A,
.I
r--
'"-'" "L
~
V!J
r,
~I!-\
30 CHAPTE R THREE
of serious plant discases (chapter 12 - Fungal Plant Pathology in Agricultu re and forestry), as well as some of animals and people (chapter 23 - Medical Mycology).
Fortun:Ue!y. there is a brighter side to fungal intervention in human affairs: we have
hamessed the biochemical virtuosity of the saprobic fungi in the production of beer. wine,
bread. some gourmet cheeses. my sauce, some antibiotics and immunosuppressants, organic acids, and many other useful chemicals. Fungi are even being used to convert plant
waste into high-protein animal feed. We ourselves eat a number of the large. spore-producing stnJctures developed by fungi: mushrooms, chamerelles, morel~ and tnJff1es are
aJl familiar to devotees of French cuisine. who prize them for their unique flavours. Some
of the parasitiC fonus are now being recruited to attack insects, weeds and other fungi
which threaten our welfare (chapter 14). And fungi in intimate, obligatory association
with the rooLS of almost all higher plants (forming mycorrhizasl. silently, invisibly and
influenti3.l1y perpetuate one of the world's oldest and mOSt successful fonns of mutua lis tic
symbiosis (chapter 17).
AhhOUghi,'h~'~~~i~~~
,,;h.
Zygospor,lIIgia. The name of the class is derived from the way in which its members
reproduce sc l>ually by the physicaJ. blending - fusion or ronjugation - of morphologically
similar gametangia to fonn ijl'gos'ji'6ran-gmiil(the teleomorphic phase). 'Zygos' is Greek
for a yoke orjoining. The gametangia arise from hyphae ora single mycelium in homoth allie SIXcicS. or from diff~rent bm sexually compatible mycelia in heterothalli c species.
Zygosporangin usually d~velop thic k walls, ~nd ~ct as r~sting spores.
The four diagrams in Fig. 3.3 show how a zygosporangium develops. When compatible mycelia of Phycom)'cts blllktsluallus meet, inqjvidual hyphae establish intima~
S0(l!(lC t. deydopjpg fing er- ljke o!!lSWWlhs and seeming to grapple wilh One anotbs;r...o.
This lets them el>change chemical signals ",hich establish that they are iltQeed sexually
compatible. Then Ihe two hyphae grow apart again. only to loop back. swelling as they
approach each other. and finally m~ting head-on. They have become gametangia. w~ich
fu se when their tips tooch. Note that there isn'l any SCl>ual differentiation in size or shape
hen:: since we can't call them male and female, we simply label the mycelia '+' and '-'
After the walls bern'ccn the twO gametangial tips have broken down and their multinucleate contems have mixed, the miJ;.(ure is quickly isolated by two septa, one at each side.
and the p~ircd-off nuclei fuse. The structure is now called a zygosporangium, and it develops
a thick and often ornamented wall. even while still supported on either side by the former
gametangia. which are now calle-d suspensors. Although the two slI.'lpeI1llors are now just
empty append:lgc.", they make it easy to recognize a zygosporangium when you sec one .
..
.." ';
EU1\-IYCOTA; ZYGOMYCOTA
,\"'-1)
DIKARYO!\WCOTA 31
Anamorphs. You won'toften see zygosporangia in field collections, though I sometimes find a homothallic species of Syzygires producing them profusely as it parasitizcs
ovcr-mature wild mushrooms. But asexual or anamorphic phascs of zygomycetes are
easy to find on mouldy bread or peaches, or on horsc dung. A number of examples are
illumated in Figs. 3.4 and 3.6.
Collect some fresh horse dUng. keep it in a damp chamber, and look at it through a
dissecting microscope, or even a hand lens, every day. You should be able to follow a
sequence of specialized coprophilous fungi - and the first to develop will probably be
the spectacular anamorph of Pi/abO/liS (Fig. 3.6), which is discussed below and in chaptcr
11. The non-motile ase:>:ual mitospores llre usually fonned inside mitosporangia borne at
the tips of specialized sporangiophores. Zygomycetous cel! walls are mainly of chitio and
the nudei in their vegetative hyphae are haploid. Now for a taxonomic survey of the
phylum and its two classcs.
anMto mosis
32 Cl:L\PTER THREE
r
r
rr
, !
B:
Cl'="",
woraogO>lH
lJ
.~~~
EUl\WCOTA: ZYGQi\.WCQTA
.1.:'<.1)
D1KARYQMYCQT A 33
unp ublishcd paper which places thc Glom al es in a new phylum ten tat ively called
Symbiomycetes. We shall sec ...
I) Orde r M ucorales. 13 families, 56 gcnera, 300 s~ie5. This order includes all
the common saprobic zygomycetes. Here belong the ubiquitous bread mould. Rhizopus
sr%nijer (fig. 3.4 A). and theequally common genus Mucor. Each globose mitosporangium
of these fungi contains hundreds of nonmotile. asexual spores, and these sporangia are
produced at the ends of tal! . stout, simple or branched hyphae called spornn 2io phores.
The trademark o f the family ~Iuooraceae is a swollen eJl:tension of the sporangiophore called a colum ell a (Fi g. 3.4 A and D). wh ich protrudes into the sporangium, and
often persists afte r the delicate outer skin or pcridium of the sporangium has disappeared
and the spomngiospores have been dispened Other families often ha ve fewer spores per
sporangium, and their sporangia have no col umell~.
it acc urately tOward any lighl roun.:e. tn a word. it is phototropic. The generation of
osmotically aClive compounds inside this gi1ml cell causes pressure in the sporangiophore and the subsporangial vesicle 10 build up until it is over 100 pounds per square inch
(7 kilograms per square centimetre). This eventually causes the vesicle to ellplode. hurling the black sporangium away to a distance of up 10 2 metres. directly toward the li~t.
The mucilaginous contents of the subsporangial vesicle go with the sporangium, and
glue it to whatever it lands on. Can you explain why P i/ooo/ros needs such a specialized
mechanism for spore dispersal: such a powerful r;annon. su r;arefully aimed11I you can't
fi gure it 01,11. you r;an find the answer in r;hnpter 11.
Note that the originality of Piioho/u$ eXtends only to the behaviour of its anamorph
- th e teleomorph (the zygosporangiurn. shown in Fig. 3.6 D) is fairly conventional.
2) O rd er Entomophthorales. As the name implies. these fungi often attack insects.
EmomophthoTa muscae infects, and eventually kills, houseflies. Dying flies. their bodies
riddl,d by 'h'
--.".. .".".. 0
O::J 0'
& 00
0 0
,;x>".r~Ofo""
1-,
~~
.YOO>tPO'ongou.:.a
I
~--::,
~
,r. /
r~
.,.P
{ 'ow.,
Fig. 3.6 AD: PilvbQ/U5 (Mucora les). A: habit of sporangiophores (anamorphJ on dung: be~ded
.
appearance is caused by condensation droplets; B,(: action of subsporangial vesicle and retlflal area III
phototropism; 0: zygosporangium (teleomorph). E,F: Entomophthora (Entomophtoo.:a.les). E: .
section through the Jnamorph sporlbting on a fly; F: zygosporangium (teleomorph) arising by fuslOrl
of hyphal bodies.
UF PECCB
36 CHAPTER THREE
That'S complex enough, but it looks simple beside Spirodactylon (Fig. 3.4 F). This,
surely the most el~borate of all zygomycetous anamo'llhs, produces a tall, branched
sporangiophore that is repeatedly tlu:own into tight coils. Within these coils arise the
sporocladia, which bear pseudopitiaiides, and these in tum bear one spored sporangioks.
It is hard to imagine why this strange configurotion might have evoh'ed, until one
learns th:u the fungus grows on mouse and ral dung. Coprophilous fungi have various
highly evolved str.l.tegies for getting back inside the gut of the animals that produce their
prefcfTed substrate. This isn't tOO difficult for genera like Pi/abo/us, that grow on herbi
vore dung, since all they have to do is get their spores onto the animal 's food, which is all
around. Bul rats and mice are not herbivores, and it is essentially impossible for the
fungus tu ensure that its spores will be present on their food. The only alternative (as 1 see
il) is to anach spores to the animal ilseIf, in tIN: hope that they will be ingested during
grooming activities. Rats and mice are creatures of habit. using wel1 -trodden paths each
day. Along tbese trails they deposit dung. and there, later, the coils of Spirodactylon
become entangled in their hair. Only Ihe zygosporangia of tbe KKkxellales convince us
that these strange fungi are ind~d zygomycetes.
4) O rd er G lomales. These soil-inhabiting fungi were placed in the Zygomycota
only tenwtively, since almost none of lhem fonn zygosporangia. Nevenheless, they are
extremely important, because their hyphae enter the li ving rOOt cells of perhaps 90% of
all higher plants and establish with them obligate mutualistic symbioses called arb~ular
myc or rhbas (Ai\I) or end omyco rrh h:as. These are illustrated and discussed in detail in
chapter 17.
AM fungi won't grow in axenic culture: Ihey must be assochllcd wilh a plant root.
Their gene rally very large and thick-walled resting spores are common in most soils, and
are stimulated to genninate by the prollimity of plant roolS (almost any plant will do,
b;:cause these fungi have such wid.:: host-ranges).
Their usually nOn-septate hyphae spread through [he soil and enter living roots,
'where they dewlop st ructures tbat are diagnostic of the order: intrac.::llular, finely
branched_ tree-li ke arbuscules (Fig. 17_3) which are the interface across which the fungus
ellchanges mineral nutrients, especially phosphorus. for photosynthales (sugllr.!. etc.)
provided by the plant. Many of the Glomales produce both arbuscules and lipid-filled
structures called l'~sicles or intra ma tri cal spores inside plant rootS.
The soil-inhabiting myc.::lium is very efficient at mobilising insoluble phosphorus
and lrans localing (moving) it to the plant. Since phosphorus is often the limiting nutrient
for plant growth, A.t\1 fungi help planls to thrive in poor soils. These fungi are therefore
vital in many natural habitats. and of great potential value in agriculture_ Again, for
details consult chapter 17.
Canada. [CD-ROI\.IJ
Zycha. H.. R. Siepm:mn and G. Linnemann (1969) i\iueoralt'5. Eine Bescltreih ung aller
Gatlungc n undArten dieser PiI7.gru ppe. Cmmer. Lehre.
UFPE.CCB
"lI:iI> BIBLIOTECA
Kingdom EUMYCOTA
Phylum 3: DIKARYOMYCOTA,
Qfr
Subphylum 1 - ASCOMYCOTINA: , ~,..Q~,~
the Ascomycetes
q.Ji" . S"
Introduction
~
38
Zygomycetes, the subjects of chapter 3. are terrestrial fungi: there's 00 doubt about
that. But they thrive and sporulate only in damp places where the atmosphere is more or
less satural~d with moisture:. For eumple, Rhi~opu!i slO/onifu will colonize the moist
interior of a loaf of bread, but won't produce its characteristic sporangiophores and
mitosporangi a on the outside of the bread unless the surrounding atmosphere is humid. If
we pel'$uade the fungus 10 sporulate by keeping the loaf in a damp chamber (a plastic bag
cont3ining a few drops of wale r will do) and then take it out of the bag. the sporangiaphares will quickly collapse.
Hyphae of mOSl zygomycetes are wide, thin-walled, and coenocytie - continuous
tubes with no cross-walls. Hyphne of phylum Dikaryomycota (Ascomycetes plus Basidi
omycetes) are nnrrower. Hyphae average nbout S microns in width. but in aggregate they
aTe ,"cry long (sometimes kil ometres per gram of soil).lhtY_lU"e also.sep ta.te -they' have
crosswalls called septa at regular intervals. These min inture bulkheads give the hyphae
Some physical rigidi ty. andlimit loss of cytoplasm if the hyphal wall is ruptured. As a
result. we find that ctikaryomycota can grow in a wide range of conditions: for example,
they can often spread and fruit in drier situations than zygomycetes could tolerate. Some
dikaryomycolan anamorphs (especially coelomytttes) grow in dead leaVe!; and stems of
desert plants. and some moulds are th e most drought tolerant of all organisms. able to
grow at water acti vities below 0.70 (for example, on jams, salt fish and Other substrates of
extremely bigh osmotic pressure - see chapter 20).
While many zygomycetes can assimilate only 'accessible' substrates like sugars
and SlaKh, ascomycetes can oflen exploit cellulose. and many basidiomycetes can digest
both cellulose and lignin, carbon sources th at are available to rem arkably fe w other
organisms. Though fungi cannot fix atmospheric nitrogen (this talen! seems 10 be restricted to the prokaryotes), dikaryomycotan fungi can use many different forms of combined nitrogen: some ascomycetes eve n specialize in metabolizing the protein keratin.
A::UMVCOTA: DlKARVO"lYCOTA:ASCO~IYC011NA 39
which is the main component of hair and skin. In case you were wondering if membe~ of
this groop constitute a health hazard - they do.
Some other orde~ of ascomycetes are obligate parasites of plants. Remember the
dery)
'dow ny mildews' caused by oomycetes? There are also plant di seases called
mildews' that we caused by ascomycetes. The similariry o f tellllinqlogy is unfortunate,
but try to remember the difference, because although the groups of fungi involved are
both obligately biotrophic, the diseases are different in many important ways. such as
host ranges and methods of control. This is just one example of how Wonomy has
practical implications (see chapter 12).
Thousands of basidiomycetes, and a quite a fe w ascomycetes, establish intimate
mutualistic symbioses (mycorrhizas) with the roots of treeS, especially conifers (see chap. ter 17). Nearly 18,000 ascomycetes, and a few basidiomycetes, have dome sticated algae.
thus becoming lichens, which can live in some of the world' s harshest climates and
colonize the barest and mOSI inhospitable substrates (see chapter 7). Some dikatyomycotan
fungi have even re-entcred the water and, lacking motile cells, have evolved Olher mechanisms, such as long appendages, to aid spore dispersal. Dikaryolllycotan fungi range from
unspecialized, almost omnivorous saprobcs, 10 fungi so specialized and ecologically
demanding that they are found only on one particular Icg of one spec ies of insccL Some
dikaryomycotan fruit bodies are microscopic (as in many ascomycetes), but often (especially among the basidiomycetes) they are large and complex, and most of the common
names appl ied to fungi rerer to the visible Ic:leomorphs o f basidiomycetes. and in a few
cases, ascomycetes. You may already be acquai nted with some of these; I will introduce
you to many more in the pages ahead.
_ ',A(,.e I"'\~_
:w... .
51 EO ['\..
;9'~t.,.O . -
'.
i
Fig. 4.1 Diagnostic chart of f...-.gal pl-tfIa, and the subphyla and classes of Dbryomycota.
40 CHAPTER FOU R
Subphylum ASCOMYCOTINA
Characteristics of Teleomorphs..
If ascomycetes and basidiomycetes share all these trungs, how do they differ? Actually, in muny ways, and with experience it's usually casy to Icllibeirsexual fructifications
ap3rt with thr n:lked eye, But their microscopic, uni cellular mriosporangia are most
diagnostic of all (compare the subphylum diagram~ in Fig, 4.1 and Fig, 5.2 on p. 80).
The meiosporangia of a$Com),cctes are asci (singul:u, ascus), They are cylindrical
or s~c -l ike and ~t maturity u~uall: contain eight haploid spores (ascospo~) which are
e.' pelled into 'he air through the top of the :lSCU.".
The meiosporangia of basidiomycetes are basidia (singular, basidium): they usually have four liny projections call~ ste rigma ta , each bearing a haploid spore (basid
lospore) which i~ shot ~way indi\'idu~ lIy at maturity.
The formation of asci or basidia marks th ~ cnd of the dikaryophase: the paired
nuclti h:lve fused and the resulting zygotc has undergone meiosis (a nd a mitosis in
ns,'omycetrs) to produce eight haplnid a~cospores or four haploid basidiospores, Compare the two sets of diagram s in Figure 5.2, and n()lC how similar the developmental
proces..~es are until the final Mages,
I,
enon. but during the d ikaryophase an effectively diploid mycelium is growing within ..
and drawing nouri shment from. the haploid ascoma tissue. This phenomenon has intcre~t.
ing paI:llleJs in the red algae, though molecular evidence doesn' t support II d ose relation
ship between the two groups (both lack motile gametes and app!':ar to have simply hit
upon the same solution to the probkm jX>SCd by the rarity of sexual enCQUnters).
Aseospores are not motile, in the sense of sclf-prop!':lling, but most ascomycetes
nevertheless send their as~ospores off with a burs! of kinetic energy. The ascus is a tiny
spore-gun, which worb by build ing up internal pre ss ure, th en rel easing it through the tip.
Thejob of most asci is to get !Mir ascospores into the turbu lent airflow aoove the ascoma.
Matu re asci of the dung-inhabitingAscobollls (Fig. 4 .2) project above the hymenium and
point toward the light before discharging their spores. In this way they ensure that the
spores will not run into any obstacles on their upward flight (see chapter 8).
_""'"
QO'''''O"U' ;
FI. 4.2 Teleomorphic cycle of anapothcd.llascomycete, AscoboluJ (Pt-zizalesJ (see text for h.
explanation).
42 CHA PT E R FOUR
.,
, 0,(;(;11
J.?'~l3ll()i~~
. .
~i.
_
.
..-
,_asci
--- -
--
,'I f _
..
_""
, If _ _
EUMYCOTA: DIKARYOMYCOTA:ASCQ)'IYCQTh'iA 43
(4) Clclstothedal As.::omata lade an opening entirely. This usually indicates that
the asci are spherical, u in!hesc iIIustratioos. and no longer shOO! their spores: the fungus
has evolved another dispersal sttategy. That may have happened because the fungus fruilS
in a confined space (for ex.ample, under bark, or below the surface of the ground) where
airbome dispersal cannot operate. We often find that the s~ of such fungi aredisperscd
by animals.
Four'Kinds of Ascus
Before we go on to explore the many orders of ascomycetes, we mUSt lake II. closer
look at the ascus ilSelf. All asci are nOI the same. There are four flavours (Fig. 4.3) :
(1) UnltunicateOpe rcuJate Asci which have II. single wall with a builtin lid or
operculum at the tip - at maturity this pops open so that the spores can be ejected.
Unitunicate-operculate asci are found only in apothecial ascomata.
(2) Unitunicate-Inopen.: ula te Asci which have 110 operculum. but have a special
elastic ring mechanism built inlO their tip. This is a pre-set pressure release valve. or sphincter. and the ring eventually stretches momentarily, or turns inside out, to let the spores shoot
through. Such inopereu late asci are found in perithecial and some apothedal ascom.ata.
(3) Proto tunicateAsci which have no active spore-shooting mechanism. These asci
are usually more or less spherical, and are found in cleiSlOthecial (occasionally peritheeia]). and by pogeous (underground) ascomata. Sometimes the waU of this kind of ascus
dissolves at marurity and releases the ascospores, which can then ooze, rather than be
shot, out of the ascoma; or they may wait inside until it decays or is ruptured. These asci
are often called prototunicate. Yet perhaps because they are found in sever.ll otherwise
rather diffe rent ordert. il seems likely th.1t they represent a Sf("oruiary condition. and have
evolved seveml times from unitunicate a<;ci (as they clearly did in the trumes - Tuberaccae
in thi s chapter).
~
(4) BilunicateAsci which have adouble wall. A thin. inextensible outer wall covert
a thick, elastic inner willI. At maturity the thin outer wall splits. and the thick inner wall
absorbs water and expands upward. carrying the ascospores with it This ' Jac k-in-a-box'
design allows the ascus 10 stretch up into the neck of the ascoma 10 expel ilS spores. The
bitunicate ascus is so different from the unituni cate ascus that we assume they diverged a
long time ago.
In many unitunicate ascomycetes. the peritheeial ascoma develops only after the
,cxual stimulus, so that the asci can grow into an actively enlarging cavity. In man y
bitunicate ascomycetes, ferti lization doesn't happen until after a solid primordium or
stroma has developed. so room has to be made for the asci by dissolving away exisling
tissue. In some cases the asci themselves do the job, but in others it is carried out by
special sterile hyphae (pseudoparnphysc.s) iIowing down from the upper layer of the
stroma; the asc i then grow up between them. Remember th at pseudol:hecial ascomata
always produce bitunicnte asci.
Subphylum ASCOMYCOTINA
Many Kinds of Anamorph
Here is a mantra to begin with - say it until you know it:
Holomorph
=
Anamorph
+
Telw morph
(the whole fungus) = (asexual reproduction) + (sexu al reproduction)
In any modem consideration of the Ascomycetes. we cannot ignore their asexual
reproductive phases, many of which are called moulds:You already know that zygomycetes
have diverse asexual phases. So you won't be surprised to discover that many asca-
44 CHAYrER FOUR
mycetcs have co mparable asexual (anamorphic) phases during which they rcproduce
rapidly, and often relatively cheaply, by means of mitospores called conidia.
The asexual ly reproducing phase of Ihe ascomycete life cycle wa.~ more Of" less ignored for many yean in favour of teleomorph srudies. But when we consider tiutt the anamoIph
is an important (andsome~ Ihe only) phenotypic expression of many ascomycete genotypes, we realize that it has much to tell us. Besides, one can get DNA and RNA from
anamorphs just as ea~ily a.~ from teleomo rphs, so we are beginning to understand the relationships of an.:unorphs bener. even in many ca.<.es wbere flO teleomorph is known.
Though they play essent ially the same role in the life cycle, the anamorphs of
ascomycetes differ from those of zygomycetes in two very important respects:
(A) While zygomycete mitospores commonly originate by rrce-cell ronna tion inside a sporangi um. many spores cleaving from a single mass of cytoplasm, the mitospores
(conidia ) of aswmycetes are basically modified bits of hyphae, either budded out as a
new structure, or converted from a whole existing cdl.
(B) In zygomycetes, anamorph a[ld leleomorph often occur together (especially in
homOtllaltic species) and always share the same binomial. In ascomycetes. anamorph and
teleomorph often develop at different times, and on different SUbstrates. Each phase has
often been collected in Iota! ignorance of the e:ljsten ce of the other, and because of this.
the International Code of Botanical Nomenclature maintains that it is legal 10 give them
separate binomials - a useful option. but (me gi ving rise to a great deal of confusion in
some studenl.'i' minds (How can one organism have two names?)
Several thousand ~namorph-telcomorph connections have now been established in
the ascomycetes. YOli can now find them at this web site:
h t t p:JI"'.....'" .biology. ua l berta.calj bn:usl 01 ana Ideo/alia td. h t m1
These represent on ly a smail proportion of the tO(;l1 number of Ia.~a, either of anamorphs
or reicomorphs (we know ubout 30,OOOof each). Be>:ause annmorphs so often occur alone.
il is still nOilllalllnd ~cccpted practice to use separate binomials for them, as you will see.
N~vertheles s. ! find it complctely unacceptable to talk about con id ial funl:!i. as many
ot her le~t~ do, as if Ihey constituted a sepa!1lte major hi gh -level tax on called th e
Deutcromycotina.' Th is ignores bOlh the evidence that thcy are all <:xpn:ssions of
dikaryomycotan genomes. and th e th ousands of contlec!ions that have already been
established with telcomorphs (and the number grows every )'eat).
Of abo ut 30,000 known llscomycetcs. 5,000 hal'e so far been connected to tM-ir
anamorphs. \\~hat about the many thou sa nds of conidial (anamorphic) fungi that arc still
'orphans'? I lhin k there is good reason In belie\'e that many of them have given up sex
altogethe r. and become 'anomorphie-holomorphs: though they seem to have retained
some genetic flexibility by: (a) having more than one kind of nucleus in the ir mycelia
(heterokaryosis) as iI re su lt of occasional hyphal fusions (anasto moses): (b) S()rn<:timc.~
undergoing a comple:\: pa rasexual process involving rare somatic dip!oidization. mit otic
crossing-over. and finally a return to the haploid condi tion (this process is more fully
explai ned in chap ter 10).
It turns out that the conidial fungi are a mixed bag. Although most of them arc (or
were) part of as.com)cete life cycles. others arc (Of were) connectcd with basidiomy~tes .
Despite this mixed ancestry. we have h~d to sct up a single classification for all of them.
because it is often impossible to tell, just by looking at them. in whic h subph>'l um the
co nnecti on lies. Unfonunately. our ~cheme for cla.o;sifying the anamorphs has so fur been
able to make lillIe refercnce to teleomo rph s, for severa! reasons: (I) tdeomorph s are
known for only 10- 15% of anamorphic species; (2) members of ....hat seems to be a single
anamorph genus lOa)' hnve teleomorphs in lIlany different holomorph genera (even from
different orders). This must be due to convergent emlution among ana morphs: (3)
EUMYCOTA: OIJ'ARYO;\lYCOTA:ASCOMYCOTINA 45
anamorphs belonging to several different anamorph genera can have sexual phases in a
single holomorph genus. This must be due to radi3tive evolution among anamorphs. So
our attempts to classify anamorphs have concentrated on: (A) their mitospores (collidia) ..
(B) the diverse stroctures (conid iogenous cells. conidiophores and conidiomnta) which
bear them, (C) the ways in which the mitospores develop (conldiogencsis). and, more
rceeotly (D) molecular te<:hniques, which are now helping us to elucidate their relation
ships.
The division of anllmorphs inlo two large groups is informal, is based on charncter
(3 ) above, and is really JUSt for convenience. The easiest decision to make is usually
whether a conidial fungus is a hyphomycete or a coelomycete. You can recognize a
hyphomyccte because its conidiophores can be single or aggregated in various ways, but
are n~ver enclosed within a covered conidioma. Coelomycetes form their conidia in
initially enc losed conidiomala, which usually devclop just beneath Ih~ surface of their
plant substrate. I am not going to discuss coelomycetes in detail (though there are thO\.l sands of them, and they cause many important diseases of crop planl~) . but I must mention
a few basic facts.
Conidium morphology
Presence or absence of pigment is important. as ru-e shape and septatiOfl. "There are seven
shape and septation C<ltegQries. (Fig. 4.4) (A) commonest of all are singl~~elled amcrospores.
(B) the addition of one crosswnllmakes tlltm didymosporcs. (C) conidia curved through
more than a half-cirele. or coiled in two or three dimensions. are called hdicospores.
(0) those with several conspicuous. radi~!ing ,um.<; orother projections are c311ed sUlurospores.
(E) septa running two ways. like the me:shcs of a 1b.'I, or like the mortnJ layers of a brick wall ..
identify diclyospores. (F) twO or more transverse septa. arranged like the rungs of a ladder.
46 CHAYfER FOUR
characterize phragmospores. (G) Finally, those which arc Ioog and thin (more 1han15 times
as long as !hey are wide), are called scoleeo:spo res (which means worm-like').
.-,
.."..
......
p/IrI.gmo-
simple
!.l
UFPECCB'
GSIBLIOTECA
i/
c : schizolytic .tces.<iGn
48 CIIAPTER FOUR
Gon.W,olf yum
~
'
"
'
ir1
~-r,
Bolrylls
.49
conidiogenous cells, and innumerable conidia accumulate in a slimy head. These spores
are insect-dispersed. Bo.sifimbria lteleolTJOrph unknown). which is common on horse dung,
has simpl e conidiophores that elongate sympodia1\y during conidiation. (Fig 4.6)
.
Type IV: blaslic-annellidic or blaSlic-percurrenl conidioge nesls
In the SpiWcata anamorph of Venn/ria il1(leqllalis, the apple scab fungus . e~e h
~ceding coni diu m leaves a ring-Like scar, an anncllation. around the c:onidiogenous cell.
",hicb then grows on through the scar ('pereurrentl}") to produce the next conidium.
Conidiogenous cells that have produced seven spores bear seven annular scars - hence
the name anndlidic. Scoplilariopsis(Fig_ 4.6. 4.7 A) has s.cvcraJ annellidic conidiogellOus
cells on each branched conidiopho~ . upl(lgraphium conidiophores may h~ve many
such cells at their a~.\ (Fig. 4.6).
II h3s =ntly been confirmed that some individual annmorpbscan be both annellidic
and sympodiaL J'll give you tWo examples of how this knowledge may cbange our classification. When it was thought, not many years ngo. thatcon id ioge ne sis in tbe synnemam l
anamorphs of Ophiosta11W species was either exclusi\<ely sympodial o r e xclusively
percurrent. they were segregated into two anamorph genera (PesQlUm and Grophill1>!).
Now it has be<::n shown tbat both kinds of conidiogenesis can occ:ur on the same conidiopho re, they are being united a,gain in the older genus, Grapltiutrl. In exactLy the same way,
some complex mononematour; anamorphs of Op/lw.flOml! species were segrcgnted into
the 'exclusively sympodial' \ lmicic/tuiid/a (which I monographcd) and the 'exclusively
~rcurre nt' uprogmphium, but are now united under the olde r name, LeplOgraphilllll.
Type V: blastic-phialidic co nidi ogenesis
Many common moulds produce conidia in rapid succession from the open en d of
spedul conidiogenOIlS cells called phiulides. Common genera such as PellicilliwlI, As
persill1ll3nd eha/am arc 311 phialidic (Fi g. 4.6). Many plant pathogenic hyphomycetes.
such as F u),/Irill'" ami VerlicilliUm, both causing serious wilt diseases of crop plants. also
produce phialides _ Pmicil/;wlI and Aspersilllls are dry- spored. Fusarium. Verticil/ium
and Stadl)'bolrys ha 'c slimy spores. Phialidic ontogeny is basically rluher similar to type
IV - percurrenl.
Most phialides don't change in length while producing many successive conidia,
though mony wall layers build up inside the open end of the cell (Fig. 4.7 B), This
accumolation of wall layers may ",,-elllually plug th<:: opening. ;Ind in phi31ides to whicb
this happens there is a tendency to produce sy mpodial extensions tbat develop new fertile
apertures . Such phialides are calkd polyphlalides sine.: th ey have mo re [b~n one
co nidiogenous locus.
Type VI: blastic-retrogressive c onidiogenesis
In Basipt lOspora (<I the rmotolerant fUl1gu~ use d in Indonesia in the preparation of a
led food colou ri ng ), a conidium forms at the tip of the rel atively undifferentiated
conid iogenous hypha and is delimited by a cross-wall; then a short zone of the hypha just
\)clow tne conidium balloons out to produc.: the second conid ium. Aft~ r this bas bee n
delimit~d by a septum, the next segm~lIt of the hypha plasticil.es and blows oul, a nd 50
on. As the ch"in of con idia elong ates. the conidiogcnous hypha becomes ,honer. Si milar
development occurs in Tricholh<,cium and C/(li/ooou),lIm, but this is an unusliol kind of
con idi ogenesis. (Fig. 4.7 C)
Type VII: basiluxic conidioge nesis
In the Oidium anamorph of Erpipht gmmittis . \\ hit ish chaills of conidio (the ' po wdery mildew') COyer the host le3ws. Each chain consists of a graded series of gradually
50 CHAPTER FOUR
maturing conidia, the oldest at the tip, the youngest barely differentiated from the hyphal
cell just below it. New material is added at the base of the chain in a fonn of intercalary
growth, arising from a sometimes swollen mother cell which appears to be a highly modifiedphialide. (Fig 4.19)
"
i)
_IH i_
8: blastic-pI"oial idic
1
1
2
2
3
\
C : llIa>tic-r.'IDg,essjve
,
,
EUMYCOTA: DlKARym,fYCOTA:ASCOMYCOTINA 51
tree-li ke eonidiophore disaI1ieulate into ronidia, ul timately leaving only the denuded
' trunk: (the stipe). Many basidiomycetes also produee thallic-arthric eonidia.
A: OIdIodmdron - !halicanhrio;
'LI ~:..!
! ' ~'.J!"
'-,
.~.':I'.
t.... t .' .
. .!
"I'. , .
:.... ~ ~ ,14
)--
...~, . " ! l ~ .~
'., , .,1 ~:';
- r- '
-~
1'-
<.J-J'':-.'
'. .
..
f--
.. I !'...
~1
':
:-:
.. , :. 1,;
.
.. .
....
. i
,! ;;.... .
i-
,IiL
o
-8
n
52 CHAPTE R FO UR
mycoto~in .
zearalcnOlle. which is a steroid, and causes ccs trogeni c synd rome - vaginal and recta!
prolap,~c - in young fem ale pigs. Many other rn~cotoxin s ha ve been di scove red in rece nt
.years, They are potential thre3ts to human and animal health of wh ich W~ are only now
becoming fully aware, and they h3\'C neccssi t::ued the development of new technique s for
toxi n monitoring and new programs for plant protection and food storage,
54 CHAPTER FOUR
A CfI!tnOnilU/I
(I) Order Taphrinales: 9 genera, 120 species. This is an ou tlying group which
causes seriou.~ diseases of some plants in the Rosaceae (e.g. Taphrjrw defonnans causing
peach leaf curl) and the Amenlifene (e.g. Taph rina populina on poplar). Fig. 4.9 shows
T!Jphrina defonnan5 attacking :I peach leaf. Le aves become thid:ened, distorted and
often yellow or midish incolour.1ltis fungus has four unique or unusual fearures: {A)"The
assimilative mycelium is dilcary(){ie ~ this would immediately distinguish it from most
otber ascomycetes (and indeed mis.es questions about the taxonomic positioo of thi s
order). (8) It produces an exposed layer of asci on the surface of the host leaf (Fig. 4.9).
Since there is no surrounding or supporting fungal tissue, there is nothing we could ,all
an ascoma. (C) The ascospores often bud in a rather yeast-like manner. even while still
inside the ascus. (D) When the asci open to re lease their spores. they tend to split across
the tip, rother than around it (Fig. 4.9), so they are not like the rest ofthc operculate group
~com!XU"e them with the asci of the Pezirules, the nex t order. As yOt! may ha'e guessed by
now. thi s group sits uneasily among the other ascomycetes. and one eminent authority
grouped the Taphrina!cs wi th the smut fungi (see order Ustiiaginales in chapter 5); both
are yeast-like whe n grown in axenic culture. Compare its features for YOlIr:se!f with some
of the orders that follow.
~a k ld
-",
""""P"'" ,
'Il
asO on
~acI1 ~a!
tIe/Iiscena
~ U~PECCI'
eB18UOTECA
EUMYCOTA: OIKARVOi\'1YCOTA:ASCOi\rvCOTINA 35
Series Unitunicatae-Operculatae
(2) Order Pw zales: ISO genera. 900 species. The ' operculate d bcomytetts' we'll look at 7 of the 13 families currcntly rccognited.
a) Family Pezizaceae. Classic 'cupfungi' producing apothecia\ as~omata that are
usually shaped more like saucers or goblets, usually without stalks, and found growing on
wood, dung or soil. They vary so much in colour, tc:<turc and ornamentation thaI most
discornyccte specialists split the Pezizaceae into several tri~s or even families. Their asci
have adiagnostlc pop-open lid or operculum (Figs. 4.3, 4.10 B). and the tips of the asci are
amyloid (sometimes e:<prcsscd as ,> or in Europe as J' - this means giving a blue, starchlike reaction in an iodine solution known as Melzer' S reagent). A small species of Peziza
(Fig. 4.10 8) often crops up on soil in greenhouses. frequently preceded by its blasticsynchrol"lQus Chromelosporium anamorph (Fig.4. IOA). Largcr species of Peuza, producing thin. rather brittle apotheda\ ascomata several centimetreS across, wilh light bro"'n or
Qrange hymenia. can ~ found on the ground in spring and fall. The c:<posed hymeni um
of each of these ascomata contains millions of asci. and if you rmd a ripe specimen and
.",, -
intene"
\
~----
TuNrHst;vum
G ;so...-.l_$pO<ft
Fig_4.11 Suggested evoIutio rklfY seq.Jence from epigeous to hypogeous Peziza les.
58 ClL\PTER FOUR
eroce by bisecting the fruit bodies. While the cap and stalk of the tNe morels are fumly
united, the cap of Velpa is attached only at the apex. In addition. the stipe of Verpa is
'stuffed' with conony mycelium, while those of Morchella are completely hollow.
(g) Family Tuberaceae - the troilles. Here, the evolutionary process still active in
the Otideaceae has run its course. The ascomata are sequestrate, hypogcous and solid (no
air spaces any more - as you can see in the bisected specimen of Tuber aeslivum in Fig.
4.10 F, which a truille dog brought to me at Scheggino in Italy). The asci of Imilles.
produced in a highly convoluted hymenium, ~ rounded and thin-walled (Fig. 4.10 G)
with no trace of an operculum or other shooting mechanism, and usually contain only 13 spores. The ascospores of truffles have complex, highly ornamented walls. They come
in two basic patterns - spiny and lacunose (Fig. 4.10 G). Only by examining a series of
microscopic characters, and considering some intennediate fonns that trace the probable
course of evolution in the group (Fig. 4.11) can we tell that these fungi ~ related to the
'operculate discomycetes:
Although it doesn't make taxonomy any easier, we must now logically place thesc
hypogeous (underground) families wilh their epigcous (above-ground) forebear.; in the
order Pezizales. The hypogeous habit has necessitated the evolution of new methods for
passive spore dispersal, in which some agency other than the fungus supplies the energy
for dispersal. Members of the Tubcraceae, especially species of the genus Tuber (the true
lr1Jffles). have achieved this by developing what ean only be called fascinating smells.
These odours are released when the ascospores are mature, and lead many mammals
unerringly to the ascomata, whieh they unearth and consume, subsequently depo~iting
the still-viable spores elsewhere. Tuber melanosporum, the black diamond, Queen or
Perigord truffle of Fn:nch gastronomy, is dependent not only on mammalian vectors but
also on the roots of oak and haze lnut trees, with which it establishes a symbiotic
edomycorrhizal relationship (see chapter 17). Tuber melano$porum and TI,ber magna
rum are. respectively, the blac k and white tromes of French and Italian haute cuisine,
perhaps the most highly esteemed (and certainly the most expensive) of all edible fu ngi .
and so are discussed in ddail in chapter 18.
(3) Order Elaphomycetalcs: I genus, 20 spec ies. At firs t sight, the hypogcol.ls
ascomata of Elaphomyces look Just like truffks; and they 're even called 'deer tmilles ' .
But they have no hymenium - the basically spherical, non-shooting asci are produced
randomly throughout the interior of the ascoma. Elaphomyces no longer offers much in
n
I
59
the way of visual dues about its possible epigeous ancestors, so only mo!etular techniquts can help us decide its relationships.
Series Unitunicatae-Inoperculatae
Although none have lids (opeKula), the asci of this group are not as uniform in
appearance or structure as we might like (Fig. 4.12). Most have thickened walls al their
tips. pierced by a fine pore. Inside the apices. many have diagnostic sphincter-like rings.
which control the expulsion of the spores. Some of those rings are a myloid OT l ' (they
stain blu e in iodine). others don't react wi th iodine and are called chltinoid. Some asci
don 't have rings at all, and in one such order-the lithenized Lecanoral cs (4 .12 G) - the
Bscal apex is extremely thick and pierced by a narrow canal. The troe relationships among
these orde rs have yet to be full y worked out.
(4) O rder Sphaeriales: 225 genera, 1.300 species. Man y members of this order
produte dark, brill Ie, globose to pe:t.r-shaped individual per:ithecial ascomata with prominent ostioles (narrow apical openings) (Fig. 4.13 A, B). Others have many perithecial
cavities immersed in a single stroma to form a compoond fructification (Figs. 4. 13 C, D).
The asc i often have an apical ring or sphincter, whith is usually, though not always,
amyloid (stains blue in iodine). Thread-like, sterile elements called paraphyses are present
between the asci in the hymenium of some members. but absent from others. Ascosporc~
can be light or dark, simple or septate. with or without germ pore or slit. sometimes witb
gelatinous sheaths or appendages.
The ~ompound fructification of Xy/arja. a common wood-inhabiting genus (Fig .
4.13 C). has hundreds of pcrithecial ascomat a just below the surface Each perithecium
contains many asci. The asci are inopeKulate. with an amyloid apical ring and contain
eight darkly pigmented. asymmetrical spores. These spores will eventually be shot OUI
through the narrow ostiole.
This order also includes such pathogens as Hypoxylon pruirla/um, which causes
poplar canker, a disease that kills milliOllS oftrccs every year. The extensive. more or less
elliptical cankers develop groups of pcrithecial :!$Comara after the tree cambium has bet:n
killcd .
(5) Order Sordariales: 5 families. 75 genera, 6OOspecies. This is agenernlly saprobic
group producing solitary perithecial ascomata. and found on dung or decaying plant
remains. Their asci sometimes have non.amyloid apical sphinctcrs. and sometimes lack
any apica l apparatus. Scveral members of this order are important tools in fungal genetic~
and biochemistry. First and foremost is NCllrospora. which has justifiably been called the
'Drosophila of the fungus world'. It was on Ncurospora CTaSJa that the science ofhapJoid
genetics was founded. The uses of NClIroSporo. and Sordnria mutantS are explored in
chapter 10. Many species of Sordari(l and PQdospor(J. (Fig. 4.13 A) fruit on herbivore
dung. and shoot their ascospores from perithecial ascomata whose necks are phototropic
(poim to,,-ard the light). Different members of the genus Podos{JQm. which has over 100
spedes. have 4, 8, 16, 32. 64. 128. 256, 5 12, 1,024 Of 2,~8 ascospores per ascus. The
\'arlOUS rombinations of tubular and gelati nou. ascospore appendages in Potk>spora not
only help in species identification. but also Slick the spores to &!'Iss after they hU"e been
shot away from the dung on which the a5Comata develop. Somc species of Podospora
have Phialophora anamorphs (Fig. 4 .J3 A). Choe/Qmium (Fig. 4 . 13 B) is un important
cellulolytic genu s that damages fabrics and paper. especially in the tcopic s. II differs from
most other Sordariali:s in that its asci, though cylindrica l, deliquesce or autolyse at maturity. Sin~e they don'l shoot their spores. thcy have no apical ring mechanism. and the
mucilaginous. lemon-shaped ascospores ooze out of the ascoma into a charncteristic mass
of toiled or dichotomously branched hairs that dcvelop on the 101' of the ascoma. Dis
~ UFPECCB
O BI BLI OTECA
60 CHAPTER FOUR
petsal must be b)' rIIin or arthropods. Chaewmiunt has BQtT),otYichufJI anamorphs (Fig.
4.13 B). Neums{'QT(i has Chrysoni/ia allamorphs.
(6) Order Diatl')'pales: 20 genera. 125 species. The bark on dead branc he~ of tree,
often devdops eruptions that mark the extensive immtrs4:d strOmata (compound ascomata)
and the grouped ostioles of sueh common genera as Dia/rype (Fig. 4.13 D) and QI/memorill.
Diatrypaienn asci have a tiny amyloid apical ring, and the ascospores, also vel)' small , ore
characteristically sausage-shaped (allantoid).
(7) Order Hypocrealcs: 80 genera, 550 species. This order is recognized by its
brigbtly coloured, simple or compound, peritbecial ascomala _ usu~lJy yellow. orange or
red - wbich are fleshy or waxy in lexrure. and usually bome on supporting layers of
mycelium (s l.lbicuJu) or in stromata. Four genera are especially well-known:
(a) Nee/ria (Fig. 4_ 14) often has bright red, superficial peri thecia (right) contai ning
two-celled (di dymOSporouS) ascospores. Some species couse cankers and diebac ks of
-.- -
...
~.
t . <''00'&
8. CI...._ (~")
"flood ucorn...
EUi\lYCOTA: DIKARYQMYCOTA:ASCOl\'1YCOTINA 61
trees. N((tria sensu laID has a "arieLy of conidial anamorphs (Fig. 4.(5), bUI all of them arc
phi::tlidic. The crumpent sporodochill of one commonl y encoumcred anamorph.
Tuben:1l10ria (Fig. 4.14 ). cause a condition known as coral spot. As you can see in Fig.
4. 14, the TIlIU'n:1l1aria anamorph oftcn grows beside the dark red NtCiria ~ritheeial
a.o;comata. It is interesting and a little unusual to see both phcnm}'pic expressions of the
g~!lOme being produced simultaneously. HOI'/eve r, the most economically important of
the nectriaceous lInamorphs are cenain Fusarium species (Fig. 4.1 5. 15.2. 21 . I 8). ITl.lny
of which cause destructive wilt diseases of higher plants or produce mycOlOxins.
(b) Gibherella also has Fusarium anamo rph s. A member of thi s genus causes a
dise::tse of rice called 'foolish seedling' in which secdling~ grow too rapidly and conse
quent!y fall over. The active principlc. a plant growth honnone called gibberellic acid.
has bee n extracted and is !lOW widely used to stimulate plant growth.
(c) H)"poll1)"ce.i laClijluurum is an orange fungus which parasitizes the agaric (mush
room) gene ra wC/arius and Russufa, producing a layer of tissue that completely covel"';
the gills and suppn:sses their development. then developing thousands of bright orange-
.. otf.e
-~----<
,
0
~ ..
..", 06ocf>rOl
~ma
TuIHrCtJI6rl.
CC"Go:)Qf\O'.
... ~ ",,!&IodH
01
TU~rcUIMfll aoarroorpl"l
.'.! UFPE.CCB
62 CHAPTER FOUR
~aISLlOTEC!'!.,
rpf
IT ,..o.'oow.
,"',,...,,,.,.,'''''0<\0.
n __ """""
i/ '\
""",,,-;;--~--:~~,"-~~~g
Fig. 4.15 HypocrroJes.: anamorphs of Nee!,;a sensu lata Arrc'J.Ns inc5cate possble i'les of
"""""'"
red perithecial ascom ata all over thc surface of the host. The Hypomyces completely
envelops the aborted mushroom and its colour gives the host-parasite combination the
name 'lobster fungus'. Strangely enough. this monstrosity is edible, though 1 regret to
have 10 tell you that it does notlaSte like the divine crustacean. Hypomyus has extremely
characte ristic spindle-shaped, two-celled. colourless ascospores. The anamorphs of
ffypomycts species belong to the hyphomycete genus CladobOlr)"um. which has an unusual blastic-retrogressive method of fonnins conidia.
(d) Hypocrea forms fleshy stromata on wood. The dark spots on these strom~ta arc
the ostioles of the embedded perithecial cavities. 1be teleomorph of Hypocrea, though
not uncommon.is recorded far less oflen than ils green-spored. phialidic anarnorph. Trichodemra (Fig. 14.3) which. because il is a broad-spectrum mycoparasite and produces
ceHulases and antibiotics. is one of the mo st important moulds in forest soils. It is now
being exploited in biolosical co ntrol of pathoge nic fungi (sec chapter 14) and in the
proouction of enzymes which can convert cellulnse to glucose (chapter 24).
(8) O rder Diaporl halt.'5: 90 genera. SOO species. Here several beaked. perithedoid
ascomat(J. are usucl.ly immersed in a single Stroma (a.'i in DiaporlM impuIsa. Fi8. 4.16).
Paraphyses are often absent; and the asci. which have an amyloid apical ring. become free
inside Ihe ascoma and then autolyze. This rather paradoxical situation suggests that
evolution is in active progress here. Two important genera stand OUl. Cryphonec rria
(Endorhia) parasWca causes chestnu t blight. which almost extinguished an important
species of NorthAmeric an tree in about SO years: you can read the full story in chapter 12.
Because of this near-extinction, you will probably nm be able 10 find speci mens of
Cryphoneclrio, but another member of this order. Gaeumannqmyus gramirtis. which
causes 'whi teheads' or 'lake-all' of wheat, is common. It rots the fOOlS of afflicted plants
and so causes premature drying OUl of the plant, sometimes reducing yields to zero.
(9) Order Leolia les: 13 families. 400 ge nera. 2.000 species. The ' inop('fculale
disl,:omyceles.' The apothecial ascomata are superficially similar to those of the Pezizales,
bul the asci are inoperculate. and usually have amyloid apical rings. This suggests to me
ElThIYCOTA: DIKARYO;\IYCOTA:ASCOi\IYC011'-"A 63
that the two major kinds of apolhecial ascomata arc examples of parallel or convergent
evolution. Several of Ihc families in this order are common and well -known. so four of
them are dealt with below.
(a) Family Sclerotiniaceae. As the name implies, Ihese fungi often fonn sclerotia.
which may be solid masses of fungal tissue. or may be of mixed origin - fungal hyphae
riddling a mummified host such as a peach, plum or cherry. or a catkin. Having ovef\\.in
tered in this guise, they germinate in spring and use the stored energy to produce slalked
apotbecial ascomata (Fig. 4.17 A). Ascospores, the primary inoculum, are shol when the
hosl is in flower. and gain entrance through the Sligma. The anamorphs are generally
responsible for sccondary dispersal during the growing season, and some cause serious
planl diseases. For example, Ihe soft brown rot of peaches (Fig. 4. 17 A) and chcrries is
produced by a Monilia anamorph of Monilinia . The beige or greyish powder on the
surface of Ihe peach and the cherry are made up of bran ched chains of conidia. The longer
I leave Ihe ripe cherries on my cherry Iree. the more oflhcm will succumb 10 the Moniiinia
sofl brown rot. as the conidia being produced on one cherry infecl others (see chapter 12).
Anolher Monilinia produces spur blight of wild cherry, killing back young shoots and
forming new conidia on the leaves.
Many members of this family have distinctive anamorphs . while the teleomorphs
are rdatively uniform . So some of the genera erected for the teleomorphs have rather
atypically been distinguished by characters of their anamorphs - and even named after
them . So we have Sclaa/illia with Sclerotium (sclerotial) anamorphs, Moni/inia with
Monilia anamorphs (blastic -acropetal), Botrya/inio with BorT)tis anamorphs (blaslic
synchronous). and Sireptotinia with Srreplobolrys anamorphs (blastic~sympodial).
Sclerotium . Monilia and Botrytis cause several serious plant diseases - grey mould
of strawberry is caused by Botrytis cinerea (chapter 12). but when BOlrytis grows on
overripe grapes in certain areas of France. Germany, Hungary. and South Africa it is called
the 'noble rot' in several langu ages ('pourrilUrc noblc ' , ' edclfaulc') becaus.c the small
quantities of sweet dessert winc that can be made from such shrivelled grapes have intense
and exquisite Oavour, and can be sold for very high prices. Find out what a boule of
Chateau d 'Y quem sauternes from France (or a 'Trockenbeerenauslese' from Germany)
costs at your local wine store: be prepared for a shock. The full story can be found in
chapter 19.
(b) Family Ph acidiaceae. Somc Phacidium spp. cause snow blight diseases of coni
fers. If we look roore closely, we will see that this family is not typical of discomycetous
fungi in general , sincc the ascomata develop inside host tissue and are at first covered by
a thick roof of dark fungal tissue (Fig. 4 . 17 D). But at maturity th e roof ,plilS open and
apical ring
host
periderm
ascospore
immersed perithecia
64 CHA PT ER fO UR
exposes the hymenium. 111C apical ring in the asci is amyloid W). Comp:m:: thi s family
with Order 10, Rhytismatales. below.... How do these orders differ? Phacidium has
coclomycetous anamorphs: those of pathogenic species such as P. coni/erar"," belong to
ApOSlrI.useria. while those of saprobic species li ke f'. beru/inlllli belong to Ceurhospora
(Fig. 4.1 7 D).
(c) family Geoglossaceae -literall y earth-tongues _ produce unusual stalked,
somewhat flattened and tongue-like aSCOm3ta which emuge from the ground (Fi. 4. 17
B). The hymenium doesn't line a cup or saucer. bUI co'ers Ihe convex upper surface of lhe
aswma, which is fleshy and yeUow in Spa/hl//aria, tough and black in Microg/o$SWII and
Geag/o!iJum. If you squash a tiny piece of the hymc nium of a mature Geog/O.'SHIII a.>coma.
you will see the asci, each of which con tains a bundle of eight long, parallel.
phragmosepuuc brown ascospores (Fig. 4.1 7 B).
M~"IIi.
anar.">Q1p/l
.,., PlOCIt
~.ti ....
.... P!'C_
In.nti"ll on
corui., n. lIn
c."mo."",. "'.me'l'"
EIDfYCOT;\: DIKARYO;\rYCOT;\:A.'iCQ:\IYCOTL"A 65
(d) Family Leotiaccac comaiM more typical 'discom)cetc.' ~uch as 8i.!porcllll.
which produces those small ycllo'" discoid apotheda so CQmmon on fallen, decorticated
tree-trunks, while Chforociboria. also fairly tommoll. stains wood green and fomlS small
green 3lX'1hecia. Less typical are the Spectacul:lr ascomat:l of uo/ia (Fig. ~ .17 C): these
are much larger; stalkM. jelly-like. and have convex fertile heads. a beautiful velvety
green in uotia ~iscosa. in conlrast with its vivid yell()\O. sti~. AnOlher rather spcct.:lCuhr
member of this order is Btl/garia inqllinalls. found on wood of deciduous trees. The
clustered apotheciaJ ascomat" h"ve "rubbery texture. and the hymenium is jet black.
(e) Fumily Dennateaceae includes Diplocarpon rowe (whi ch. with its MarSS/Jllina
anamorph. causes bluck spot of roses) and a cornman but interesting fungu~. TnJ(ilUa
j!ideo/a, that fruits on the upper surt'ace of dead leaves of holly (f/ex ) in my garden. Its
ascomata have a hinged lid. which opens when thc leaf is kept in a dump chamber.
( 10) Order Rhytismatales: 70 genera. 400 species. The ascom:ua.like thOSt: of the
Phaddiaccae. develop irnmcr!.Cd in host tissue or a fung~l stroma. .... hich ultimately ruptures 10 exposc the hymenium. The asci often have apical rings, but these are small and
chitil}()id (do nO! Slain blue in iodine). The aseospores ~re usually long and thin. and have
a slimy sheath (absent in the Phacidi:lCcae). The gcnus Lophodl'rmillm is sometimes
endophytic :lr\d asymptomatic in pine needles fOl" much of ilS life. but c\'entually fruits
after the needles die (see chapter 11). Rh)"lisma acerililim cau~s 'tar spot" of red maplc
leaves in eastern North America. Rhyrisma p""cralllm produces ~ simi13r syndrome on
big-leaf maple in westcrn l\orth Americ~. but the small. Individual aseomata do not fuse .
( 11) Order Cla vid pitalcs: 27 genera. 270 species. This order comprises a group of
high ly evolved and sophisticated. obligutely parasitic fungi with: (a) frequcmly ~talked.
all-fungal stroma!a (Fig. 4.18 B.C.D.E). (b) long asci without apical rings, but with thick_
ened tips (Fig. 4.18 F). and (c) long. Thread-like asco~pores thm in some taxa rr~gtii1fnt at
or following release. ( Fig. -1.18 F). Three bizarre and spectacular genera. Cltll"kt>ps.
Cord)"C(ps and !:.p ichl.u.
gh'e us a snapshOi of this fascinating order.
(a) Claviups pllrpurea (Fig. 4.18 AC)diseharges ilS ascospores when ilS main host.
rye. is in flower. and infection Illkes pla~"C through the stigma. As the infection progresses.
the fungus lakes over thc food being channeled imo seed-production by the host. The
ovarian tissues are repl aced by a mycelial mat that prod uces rm.$ses of conidia of the
Spilact/ia anarnorph in a sweet,smelling neCI~r. In sects nre attractcd 10 tht: nectar, and
spread the conidia tn other host phmts. The m)'cclial mal haraens and becomes a purpli~h
sdcro tium - the ergot - which r~p1a~'es the grai n (Fig . -l.18 Al.
,,m
shore in the Pacific Northw~st. The largest ergot is 4 cm long ana almo~t5rnm wide. The,;.:
sderotia fall to the gwund in autumn. overwinter. ana g~nninme the following spring,
each producing scve-ral stalked slwmata (Fig. 4.1& B. C). Each stroma has a spocrical head
"'ithin ,,hich many pcrithe.:ia de"elop ju~t below thc surface. Each ]X'rilhecial cavit)"
contains many asci. each with eight extremely long ascosporcs.
Because this fungus has a small larget, the stigma of the rye flo"'cr. which is avail nble only during a narro ..... time-w; ndo", ~nd because spores reach it only by chancc. the
fungus must dispcr;c a large number of aSCO$pores in a short time. A rough e;rlcubtion
suggests th~t a single ergot can give rise to 5 stromata. and each of th Ose may contain 100
pcrithecial ca"ities. each cavity with 50 asci, and each ascus producing 8 ascospores: a
towl of 5 x 100 x 50 x 8 ::: 200,000 propagules per ergo!.
If the sclerotia are a,cidentally co ns umed by cank. or if ryc bread made from ergoty
rye is e~ten by humans. a large number of alkaloids founa in lhe ergot cause a form of
poisoning knO"'n as ergotism. Of. more picturesquely, SI. Anthony's Fire. Human vktims
66 CHAPTER FOUR
frequ~ntly
hallucinate and fee! that they are burning (see chapter 21 for a fuHer account of
this mycotoxicosis). The alkaloids ergotamine and ergotaline cause contractions of the
smooth muscles, and the ensuing restriction of the peripheral blood supply can lead to
gangrene and even death. SI. Anthony's Fire was fairly common in the Middle Ages, and
sporadic outbreaks occurred until recently_ Ergot, the only fungal structure in the British
Phannacopoeia Codex. has been used in obstetrics both to induce childbinh and to
control post-parruml bleeding. Another species of Claviceps broughtlhe germs renewed
fame, or perhaps I should say notoriety, as the prime source of LSD (lysergic acid diethylamide), one of the most powerful psychedelic drugs (it is a hundred times more potent
than psilocybin, the active ingredie nt of ' magic' mushrooms).
(b) CQrdyceps species (Fig. 4.18 D-F) are bizarre: they generally parasitize insttts
or spiders, or hypogeous (underground) fungi, aod their large stromata spring up directly
L~ po<\O?I ",.n
""'",pillar
I""'"
ElophamycfS {no<ll
-,
~ UFPE.CC8'
OS !B LIOTECA\
EUMYCOTA:DIKARYO;\lIYCOTA:ASCOMYCOTlNA 67
from their victims. These perithecial stromata arising from an insect larva or pupa are
known as "vegetable caterpillars," in recognition of the fact that they always incorporate
elements from more than one kingdom. These strange 'two Kingdom' structures are used
in traditional Chinese medicine as a treatment for "general debility after illness, weakness, spitting of blood caused by TE ... chronic coughing and asthma ... night sweating
... anaemia ... malignant tumour."
As mentioned, a few species of Cordyceps don't pick on arthropods, but cannibalistically attack another fungus. Actually, it's even another ascomycete - the underground
deer uuffle (Elaphomyccs). The large, stalked Hroma of the Cordyceps can be seen
emerging from the host troffle in Fig. 4.1 8 E. Every September for many years, during a
mycology field course I taught, we found Cordyceps parasitizing Elaplromyces along one
of the hiking trails in Algonquin Park, Ontario. Once one of the students had spotted the
club-shaped stroma of the parasite, excitement ensued as we dug down, following the
yellow rhizomorphs of the fungus , UUlil we finally excavated the host. This fmd was often
dubbed _ and with good rcason - 'fungus of the day,' though perhaps that title should
have been pluralized.
Cordyceps, which must infect target organisms that are clearly far scarcer than rye
flowers, goes a big step funher than Claviceps in the multiplication of spores. Each of the
8 long ascospores breaks up into about 100 partsporos, often while still in the ascus (Fig.
4.18 F). I estimate that the usually single large stroma produced by this genus from its
fungal or insect host may bear as many as 800 perlthecial ascomata , each containing at
least 100 asci, each ascus containing 8 spores, and each of them fragmenting into 100
part-spores, for a total of800)( 100)( 8)( 100:; 64.000,000 propagules: sixty-four million
spores from a single stroma.
Many of the anamorphs of the Clavicipitales are in the genus Acremonium, with
simple, tapered phialides, but in 1996 Cordyceps $lIbsess;Us was discovered to be the
holomorph of TolY[Jodadillm ni\"~um (as T. inj1anun) . So what , you might say, until you
realized that Tolypoc/adillm inj1alwn is the fungus that produces the medically important,
selective immunosuppressant Cydosporine. which has made the organ transplant revolution possible. For the story of that amazing phannaccutical, see chapter 24.
(c) Epichloc causes 'choke' disease of grasses. A grass called Glyceria normally produces open, nodding inflorescences. When Epiclrloif attacks , the energy for the inflorescences is stolen by the fungus and used to produce creamy yellow perithecial stromata, each
incorporating many peritheda, that surround the stalk of the now sterile grass. In.a recently
discovered twist to thi!; story, this apparently damaging parasilic fungus has been found to
have a mutual istic symbiosis with the grass. The simple, phialidic anamorph of Epichloif
(which used 10 be calledAcremon;um, but has recently been segregated into a new anamorph
genus, Neoryplrodium), grows systemically throughout the grass plant withollt producing
any disease symptoms, and actually protects the grass from herbivores by producing a
virulent neurotoxin. A more detai led discussion of this relationship is given in chapter 2 1.
(\2) Order Erysiphales: 28 genera. 100 species. All members of this order are
obligate parasites on leaves and fruits of higher plants, causing diseases called powdery
mildews. These fungi have superficial mycelium which extracts nourishment from the
host plant through specialized hyph ae that penetrate the epidennal cells of the host and
develop special absorbing organs called haustoria (Fig. 4.19). You should have no diffiClllty spotting a few powdery mildews in sununer because their whitish co lonie, growing
on living leaves are unlike anything else. In dry sununers they are particularly common
on gra,s in shady parts of lawns, on squash plants (cucurbits), on perennial Phlox, on
Ainus rugos a, and many other angiosperms. Basauxic chains of conidia of the Oidillm
anamorph (Fig. 4.19), whose powdery, whitish appearance gives these disca,es their name,
63 ' CHAPTRFOUR
=m,
Sphaerorheca
ErJ~iphe
Prxlosphaero.
MicrosplUlera
Uncinlila
Phyllaclinia
arise from the mycelium in carly summer. Airborne conidia spread the disease from plan!
to plant. and are later succeeded by dark -coloured ascomma which mature slow ly in fall.
and release ascospores the following spring. This orde r parasitiz.es well over 1.000 higher
planl species. and the powdery mildews of gl'3pes, hops, gooseberries and cereals are
eeonomically important diseases_
The generic COncepls in this order are unusually straighlforward and easy to appl)'.
since they depend on two major features of the a~oma: (I) the number of asci within it.
and (2) the kind of (lppendage growing out from it (fig. 4. 19). In one way. the ErysiphaJcs
arc the anti thesis of Lhe Sclerotiniaccae. Thel1;). the anamorph s were far more distintti'e
and diverse than th e lekomorphs; here , the reverse is true. Most anamorphs of the
Erysipbales beloltg to tbe hypbomycete genus Oidilllll. Althou gh Ihe order Erysiphalcs is
~ery easy to charactcrizc and reeognilc, its sy~tClllatic jX.Isition is comro\ er.;iaL Some
mycologists insbt Chat its asci are bituilica ce. which would place it alongside the
Dothidca!cs (see below). but many mycologists do nO{ accept this. and place the order
among the unirunicatt: ascomycetes. The asci are sometimes ralher Lhick-walled. but one
of the world experts on the group, Dr. Zheng Ru-yong of Beijing. tell s me that she has seen
dislinctive inner and outer wall layers only in an un described taxon frorn Tibet. and has
never seen the "Jack-in-a box" mechani sm so typical of the bitunic:lIae. The usci seem to
have neither an o~rculum nor an apical ring apparatus_ This information, plus their
strange arrangements for dispersal and dehiscence (see chapwr 8). cheir unique basau",ic
anamorphs. and their obligatdy para5itic )'et slrange1y superficial lifestyle. make them a
rather peri phera.l (though important and interesting) groLp.
A!der le3\' oflen bear extensive colonies of PhyllaCli/!ia. Under the dissecting
microscope you can see ascomata with unique appo::ndage.> (Fig. 4.19). The basal bulbs of
the appendages develop Ilrst, then the needl e- like extension, grow OUI. At ITIJturi(y. these
~pp<;:ndages aJj b.:nd downwnrd in unison ,111d lever the uscoma off the leaf surface, br~Jkin !!
its conneclions with the mycelium. it is then free 10 be blown or splashed away. becoming
attached LO a new ~uhstrntc by an Jpical blob of mu<:il~ge seneted by specialized hyphae.
Par.Jdoxic~ll)'. this leaves the ao;ci. which are designed to shOO( their spores, facing down
w:lTd. The final chaplcris written when Ihe ascoma splits around thecquatorat J builtin line
of ".'cakness. and hlngo:s open so that thc sjX.Ires can finally be ,hot away. (Fig. 1l.3).
Series Prototunicatae
In (hc following fOllr orders, the walls of the asci break down when the a,cosporcs
mature, and therefore the SjX.Ires cannot be forcibly ejected. This has led to (he evolution
of new ways of dispersing the spores.
70 CHAPTER FOUR
can make identification easy - if the teleomorph is present The ascomata of various genera
are illustrated in Fig. 4.20 under 'peridia and appendages'.
If you isolate dermatophytes in pure culture, the y mayor may not produce
tekomorphs. But they will develop characteristic thallie conidial anamorphs (Fig. 4.20).
Sometimes these produce small, thallic-arthric conidia (Chr)'sosporium or A/albranchca),
sometimes large, spindle-shaped. transversely septate, solitary thanic conidia (Trichophyton or Microsporum), and sometimes the same culture will produce both kinds of
conidia. When a fungus has two or more different anamorphs, thes e are called
synanamorphs. The three most important anamorph genera of dennatophytes are Epidermophyton, Microsporum and Trichophyton. Of these. Epidermophyton has no known
te!eomorph, nine species of Microsponun have telcomorphs in Nanniuia, and se .... en
species of Trichophyton have teleomorphs in Arthrodemw .
."
,,
-------
---
.......
~o
---0
-~ ----....
---@O
--0
-.
---...-.--- -.
0
.... .
~,
...... ......
1I
..~"'''''"
0"""" ...
_
..
----- --. ........
,,
""""
:~ UP ~. CCiil'
~"<,; 3:::3 LIOTECA
-.
' . ~"" '/i.",,
5:
O<>h"""''''' .....
72 CHAPTER FOUR
CeralocySlis jagacearwn and itS Chara", qu(!rcina phi~lidic :mamorph are the
cause of another widespread and serious tree disease. oak wi lt. The tdeomorphs of
Ophiostomn and CerolOC)'slis are very similar, but the genera are easily distinguished by
their anamorphs: the Chalara anamorphs of Cer(llQC)'Stis have solitary phialides with
long, mbular coHarettes. and form long. cylindrical conidia (Fig. 4.6): OphioslOma has
se\'eral different anamorphs, none of them anything like Chala",_
(16) Order Lahoulbenlales: 75 genera, L700 species. (Fig. 4.22). This group i, so
distinct fTOm the other ascomycetes that some ~ople put it in a se parate Class.
Laboulbeniomycetcs. While thai might be justifiable. it wO\lld also complicate our clas
sification and make life a little mOle difficult for you. So. having noted the possibility of
suc h ele\,ned status, I will press on. All 1.700 known species are invariably found at
tached to the exoskeleton of insects. or occasionally millipedes and mites. Thc dewlapmcnt of SligmalQm},ces baerii. which is found on houseflies. is followed in fig . 4.22 C An
as(osporc becomes !mached to lhe animal. gcnn inat.:s, and sends a foot inlO lhe exoskel
eton to absorb nutricnts. Although haustoria may penetrate as far as the epid~rmal cells.
Ih~re is never any real invasion of host tissues. Thc ascospore develops a median septum.
Series Bitunicatae
These all produce biwnicate asci. (Again. if you don't remember what these
look. back. at Fig. 4.3).
A.
.von""'
. "'""-.
itlHq~~!i.
lITe.
74 CHAPTER FOUR
(17) Order Dothideales: 50 families, 650 gene,.!, 6,300 species. This is an extremely large and diverse order, which will obviously need 10 be subdivided when its
taxonomy is better understood; I will mention only one or two conunon examples.
(a) Family Venturiaceae. Venturia inaequalis causes apple scab, an economically
important disease. You'll find the Spi/oca ea pomi hyphomycctous anamorph causing
large brownish spots on the leaves and disfiguring blacldsh scabs on the fruit. It produces
its blastic-annellidic conidiogenous cclls (Fig. 4.23 A _ you can see the rings clearly) and
obclavate conidia on those spots and scabs. But you won ' t find the teleomorph during the
growing season. Its psel.ldothecial ascomata (seen in section in Fig. 4.23 A) develop
slowly in the dead apple leaves over the winter, and the ascospores are shot in spring when
the susceptible young leaves appear.
Apiosporina morbosa causes the extremely common and disfiguring black knot of
some rosaceous trees. especially wild cherry and damson plum, its pseudothecial ascomata
developing on conspicuous black fungal stromata: you shouldn't have too much trouble
spotting these on wild cherry trees. lbis fungus damaged and disfigured my damson
plum tree despite my best efforts at control.
(b) Family Pleosporaccac. Pleospora herbarum is common on dead herbaceous
stems, and has anamorphs in the hyphomycete genera Stemphylium and Alternaria (the
fonner shown in Fig. 4.23 B).Asco,pores and conidia in this genus are both dictyoseptate.
Phragmoseptate or dictyoseptate ascospores are common in the Dothideaks; in fact, if a
fungus has ascospores of this kind, the odds arc about 9 tol that it is a member of the
Dothideales. Coelomycetous anamorphs are also conunon in the bitunicatae.
(e) Family Botryosphaeriacea e. Guignardia aesculi and its Phyllosticta
coelomycetous anamorph cause a leaf scorch of Aesculus (horse-chestnut. buckeye) that
defo!iat~s many ornamental horse -chestnut trees in eastern Canada a month or so before
they would nonnally lose their leaves. It doesn't kill the trees, but it is extremely unsightly and significantly shortens the trees' growing season. Horse-chestnuts on Vancouver
Island aren't affected: perhaps the disease has not yet reached the west coast.
(d) Family Capnodiaceac. Commonly known as 'sooty moulds,' these fungi grow
on the sugary excreta of various insects such as mealy bugs and scale insects. I have found
blankcts of their thick black mycelia covering the trunks and leaves of southern bcech
(Nolhofagus) in the forests of South Island, New Zealand. The black. feathery branches of
the numerous anamorphs are easily scen by the naked eye.
Now I will provide a dichotomous key to lie 17 orders just discussed. But you will
see at the very beginning of the key that this chaptcr has by no means dealt with all fungi
that produce asci. Many thousands of fungi are always found in intimate relationships
with algae, and are called lichens (chapter 7). Many more never produce ascomata, often
have unicellular thalli. and are chemically rather different from other ascus-producing
fungi. These are known as yeasts (sec chapter 6). [have treated yeasts and lichens se parately because each group is phylogenetica!ly diverse, and includes non-ascomycetous
fungi (notably basidiomycetes).
Asci
Asci
Asci
Asci
wilh
with
with
with
,---
~~.
:. , .... '\,0 ~
... -
-'
-,:;',-,
"
. . .)
LeoUaJes
Rhytis-matales
14
15
Dia trypaJes
Sphaeriales
So rd.llrial es
16
16 CH:\.I'1ER F OU R
often stalked: asci long. n:urow, lacking sphincter,
but apex thi ck. with pore: ascospores long and thread- like.
often fragmeDting at maturity: all obligatel),
..... ........ ...... .. Cl avicipilales
parasitic (on plants. arthropods or fungi) ...
16 Stroma never stalked: asci and aseospores not as above .......... 17
17 Ascomota compound. perithecia immersed, with long neck
or beak: asci with apical ring but lysing ................................... Di3()Ort haies
16
Strom~
J n~ti
lu tC. Kew.
El1i5. 1'>1.8. (1976) 1\ lo re Inmatiaceous H )'ph om~'ecte.~. Commonwealth Mycol ogical
Institute. Kew.
Ellis. M.8. and J.P_ Ellis (1985) :'I lict'ofungi o n Land prant~. An Id ent ifi cation Hand book. Croom Helm. London.
Ellis, 1'> 1.B. and J.P. Ellis ( 1988) :\'Ikro fu ngi on ~ lisceIl3 ncousSuhst ...J tes. An Identificatloll Han dbook . Croom He lm. ull1don.
Hawkswonh. D.L . P.M. Kirk, B.C. SUlton and O. M. Pegler (1995) Dic tionary of the
Fungi. Sih Edn. CAB 1n1Crnali(mal, Wallin gford.
Hughes, S.1. (1976) Soot)' moulds. l\ l ycolOf;ia 68: 693-820.
K~n .
um:c!:P
D81BLIOTECA
&!!
Kingdom EUMYCOTA
Phylum 3: DIKARYOMYCOTA
Subphylum 2 - Basidiomycotina:
the Basidiomycetes
5
i
I
Introduction
With tht: Ascomycetes under your belt. you should now find it easier to cope with the
other half of Phylum DikaryomyCQIa. Subpilylum Basidiomyootina has many important
fe:uures in common with the AS(;om)'cotina: (1) haploid lIudei in 5Om3!ic hyphae; (2)
chitinous hyphal v.w]s; (3) regularly sepia!!: hyphae; (4) presence of central pores piercing
the septa; (5) !he potential for somalic, assimilath'c hyphae 10 anastomose; (6) the produc-
tion of complex and often m3Cf05Copic sexual fruit bodies; (7) the presence of a dikaryophase
in the life cycle (e.lcept in some anamorphic holomofphs): (8) a specialized mechAnism for
launching the tociospores into the air: (9) proouchon of a conidial anamorph by many
species. Make no mistake. ascomycetes and basidiomycetes evolved from 0 common stock.
Yet they are usually relatively easy 10 tell apart , macroscopi cal!y, microscopically
and ultrastrocturaHy, because it is probably a long time , even in geological tenns, since they
evolved apart , 5 0 we can expect to find a lot of differences as well, Here are some of them,
A) Walls: The wall s of ascomycete hyphae aTe basically two-layered, those o f basidiomycete hyphae are multi-layered, Don't worry about this, because it can be determined only with me transmission electron microscope,
B) Se pta (cross walls): DikaryomyCOIan hyphae are regularly septate, but the stlUCture of the septal pore in different c:lassesofthe Iw05ubphyla differs, as you can see in Fig,
5. 1. The differences are importllnl, bul can usually be seen only wilh the electron microscope. Ascomycete sepia (Fig. 5.1 A) are pierced by a simple, central porc, wilh a round
' Vo r oni n body hovering on each side, ready to plug the pore if the hypha is damaged.
Septa of class SacchaTcmycetes (many yeasts and related fungi that fonn ascus-like
mciosporangia; sec chapter 6). are often perforated by many mlcropo r cs (Fig. 5.1 B). In
dasses Holobasidiomycctes (mushrooms. brac ket fungi, etc.) and Phragmobasidiomycetes
(jell y fungi) the se pta have a central barrelshaped structure called a dolipo r~ covered on
both sides by a cap of membralle called a parenthesome (Fig. 5.1 C). The septal poTe of
the rust fungi (atypical basidiomyootilla placed in class Teiiomycetes), is simpler. but is
78
Ascomycetes
,
Saccharamycetas
doIip<lre
C
Hotot>asKliom ycet9s
& p l'u"agmobasic!iomycet9s
uoonale$
(TetlomycetH)
8U CHAM E R FIV E
divide simultan eous ly. one in the hypha. one in thc hook of the crozi er. in such a way that
Ihe subsequentl y delimited ascus mother cell comes to contain a eomp~tib[e p.:lir of
nuclei (Fig. 5.2 A). In ascom ycetes. tbis phenomenon is generally restricted to the hyme nlum. but in many basidiomycetes. similar bypasses are found. not just allhe base of the
basidium. but al every septum In the dikaryophllSl!:. In basidiomycetes. they are called
clam p conn ttt ioflS. and their development is shown in Fig. 5.2 B. If a septate. som~tic
hypha has regular clamp eonnectiol1~. like those in the phase contrast picture (above.
right) it must be that of a dikary{){ic basidiomycete. If clamps are absent. the hyph ae could
still be those of a dikarymic basidiomycctc (many of the mushrooms called boletes have
no clamps on their hyphae), but they could equally be those of a monokaryutic basidi
omyccte. or of an ascomycete, or even those of a zygomycete. since members of Ihe Order
Kicbellales have regularly septate hyphae.
E) Basidia. This is perhaps the most basic difference and one of the easiest to see.
Whik the me iospores of a:s<:omycete~ are developed inside meiosporangia called asci
(Fig. 5.2 A, Fig. 4 .3). those ofbasidiomycctes are fonned outside specialized meiosporangia
called basidia (Fig. 5.1 B). Nudear fusion aud the subsequent meiosis bappen inside th"
cell. but the spores blow out lil<:e tiny balloons at the ends of four tiny tapered outgrowths
called ste rigma llt.
[n most ba~idiomycctcs. the se spores are then actively cxpelled from the ir percher
(Fig 5.3). But remembe r that just ~s in the a:s<:omycetes. there is a Significant minority 0
basidiom ycetes ",,hieh de\elop basidia. but have lost the spore.shooting mechanism.
The,," we call seques tra te. ~ausc the mature bJsidiospores are kept in side the basidioma
(which m~y simply remain dOiSed. or may develop underground). ~ing released l:lter in
a variety of ways. some of which in\olve animal veclOrs. as wc shall sec.
m_.
ern''''
~~~'
~
.
[
!
I \ \
\" \.-:,. \
".1 !::J.
i.'
~
\0
a
\\
"
,
~ ! .I
~\ ~\
,~
<:14"",
I,
,.
1 i
" ~,V~ ~:
'
90
to '"
I '
& ~
h~
'/
'''' m....,...
~)
,:JQ'.
8 ..-.:Io\ienoo...
. ~&,
, ;
.=.
W ti 1!
, \
m.,=
<:<00"1>0"
.
0
I
,
\i' j (fjf
::I
(~~
\
!
r,:, 1
-~
~~~
'\
4 ~ >OQ. " _
' I
I I
,,
,~
Class Holobasidiomycetes
All basidiomycet<)s with holohasidia - those that arc not subdivided by septa belong here. This is the kind ofbJsidium illustrated ubove. bel.:llU'C it is the kin d found in
most basidiomycetes. Again. the presence or absence of cross-walls is a microscopic
chura~ter tha! is ofte n difficuh to see. And again. there are macroscopic features that
enable us to recognize 99% of all holobasidiomy~tcs as belonging to this class. If you
don' t hove these femurc s at your fi ngertip5 a lready. ti me spe nt looking al the various
illustrations in thi s text. and at one of the beautifully illustrated field guides lisled III the
endofthis chapter. will pay off handsomely when ),OU go outdn<m to lool:.for the.~ fUngi.
Its nOt that holobasidiomycctes are all the ~ame : in fac t. they present a dn7.ziing di vCllSjt y
of fonn lmd function. But .... hi'! most hoJobasidiomycctes dcvclop ch~r.tcteristic fleshy_
corky or woody basidiomat!l~ tho~ of phragmobasidiom}cete~ (\\hich have b asidia
sudividcd by septa) (Ire often gelatinous. ~nd tcliomycetes ha,'e nothing you eQuId CJII a
Scp::mlte frui t body. merel)" fonning pustules on thcir Ii'ing hOSK And in ld iomyceles.
toc basidia develop directly from a specialiZed resting sporc called a tdiospore.
Th e Holobasid iomycetes comprise tWO highly interrdatt:d se ries. called
Hym~llomyce t~e and Gnsleromycetae. Most Hymcnomycett:~ shoot their bJ:;idiosro re~
actively from hymenia that are exposed al maturity (G<lSleroulycetes do not). Basi diospor;:s which are to b.:: forcibly dis.;harged (ballistospores) blowout at an angle to the
fine Sterigma that btears them : in other words Ihey are asymmetrically moullIed, or offse!.
as can bte seen in Figs. 5.2 B. 5.4 B and 5.10. JUSI before d\~harge. a droplet of fluid,
enclosed within a membrane. appean at one side of the spore b::tSe, and within seconds Ihe
spore is ~hot away. A minutc quantity of mannitol and he.\0se sugars is secreted from a
small area at lhe base of the spore. forming a hygroscopi c spot on wh ich woter cUlldcllse;;
from the saturated air 'iullounding the bJ~idium. The droplet th~n coalesces instantaneously with a film of wat<,r on the $urf:l<'e of the spore, as in Fig. 5.3, call5ing a rapid
displacement of the sporc's cenlre of gravit,'. Thi~ rcdistribution of ma ss is opposed by the
sterigma whi ch is under high turgor pressure. As ~ result. Ihe spore imm~diately breaks its
fragile conneetion with the sterigma ~nd shoots away with ,'t:ry high initial acre!er.uion,
though it doesn't go very far. The mechanism has been describ.::d as a surface tcnsion
catapult. ft is fascinating IMt esselllial!y the samc mechani sm is found in the bas idia of
mushrooms, jelly fungi. ruSt fungland some ye~sts. II is a HfOng argument for the monoph~'ly of 'he Basid iomycetes.
If you want to follow the extended trail of experiment (tnd observatiun that led to
the \.Current CXpIUn:ltion. I recomm~ nd that you read Mon~y. KP. (1998) ' More g 's than the
82 CHAPTER FIVE
Space Shuttle: ballistospore discharge' Mycologia 90: 547-558. There is also new evidence that some mushrooms chill their fruit bodies by evaporative cooling. This enhances condensation on theiT spores, which apparently need a layer of free water if the
shooting mechanism just described is to work [see Husher et aI. (1999) 'Evaporative
cooling of mushrooms' Mycologia 91: 351 -35 2)
Gasteromycetes, if they have bymenia, don't expose them when the spores are
mature; the spores ~ symmetrically placed on the sterigmata, and are never actively shot
away. I believe that the basidium originally evolved as a spore-shooting mechanism, but
that for various ecological reasons, which we will explore, it has on many separate occasions lost that function. So our assumption is that the various kinds of gasteromycete have
emerged independently. on many occasions, from among the Holobasidiomycetes.
Oberwinkler, an authority on the classification of the Basidiomyce te~ has recognized
nineteen Orders of Holobasidiomycetes, but I will discuss only ten (and give a key to
them later). Why the difference? He subdivides what I cal! thc Order Aphyllophorales
(bracket fungi and relatives) into si)"; Orders, what I call the Agaricales (mushrooms) into
three , and recognizes one or two obscure Orders I did not feel it essential to enumerate
here (Only if you become a professional mycologist will you have 10 think about the
possibility that there may indeed be nineteen Orders of Holobasidiomycetes!) First, two
'outlier' or atypical Orders:
I) Order Exobasidiales: 10 genera, 67 species. This Order is atypical in much the
same way that the Taphrinales was atypical of the ascomycetes. Unli ke most other
holobasidiomycetes, Exobasidium doesn't produce a fruit body (a basidioma) - just a
whitish layer of basidia on the surface of the host plant. The host in this case is a member
of the Ericaceae. Other E)";oba~idiaJes occur on members of the family Commelinaceae.
Ex()hasidillm produces symptoms like those caused by the Taphrinales - excessive growth
of the leaf tissu es, and disturbances in photosynthesis that often cause the leaves to turn
n::d. This has led to speculationJhat these two Orders represent some kind of connection
between the subphy la.
(2) Order Oacrymyeetales: I! genera, 72 species_ These are all 'jelly fungi: again
atypical of the elass. that grow on rotting wood. Their gelatinous, yellow basidiomata are
common and conspicuous in wet weather, but shrivel up and almost disappear in dry
periods. The basidiomnta of Dacrymyces are irregular to the point of 5hapelessness, and
look like those of some Phragmobasidiomycetes (the real jelly fungi) - a quick look at the
basidia (Fig. 5.'4 B) will settle the issue. Basidia of Phragmobasidiomycetes are septate.
but dacrymycetalean b~sidia are not. They have a unique appearaoce: we call them tun,
I,
,
Fig 5.3. Current explanation 01 basidiospore discharge mechanism, from N.P. Money, 1998.
j
;
,
8:
l~omorpll
~ UFPECCe
~!l 1 6L!OI eCtl
,,
,
,,
,
'J
f,
, ),
,
!
!!
i
. ,-
-,
EUMYCOT,\:
D1KARYO ~ IYCOTA:
BASIDIO;"IYCOTL'iA 85
iospores are irregular in shape, ornamented, brown to colourless, and nonamyloid. The
dark tissue give~ a green reaction with KOH (10% aqueous potassium hydroxide) _
Thdepllora terresfris (Fi g. 5. 5 B), with brown. fibrous. vase-shaped basidiom~!a and a
smooth hymenium. often establishes mycorrhizal relationships .... ilb young oonifers in
tree nurseries (see chaph:r 17).
e) Family Clavariaeeae. Club and cora! fungi. Arising from the ground or from
wood, the erect, beige, yellow, while or purple busidiom:ua may be unbranched and clubshaped, as in ClamrimfelphU$ (Fig 5.5 E), clustered. as in C/(IIaria and CI(IIulinupsis. or
repeatedly branched and coral1oid. as in Ramana (Fig 5.5 E). Th ey are monomitic or
dirnitic. The hymcnium covers the uppe r pan of the basidiOffiatil.. and is no! put OUI of
action by repeated wetting, as those of most other hymenomycetes would be. Basidiospores are colou rless. smooth, and non-am>loid.
d) Family Canthare!laceae. The basidiomata are monomitic (coostructe<! from a
single kind of hypha) and arise from the ground. They may be yellow. stalked and ra!h~r
mushroom-like. as in Camharellu$ cibar;us (the 'chanterdlc' or 'pfifferlingc: Fig. 5.5 D),
though the hymeniurn is thrown into thick, fleshy folds which only sup,;,rlicially resemble
gills. The cap of the more deli~ate (bu t still edible) Can lharellus 1:,b(U!Ofl/l;.\ is umbihcute (that is. it has a central. navdlikt depression). Basidiomata may also be: large and
highly convoluted. as in lhe edible Spumssis. the cauliflower fungus. which can actually
be much brger than any cauliflower I've ever seen. The edible 'hom of pknty,' CmltrdlU5.
is often almost black, and has a rather smooth hymenium. Gcmplws looks rather chanteIelie-like, but is nOt edible, The bas idi ospores of !he Ca nth JrelJacca~ ure smooth.
colourless and non-amyloid.
e) Family Coniophoraceae. Thll monomi!ic basi diomata usually appear on wOPd.
and the hymenium can be: smooth. toOthed. folded or tubulate. That of Serpula laCT)"IJiJJs,
the dry rot fungus, is d impled . The basidiospores are smooth, bro" nand double-wall:d.
Sapl/fa and Coniop/lOnl (the ce llar fungus) cause scrious rots of strt!~t urallimbc: r.;. and
Serpu/a can e\'en grow through brick wallS to find suitable substrate_
f) Family Hydnace~"" Th e tooth fungi (Fi g 5. 5 C). The hymenium covcrs tupcring
tceth that point vertically downward. like miniature stalactites_ The basilliomata may ~
ra!h~f irregulur and e)(centric, as in H(ricillllJ erinacells (the wood urchin. which froits on
the sid~ of trees) and Heridmn coral/oidu. or very mushroom-jik. as in D~nlinllln
( Hydnum) relxmdmn. the edible 'heds-ehog mushroom' or s,,eeHooth: Aurisco/piulil
I"II/gare, a dcJ:cat~ mem~r of th~ Hydnaceae with a lon g stipe al\d an e ,centri c cap. frUl t~
on decaying Douglas fir cones. 1'.hny corky or "oody spccie~ of H:.dnellum gro" Oil the
f(lrest floor. ufte n developin:; around and engulfing ccnifer necdle~ and twigs Sarcodmi
i, large, wi th a scaly cap 3011 a dark stipe. The spores o f thi $ family are imooth, colou rless.
and nonamyluid.
) Family S<:hi zophylbceae. The common (amI therefore succe"ful) Schiwphyll"",
commune ( Fig. 5.5 F), often seen on dead branches. looks like an agaric without 3 Sialk.
but is Ie;' !!y 0 compound fructification, in wh ich tll ~ inroned cdg~ ~ of contiguous cupu
!at~ i).asidiomuta give it its mislead ing common naln.:, split gill: This sp..'Ci.:s is easil~
grown in culture, and is a popular subj~ct for gnetic rcse3rch.
86 CHAPTER FrYE
nial f\\lit bodies also add a new layer of tubes each year and may eventually become
almost a metre across, so spore production may reach astronomical numbers,
Bridgeopoms (Oxypon/s) nobilissimus is a rare and threatened species found only
in oldgrowth forests of the Pacific Northwest. United States law now mandates that 240
hectares (600 acres) of forest must remain undisturbed around each known site of this
fungu>, Progress! A basidioma of this species was fonnedy noted in the Guinness Book of
Records as the world's largest fungal fruit body, but it has now been supplanted by a
specimen of Rigidoporus u/mnrius that is still growing actively at teew, England, Po/ypoms
squamosus, the Dryad's saddle, is 'easily recognized by the conspicuous scales on the
upper surface of it> fruit body and its relatively soft texture. Fornes fomenrarius has very
tough, hoof-,haped basidiomata. A few polypores, such as Laeliporus sulphureus, which
produces spectacular orange and yellow fruit bodies on fallen trees, are soft enough when
young to be eaten (conunon name: Chicken-of-the-Woods), though they should be avoided
if the substrate is Eucalyp/!ls. Albmrellus ovinus is another unusual polypore which looks
very like an agaric, grows on the ground, and has soft flesh. The pores are very narrow and
shallow. Heteroba.lidion annosum is highly pathogenic to many conifers, and causes
serious root-rots. I have seen a forest clearing produced by this fungus: it had killed
represematives of fourteen different conifers, many of them introduced species. PipIOporu,~
b,m.!inuJ, on the other hand , kills ouly birch trees. Tmmetes versicolor (often called the
turkey tail) is one of the smaller and most conunon saprobic polypores.
Like many other fungi, polypores often have anamorphs (see Kendrick and Watling
1979), though these may be very inconspicuous. Heterobasidion annosum has a
hyphomycetons anamorph in the genus Spiniger, which forms many conidia synchronously on an apical vesicle. The Ptychogaster anamorph of Trameles fOnTIS altemateanhric conidia (to review conidium deYe\opmcm, return to chapler 4).
Many polypores, e.g. Poria, Po/yporu$, and Ganoderma, may not kill trees, bl.lt Ihey
cause serious decays of both standing and structural timber. These rots cost us many
millions of doll ars every year. The general division here is into brown rots, where only the
cellulose is digested. and white rots, where both ceUl.llose and lignin are metabolized.
Collricia cillnamomea, a centrally stalked, ground-fruiting polyp<Jre. is atypical in being
ectomycorrhizal (see chapter 17)
The generic concepts among thc polypores have changed a lot in recent years as a
resuh of extensive anatomical and enzymological research. and identification is rather
difficult for the amateur. How do we ddine genera in the Polyporaceae?
To the uninitiated, most polYp<Jres tend to appear rather similar - a bracket-shaped
excrescence on a branch or trunk of a tree. Most of the bracket fungi were at one time put
into the genus PolYPoTHs_ No more! Mycologists now recognize almost 100 genera of
bracket fungi. Why has this plethora of names becn imroduced? It is because a 101 of new
microscopic and biochemical characters have been recogni7.ed (which certainly doesn ' t
make life easier for the student). These characteristics arc as follows:
(I) The kind of hyphal system. All fungal fruit bodies arc built up of hyphae, but
those of poly pores can have as many as three different major kinds of interwo,'en hyphae,
and are calkd monomitic, dimitic or trimitic, according to whether they haye one. two or
three major hypha! systems _Monomitic fruit bodies are made up of what we call generatiye hyphae, which arc septate, can be thick- or thin-walled. and mayor may not have
clamps. Mosl such sp<::cies are rebtively soft in texture (e _g., the white cheese polyporc,
Tyromy(u chioneus). Dimitic busidiomala have two hyphal systems, the generative being supplemented by either thick-walled, non-septate skeletal hyphae which give
basidiomata a hard. tough texture (e.g., the artist's conk, Ganoderma applanal"",), or by
thin-wall ed, highly branched binding hyphae (e ,g" the sulphur shelf. LaetiporuJ
j
j
,
,
EUi\IYCOTA,
DlKARYO~'lYCOTA,
BASIDIOl\lYCOTlNA 87
sulphureIIS). Trimitic basidiomata are composed of generalive hyphae. plus skele tal
hyphae, plus binding hyphae (e.g., the turkey lail. Tramell'S versicolor) (Fig. S.6 - afte r
HJ. Hudson, Fungal Biology)
(2) The kinds of digcslin or degrndalh'e enzymcs produM by the fu ngus. Brown
rot fungi digest cellulose bUI IK)llignin. White I"Q( fungi digest lignin. but tend to leave
some cellulose. Mycorrhizal fungi may not degrade wood .11 aIL
(3) The septation of the generative hyphae, In some species they are simple septate, while in olhers they are regularly damped.
(4) The kinds of cystidia produced, and th eir origin.
(S) The reaction of basldios pores with Melzer's reagent (they are amyloid [stain
blue) in BOlldaruwia, dextrinoid [slain brown] in Perenniporia).
(6) The size, shape, ornamen tati on and watls of basidiospores (spores h~ve a
troncate base and a double wall in Ganodenna, are minutely spiny in Ht/trolxuidion).
Perh~ps the best keys a\'ailable are \0 be found in the two-volume NOr/h Americoll
Polypores by Gilbertson and Ryvarden (1986,1987; Funginora. Oslo). but many mush.
10p.m I
Fig. 5.6. Diagram of trlTitic hyphae (after H.~ Hodson, FlIgillBiOOgy, 1986).
(iJ u~PECel
GSIBLIOTECA
8S C HAPTER F IVE
room field guidl:s also contain relatively good co'<ernge of polyporcs, and if you incluck
these persistent (ungi among your collections, you will come home with something inleresting at any time of year - eyen in the depths of winter, or the dri~st month of summ~T_
worse than photocopy the chart on page 90-91 and fi ll in as many of the blanks as )'ou can
before going to the books. or to 3 mushroom identification software program such a~
Matchmaker.
If you 11)' to fi nd :lll of th ose characters in a number of agarics (admilledly a counsel
of perfcction). yoil willieam 3 tremendous amount abom them, In fact. you C:ln usu:llly
idemify them 10 ge nus wi th a sm:lU fraction of those c haracters. lhdugh getti ng the m to
species will probably call for muc h more information. If you read "",hat follows. in which
I introduce you to representatives of si~teen fami lies. you will sec which or the characters
m"ntioncd above arc the most important in se parating them.
a) Family Agruic:lceae. The genus AgariClu (Fig. 5.7 B). to wh ich the supermarkct
mushroom belongs. (I) has a ring. (2) lacks a vulva (that is. it has a partial ,'ei! blll no
universal ve il), (3) its gills are no t attached to the stipe (they arc described as free). and (4)
its spore prinl is dark. Other members of the fami ly such as Ullcoagari"IIS may h:lve spore
prinl~ of different colours. but they are never rusty brown or cinnamon. Leuco(:lgaricus
IIIHltim's. whic h ;s common on law ns. is all aU-while or c re<lmcolollred :lgaric wlth a ri ng.
but no vol va. 11 has an uncomfortable resemblance to th~ deadly poisonous Amauila
I"iro.w, so although it is no! dangerous (edible to some. a gal;tric irritantl00lhcrs). [always
'~ --1
S_ Ap ......
C, Copt/tWS
.-
D: Bolo/us
90 CHAPTER FIVE
~ IDate:'
_ _ _
Habitat notes:
sol t ype
soil pH:_
,._
vegetationalcommunity:_ _ _ __ _ __ _ __
"'=::-::-________
BAS IDIOMAT A:
solitary / in troops / in rings / on ground / on wood / on living tree/other
{describe)~~~~~~~_
(Photograph, draw or preferably paint general view and vertical section of fruil-body)
MACROSCOPIC CHARACTERS
CAP (PILEUS): Diameter: (range) _ - _ em
Shape: convex / bell-shaped / conical/ umbonate / flat / depressed / umbilicate /
(whenmature) _ _
funnel -shaped/cylindrical {when you ng)
Margin: (choose one or more) regular / wavy / upcurved /incurved/ smooth / rough /
furrowed/ striate / split / shaggy! with veil fragments
GILLS (or TU BES or TEETH):
(c hoose as appropriate) remote / fre e / adnate! adnexed / sinuate I decurrent /
crowded/ distant / forked / anastomosing
Easily sep<lrable from the cap-tissue: Yes/No
thick / thin
consistency: brittle / pliable / fleshy / waxy
Colour: when immature
atmaturity_~~-,Number of different giD lengths (series) _ or number of tube layers _
Obvious featuresof ginedge, tube-edge, e.g., colour (esp. if different from rest, i.e,
marginate); outline - smooth I jagged _ _ __ _
STIPE:
central! offcentre! absent / hollow / solid! sluffed (with cottony mycelium) /
tapering upward / equal (not tapering) / rooting
Dimensions: length (range) _ -_ thickness _ - _
Colour: when immature
at maturity' _ _ _~
woody
Surface: fibrillose / dry! viscid/ scaly! smooth
Characters of stipe base (e.g., swollen, rooting, etc.},,______ _ _
~ ~ -_
Jlm
"m
~ U ~P EC C~
~B I 8 L! 'JT E CA
--
92 CHAPTER fi VE
advise people agaiMt making a mcal of it. Up/ora dypeolaria has a scaly cap and a ring.
both typic al of the genus. Macrolepiora rachodes is a much larger, edible species. Again,
note the large cap scales and the conspicuous ring. This species was placed in vpiora
until rentl y. Endoprychum is a scquestr.ue derivath'e of Agaricus. The gill cavity never
opens. and the gills themselves are convoluted and spongy - a totally inappropriate
configuration for dropping spores into the air.
b) Family Amanit:l~~ae. All members of the genus Amaniw (Fig 5.7 A) have (I)
wbite spore prints, and all ha\'e (2) a universal "eil and (3) a partial ,'eiL MOSt therefore
have a ring and a volva at maturity, as in Amanila calyptra . However. these generali zations camouflage ~ lot of vari abi lity, especially in the vol va. (4) The gill tramR is divergent (Fig. 5.7 E). (5) the gills are often. but not always, free (not auachcd to the sti pe). In
some species. e,g., Am(lJlila muscaria, at maturity the vol,'a is reduced 10 scurfy rings
around the base ortbe stipe. Howevcr. the upper part of the univc rsal veil oftcn bn=ah up
into SPOB, warts or patches on the cap as the frui t body cxpands. These are an excellent
due to the prior existence of a univcrsal yeil. and are partic ularly obvious in AmlJnita
mrlscaria. In Amoniuriuiwi Honncrly placed in me genus Atn<1niIOpsis) the ring is essenti31ly absent. The volva is conspicuous. but splits cleanly and so does not leave patches
on the cap.
Becausc some AmaniIG species an:: dcadly poisonous (see ehapter22). the genus has
",,-en made me cover of 'Scientific American: and mushroom huntcrs (especially those
pllnning to eat what they collect) should always make sure they get to the base of the
stipe of any agaric they pick. so they ca n see whether or not there 'S u volva. Th e 'destroying angcl,' AnI/mila l'iIVsa, is pure white. with ring. conspicuous volya and even a wbitc
spore print. But this species. like A.fuim. does nOI have spots (p.ltches of universal veil)
on the cap. Like most other mem bers of the famj!y, thi s lethal species (see chapter 22) is
ectomycorrhi zal. and so [nllts on ly n",~r tree species with whic h it i, symbiotic (see
ch3ptcr 17).
Temrilotn)'Cts. a saprobic genus. is involved in anO(her !tind of mutualistic symbiosis: with mound-building termites in Afri ca and Asi a. a relationship discussed in chaptcr
16. Irs frui t bodies arc al so widely eaten - sec c hapter 18.
c) Family Bolbitiaceae. Basidiornata of the genus Balbi/ius are small and ephemeral. since their tissucs autol yze (sc lf-digesl) at maturity. (I) The surface layer of the cap
(the pileipcllis) is epithelial (the cells are swo!len. and don't appear filamcntous). (2) The
spore print is ochr;rceous to ru sty brown. and (3 ) the spores havc a gcnn pore. Representath~ genera are A,~fOC}'be, Bol/Jilills. and Cl)nocybe. CQ',oc),be fillJris contains deadl)'
am~toxins (sec chapter 22).
In addition to nonnat ag~ricoid species. the Bolbitiaceae has sequestrat~ members
\\ ith b;rsidia thaL don' t shoot their spo re~. Th e genu~ Guslroc)'be st iII looks like an agaric.
but its spores are symmetrically mountcd. its C,IP does not ope n. and it has a habit of
falling over as soon as it comes up. The~c fealllre5 show that it is e'-en now acti,'ely
",\ol\;ng. and that its spores are not wimldispased.
d) Famil)' Copri naceae, This fami ly also has ( I) a pileipellis ofswol1cn cells. but (1)
th: ba~idio$pores are usually black and smooth. and (3) have a genu pore. :Vkmbers of the
ad'~n~d genr.:s Coprinus h:tve weed-like vigour and opportun ism. pionecring tho: exp~vit.:ltion of such habi tats as recently di sturbed ground and dung, The be,t-known species. Cop rimlS COIII(l/US (Fig, 5,6 C). the 'shugg)' man e' or 'shaggy ink cap,' has a co mplex
SCt of physical arrangements and 3. precisely timed o;cquel\Ce of events during spore liberation th~t make it one oftb.- most advanced of all agarics. It is ediblc. but only when young.
"hen thc gills are still white. Later they tum redbrown. then bI~cI::. an d melt away from
bo1!om to top. This behaviour is described in detail in chapte r 8. Capri" us arramClIIll rius
bodies are oftcn s~lurat~d with a purple pigment that is differcnt from the pigments found
in the other groups. Only a few species afe now placed her~. bll\ tb~se indlldc the ",eU
known Cortillari." via!a,e/lS.
(2) Members of Subgenus My.wdllm h<lve a slimy cup and a slimy stipe.
(3) 1o.1embe.s of Subgenus Phiegl1lacillm ha\'e a slimy cap, a <.Iry sfipe and a bulbous
basco
(4) ,\-!em bers of Subgenus Tdamoll;a have a dry. hygrophanous cap. and the ,ap
tissue blackens in KOH.
(5) Members of Subgenus Lepmcybe have n dry, non-hygrophanous cop. and luck
anthraqulnonc pigmcnrs. All de~dly poisonous cortinarii arc membo:rs of this subgenus.
(6) 1o.lembers of Subgenus Dennocybe ha ve dry caps. and are saturated with waler
soluble nnlllrllquinonc pigments - the gills are especially brightly pigmented.
(7) 1o.1embers of Subgenus SI!T;C<!ocybe have dry caps with a silky .urface. and 3rc
non-hyg rophanous. They are often difficu lt to separate from the Tc \amon ias.
Some species of Corlill(lr;u.! subgenus Leprocybe are insidiou$ly poisonous because Ihey contain tfu? lox;n orellanine. You C:ln read the rather horrible details in chapter
22. Many H(/)e/OIr.n species afe tctomycoIThiza1. Gaierilla aumml/ali:; is a smull but
deadly poisonous. amatoxin-containing species Ihat grows on rOUcn \\'ood in Norlh
Amenca. Mo~a species of the ectom ycorrhi zal Inocybe are also poisonous because they
cQntain mtlscarin~ . ond GYlliliopilus specwbiliJ' sometimcs contains the halludnogen
psilocJbln (seechaplcr22). But at ]cast one meml>cr of the Coninarlaceae, RO~;leSCllperat(l,
is a well-known and highly regarded edible (sec ,hapter 18). CrepidO/lls is atypical: il is
one of a fairly small num ber of asymmetrical or fan-shaped agaric~ in which the cap is
laterally attached to Ihe substrate and has liule or no SlipI.'.
94 CHAPTER FIVE
Some members of the Coninariaceae have become sequestrate. The genus
Thaxluvgasler closely resembles Conioorius in many ways, but its cap never expands,
and its gills have become so convoluted thai even if they were 10 be exposed, they cou ld
not successfully drop many spores into the air. I have often found a beautiful purple
species of 17raxterogasrer in the Southern beecb (Norlw/ngus) forests of New Zealand. A
brown species of Tha:rrerogaster Ihat I also found in New Zealand had even lost its
ellternal slipe, and looked rather like a puffball, though a vertical section of the froil body
revealed a central column of stipe tissue - the transformation slill isn't comp lele. The
stal ked_ brown-capped ThaxlerogQSlu pinsue occurs in wes tern Nonh America.
HymenoglU/u is another sequestrate derivative of the Cortinariaceae.
Family Entoloma~. ( I) The spore print is pink to salmon-coloured. and (2)
individual spores are e:ureme1y angular or sometimes longirudina11y ridged; (3) the gills
are altached to the stipe. En/oloma, Nolaneo., Lepfonio. and Cli/opi/us are representative
genera of this mainly terrl colous (grou nd-fruiting) family. Most species of the mycorrhizal g~nus Ellloloma contain gastro-intestinal irritants, and some can cause serious
poisoning. Ellt%ma abortil"llm is a common specics in whlch nonnal fruit bodies are
ofte n accompan ied by lumpy, rounded. misshapen ones. We now know Ihal the latter are
being anackcd by anl)(her agaric, Am/illaria mellea (fricbolomataceae), whose basidia
can be found in them. Theeasily recognized parasitized basidiomata are edible. El1lolo11UJ
has gi"en rise to a sequestrat~ offshoot, Richonitlla, whose basidiospores are angular.
clIactly li ke those of Entaloma, and unerringly reveal the evolutionary origin of this
seq ucm:uc fonn.
g} Family Pluteaceae. (I) The spore print is pink, like that of the Ento lom ataceae.
but (2) the spores are ellipsoidal and smooth, (3) the gills are free (not attached to the
stipe). and (4) the gill tissue or Irama is convergent. The lign icolous (wood-inhabiting)
genus PIUleus has 100 species. of which P/llleus crrvinus may be the most common.
Pcmaps the easiest way to make an unequivocal i<kntification of this species is to squash
a tiny pl~ce of a gill un<kr a coverslip on a 3 x \" glass slide, and eumine it under a
micror.cope. This should reveal what wc call 'comute cystidia,' large cells bearing apical
homlike projections that are unique to the gills of Plllltus ctnoinu.!. They are one of the
excellent reason s that those studying mushrooms should get hold of a microscope if at all
possible: il can sometimes mill identification really easy.
Voll"uriel/a "O/I'lIcea, the straw mushroom. though not nalive to North America. is
the Ixst-known member of the genus. since it is widely cultivated in the Far East (see
chapter 18). NellI time you eat mushrooms 11.1 a Chinese restaurant., see if they belong to
this sptcies - you can easily spot the persistent volva almost enclosing the whole
basidioma. I got some living speci mens of thi s fungus from a mushroom grower in Java,
and later watched them optn and make a profuse pink spore print.
h) Family Hygroplloraceae. (I)The basidia arc long, (2) the spore print is white. and
(3) the gill lrama is div\!rgent or parallel. Species of Hygrocybe. the most common and
conspicuous gellus. have parallel gill trama (Fig. 5.7F). are usually ye llow, orange or red.
and haw a very charactcristic ""uy, tr.mslucent appearance. Species of Hygrophorus. {hc
other ~enus of the family, have divergent gill trama (Fig. 5.7E). often have a partial veil.
and are white. grey or brown. (Divergent gill trama '" Hygrophorus. parallel gill trama '"
H)"groc)"be).
UFPECCB
OBIBLIOTECA
96 CH,\PTER fiVE
10 break up the Tricholomal:lceae into smaller families. II is placed in Ihe recently-proj.l'OSed family Xerulaceae. One of the mysteries attached to the Tricholomataceae is that
despite the very large number of ta",a it encompas$.CS. only twO sequestrate forms alt
known: HJllnmrgiunJ and Podolrydnangium. both of which arose from Lacc<lria. Compare thai with ,"'hal happened in the ne",l family, where sequestrate genera outnumber
those that shoot their spores.
k) Family RU5sulaceae. An almost emirely ectomyrorrhizal group, with flesh that is
distinctively brittle due to the presence of groups of unique. turgid, spherical, thi n-walled
cells called sp haerocys l~. Some ta:>;onomists think these fu ngi are sufficiently different
from other agarics to give them the rank of Ordcr (Russulales).
The spores are also unique in having elaborate omamcm':llion of ridges and warts.
Thisomamenlation. but not the rest of the spore wall, stains darkly (usually blue-blac k) in
~ofel zer's reagent. This is known as the am yloid (or starch-like) reaction. Thc spore print of
the RUS5uiaceae is white. cream or yellow.
The family Russu laceae contains two large epigeous agaric genera, Russula and
Lactarius. and 5i:\: much less common ~cqucstrate derivatives (which don't shoot their
sporcs, and so don ' t give spore printS). Allhough RUSJu/a and Luctarills are similar in
many respectS, they are easily distinguished by the presence of a milky late:>; in LoClariu$
('milky caps'). and by the absence of late:\: and thc bright colour of the pi lcu.~ in mOSl
species of Russula. Russula vircsccns is widely eatCn in Chin:l. though only Rusmla
ruarnpclina. with its shrim p-like flavou r, is widely eaten in ;-':onh Amcrica.
A sectio n through a spec ies of the sequestrate ,'r/acowanirtl re" ea ls a reduced stipe.
and shows that the gills are distorted and clearly not the vertical plates of tissue s~n in
troe Ru ssulas. Nevcrthe less, the spores of Mt.lC()Wallires have amyloid ornamentat io n and
are clea rly rus~ ubc eous . Russula has giv cn rise to IWO s~paratc sequestratc lincs.
M"':owanirn - Gynmom)"ces and Elasm()m)"ce.' - Mancllia. Both invo!\lC an agaricoid and
a hypog~ou s form, and both reta in m icro- amltomic~1 cha racters. like sphaerocysts and
amyloid spore o rnamentation. that give su rprising proof of [heir origin in Ru,uula.
AI! species of Lactarius bleed some ki nd oflale:\: when damaged, givi ng them the ir
common name of mil ky-caps. rhe highly appropriate Latin nJllle also eon"eys this message. The latex unequivocally separates Luctari"s from RUHllla _ Luc/arius dtliciQSUS
broi~s green. but has orange latex which OOl.es OUi wh~n the basidio mu L'i damaJ;ed _The
late", in wcrarius vinace,miftscen.! is especially conce ntrated just above the gills. and
although whi tish wh... n it emerges, becomes yellow after a few secondS.
From Ll,cUlriu.1 have evolved two sequcstmte gcncra: Arc,mgdit /l(l (~ti!l mushroom-like [agoricoid). bllt with a cap that encloses the gills. and n<HI-shooting basidia),
and L-1/<"vIllYccs (wh ich has become hypogeous and tfUme-like). All three genem produce latex.
I) Family Boletaceae. Some mycologists consider this group sufficiently distinct
from the other agaric s \0 meri t its own Order. Boletalcs. I prefer to keep these mu~hroom
li ke organisms wi th in thc Agaricaics (con"eniently r.:d ucing [he number of Order.; you
need to mcmori le). BoletI'S, as they are usually called. afC often large. solid agarics, "'ilh
the h>'me niu m lining 0 laycr of vcni cal fleshy tubi:s that (diag nostically) can be easily
separated from thc nc.'ih of the ca p. The often swollen stipe freq uentl y has nct-like or
" 'arty ornamentation (Fig. 5.7 D). and somdimes a pan ial veil. The sporc~ are elongated.
and yellow ish-brown in mass. The re arc no cla mp connections 011 the hyph ae. Most
boletes are t<:tomycorrhizal.
Bo/n'f$ tdu/iJ- is the famous edible 'Steinpilz' or 'ccp' of Europe, and fonuna[el y
also occurs in Nonh America. [t is cither a rather variable spedes. or more probably a
Eli,VIYCOTA: DlKARYOMYCOTA:
BASlDlo:\rYCOT I~A
')7
spc!cies /;ompkx. Many other boletes are also eatcn. though specie, with ornnge or reddish pore-muuths, like thuse of S o/ellis frosti i, -SO/eIllS sa/anas. and many other speci~>.
mUSt be avoided. Those whose flesh turns blue when bru ised should also tu~ted with
caution_ Ty/opi/us fel/ells is visually spectacular. but gastronomically a bust. It often
occurs in liUge numbers under conifers. raising the expt:Clat;Ons of the onlooker. but
hopes iUe dashed when the pink tube mouths are secn. and we realize that we ha\'c found
the biuer boletc.'
The blue-staining Gasrrobo/e/'IS is alleged to be a sequestrate deriv;:u he of 8 01 etu~. though it is SOmetimes placed in the Xerocomac~a~. Suil/us spraguei demonstrak s
the panial veil that is found in many species of this genus, as does SuiIllIS gre.-il/ei. Mony
species of Suillus alSO ha,"e viscid caps. TnmcocQ/llmella . which has a "estigial stipe. and
Rhitopogon. whic h does nut, arc seq uestrate. hypogeous offshoots of SlIilIl'S. Like the
pare nt ge nus. th ey are important e<:tomycorrh ilal panner~ o f COnifers in west~m North
America. RhitopogQn porksii. a very commOn western species. has a spongy. lacunosc
basidioma. The spores. howeycr. ~ just like those of 11 Suillus. and DNA studies ha,'e
established that RlrhfJpogou is very closely related to S"i/l"s .
m) Famil y Gornphidiaccae. This mycorrhilul family has (I) viscid caps. (2) decurrent gills (not tubes). (3) a dark grey to brown ish-black spon: prin t und (4) microscopic
struclllre that shows it is closely related to the Bolela<:eac:. Gomphidilts haS \\ hitc flesh;
that of ChfrJQgompJms i5 pin!:: to orange. Sequestrnte fOIms have arisen from both gcnern.
This family is common in western ~onh America, much Ie,s so in the ~a5t.
n) family Gyrodontaceae. This family superficially resembles the
ll ol~I;lceac.
bUI
(I) the lubes are shallow and not easily detached: (2) thc spore print is yellowish or
olivaceoos brown: (3) the spores are subgloOOsc to ellipsoid: and (4) the h ~phae have
clamp conne<:tions. Fuscoboferinus. Boferinm, Gyrodon and G}"ropomf are represema
Ilve ge nera.
0) Family Paxillaceae. Like the Gom phidiaceae. this mycorrhizol f~mily II) has
gills. nOlIllI1e-S. but (2) the gills are easily separated from the flesh of the cap. (3) The gi n
trama is divergent and gelalini1.ed. (4) The spore print is brown or "hite. and (5) the spore~
are ovoid to elli(}Soid. The common species. Paxill/l.~ ""'o/mus, i~ a s)' mbiom of cQnifer;.
and is easi ly rccogni1.ed by it, inrolled cap margin. its decurren t gi!l$ and the brown stain,
th at appear after it has b.:en handled. Hygmpltoropsis alium/i(lC(I is kn own as the '1~1bc
ch:mtcrclle. It has conspicuously forking gills.
In 1989 Canada joined the many countries that have issued stamps depicting
macrofungi. producing hand some (if slightly stylized) stamps of CI(lnt/ino{J.~is fusiform;'.
flo/elUs mirabi/is, Caltllwrel/'lS cinnabarimlS lInd .Morchella esculmra. (I ha\"~ been
trying to get th e Canadian pOSt oflice to bring out some Stamps on moulds. thus far
without success. despitc the important roles tho::se fungi playas producers of penidllin.
griseofulvin. cyclospori ne. an ato~in. etc.)
98 CHAPTER FIVE
The foregoing is no more than a gesture sketch of the world of the agarics_ If you
want to learn more about what many people consider the most fascinating of all fungi. you
must buy or borrow one of the field guides listed under 'Further Reading' at the end of this
chapter. The large tome by Ren~ Pomerleau has all the minutiae a Northeasterner needs
(though the colour illustrations are poor). but the pocket-sized Audubon Guide by Lincoff.
though less detailed. covers the whole continent and can go anywhere with you. "The
larger-fannal Mushrooms of North Amuica by Roger Phillips. published in 1991, h.;J.s
over 1,000 colour photographs. and includes many more species of. for eump!e,
Coninarius (93}.Amanita (41). Lacfarius (64) and Russula (8 I). than other guides. Mush
rooms DemYSlified by Arora, though oriented toward western North America, is a mine of
useful and often amusing information for all mushroom-fanciers; it also covers a wide
range of taJla (even dealing with many sequeStrate forms). The Ntw Savory lVild Mush
room has CllcclIent colour photographs. hul is mainly uscfullo those in !he Pacific Nonhwest. The latest addition 10 these field guides is Fungi of Easum Canada and rhl!- NonhI!astem United Slall!S by George Barron. It covers over 600 species of fungi and is illustrated with more than 650 photographs.
In addition to agaric s, these books cover the more conspicuous Gasteromycetes.
Ascomycetes and Aphyl1ophorales. Some of the larger and more difficult genera caU for
separate keys, and those [0 the northeastern species of Russula by Kibby and FallO are
excellent eumples. "Malclunaker" is a new. profusely illustrated synoptic key [0 2.000
mushrooms on CD-ROM (see Bibliography at the end of this chapter).
Series Gasteromycetes
Althoogh many kinds of sequestrate fuogi can be traced to their agaricoid origin.
many others probably evolved so long ago that i[ is no longer possible to trace their
ancestr), with any degree of certainly. For these. which we call Gasteromy~etes. we ha\'e
erC(;ted special Orders, based on the mode of passive spore dispersal iDlO which mey have
evol ved. I think you will agree that if these groups have any agaric ancestry, it is well
concealed. All have non-shooting holobasidia.
Umnoperdon. a minute floating g~teromyccte. occurs in woodland ponds. Its basidia are produced inside a tiny, entirely closed. hollow basidioma. so there II.w ld be no
point in the spores being forcibly silO! from the basid ium. The non-shQO{ing nature of the
basidium is apparent from the symmetrical way in which me spores are mounted on the
sterigmata (remcmber that typical shooting basidia have their spores asymmetrically
mounted as an integral part ohhe shooting me~hanism)_ Fig. 5.8 AE shows non.shooting
basidia of a range of gasteromycetes.
(5) Order Sclerodennatales: I I genera. 38 species. The 'earthballs' (as opposed 10
puffballs'). Here the spore mass (gleba) has small spore-rontaining cavities (locul!1S)
wilh no real hymenium, ,md is powdery at maturity. with no true stipe or capillitia!
thread.,. In the com mon genus Sclcrodenn{1 the spore mass is blackish at maturity. and the
basidioma has no ostiole.
The separate locules are clearly visible in Pisolirhus linC/orills (Fig. 5.8 F). which is
perhaps the mosI famous of all ectomycorrhiz.al fungi, since il helpscooifers andeucal)'ptS
[0 thrive on panicularly unfavourable si[cs. It has been the subject of many research
projects. as you will read in chap[cr 17. I have found this fungus fruiting at various places
in North America,Australia and South Africa. The basidiomata are often lumpy and almost
shopeless. and it is sometimes called the ugliest fungus in the world. despite its cllcellent
qualities as a mycorrhizal symbiont. Mature fruit bodies hove becn collected as a source
of spore inoculum aod. as I have seen, can also be used in a hot-weather version of a
snowball fight.
..
~ UFPI:C CtJ
~ BIBLl 0 TE CA
B. CHI/rum
'.r
A. H~""g..
( ........... tal.
eo.u/Wlaco"'l
c SeW_ _
,,
----;T~,."'"
.....
,..::-:l" ',:'
. '.-:
\~--'
,,!..."
~"
"'"~."y''''--'',,--
~<
",'"
Fig. 5.8 HoIobasidom)'l":etes which lack active spore <ischarge. A: Agaticaies; ~H,t L)'I":operdales;
C,F: Sderodermalales; D,G: T~ostomalales; E: Phallales.
(7) Order Tulostomatal('s: 9 genera and 75 species of smlked puffballs. with dry.
powdery gleba. TU/o$toma looks a bit like a rabbit pell~t on a stal k, but has a bu ill-in
ostiole (Fig. 5.8 G). Cu/os/omQ has a ge latinous stipe and a most peculiar stell:lt.: ostiolc
rimmed with red pigment-the only puffball that WCQP; lipstick. I first saw this fungus in
New Zealand. but have found si milar species in the Carolinas.
(8) Order L~'cop('rdale5 : 26 genera. 260 species. These are the common and wellknown pu rtbaJl s and eanhs tars, with powdery glebas. Though most are saprob ic in soil
and on rotten wood, some may be ectomycOlThi7.al. In contrast to the Sderodermatales.
the glebal ,avilies are lined by a hymenium wh en young. The mature spore mass is
usu:llly kh:lki---coloured :lnd milled with capi11itial filaments. The peridium has [\\-'0 or
more l:lyers. and usually develop> an apical Qstiole. The papery inncr peridium can be
compressed by raindrops. expelling air and spores Ihrou gh the OSliole. L)"CQptrdon (Fig.
5.8 H) is the best-known genus, to which most common puffballs ~Iong. ul/Ige rm rlnnia
(fonncrly Coh'(lIia ) gig(lrIleo is thc giant puftball. Before the spore mass (g leb:l) malures.
and while tile imerior looks like white II\aM;hmaUow. thi s fungus is often collected :lnd
emen. A C:lnadial1 specimen collected in 1987 held the world record I1l1til 2000 for the
largest edible funglls - 2.6-t metres in circumfercllCe and weighing 22 kg.
GeaSlmm species (Fig. 5. 8 l) are known as carthstars. In this genus the thick OUler
pcridium spli ts stellately as it dries out. and the Sl:gments fold back in order to raise the
gl eba. in its inner. papery pcridium, above the dC:ld leaves that might otherwi se preve nt
the puffball l1lechanism fTom wo rking.
(9) Order Nidulariales: 5 genera, 60 species. These are the bird's nest fun gi. in
wh kh the ba~idioma has be:cn modified to be<;;ome a splashcup spore dipersal mecha
ni sm. The basidiospore mass. or gl eba, is divided up among ;.everal indiv idu al 'egg,'
(morc formally. pcridioles). The kineti c energy of rnindrops is focused :lnd rcnttted by
the funnelshaped b:lsidioma. and the rebounding water carri es the pcridiolc~ with it.
Crw;ibil/ulli. Cyoliws. Nidu/(1 ;lnu Nidillaria arc represcntotive genera.
In C'ymilus (Fig. 5.9 A) the pcridioles nre atlll.chcd to the wull of the basidio m~ by a
long thread. most of wh ich is folded up inside the stipe of the peridio lc. When the peridio1c
is ~plashed out. the thread unwinds rapidly. mtil ing behind. At the e nd of the thread is a
sticky blob which acts to anchor the pcridi o1c to wholever it strikes.
(I OJ Orde r Phallo. lcs: 25 genern.45 species. These :lre the st inkhom~ ..... hose spore,
are di~pcfSed by nni mal vectors. The gkba is slimy and re all y do.::s smcll bad, so it auraet,
flies .... hieh wallow in the mess, eating some spores and carrying others away on their fut.
Althou gh two well-known ~tinkhoms. representing the ge nera Ph(ll/II.! nn d Milfillllol. are
fairl ~ common in NonhAmctica. the most bizorre genera are commoner in Austrol:lsia and
the tTOpics. All stinl.:hom~ de~"Clop in a gd:Uinous matrill wtthin a membranous 'egg shdl" or peridiu nl. but when thcy 'h3tch: their mature fruit bodies can be: strikingly
different.
Pll<IllljS (Fig. 5.9 D) and M ul;,W$ (Fig. 5.9 B) hnve the simplest morphology: the
stipe elonsatcs rnpidly, can:ying their respectively th imble-shaped and conical heads
(of\~n called receptacl es). into lhe air. whcr~ they can relea~c Iheir effiuviu m and :lttraet
thc nies more easily. Europe:lns h3~'C sufficient knowledge of these fungi 10 enjoy cartoon; of lh~m. Nonh Ame ric ans. 10 whom th.:y nre les, f~miliar. look al such artwork
a~kance .
The genus Dict)"lIphora (whose na me means 'nel-beare r') docs ind~ed have a vi sually striking lacy skirt h:lnging below Ihe n:ceptac1e. My guess is that this is 3 landing
platfonn for flies qucuing up for a sample of gleba. InAni/umlS (Fig. 5.9 C). the gleba is al
fi ~l central in the egg. LIter the spore mass covers the inner side of seve ral IX:topus-Jike
EUI\'1 YC OTt\: DlKA RYO;\ IY COT A: BAS lD IO;\ IYC OTL'iA 101
arms. In CIllIhru$ (Fig. 5.9 F) the arms remain fused. and in some species ronn an open
lanice. again with the gleba on the inside. Astroi (Fig. 5.9 E) is ~ urely one of the mo,t
numboy~nt members of a truly spectacular Order. Bright orange-red extensions of its
receptacle radiale OUt like the petals of a flower. and also look rather like meat, providing
a d iverse range of visual as well as olfactory clues to would-be vectors, which can be
drawn from among the meat-ealcrs (e.g. wasps). the nect~r-eaters (e.g. butterflies) and the
visitors to excreta. H)"sierangiwn is hypogeous, so the gelatinous layer found in most
Phallales is nOt welldeveloped, and there is no dramatic ruptu re of the peridium at maturity. But the affinities of this ~lusive sequestrate genus with the otherwi.o;e e;(hibitionis.
tic Phallalcs are accepted.
.
. ....
B Mul/I>UJ
4n!lwws
CI~ lhtu~
Class Phragmobasidiomycetes
This group contains four Orders: Tremellales, Auricularialcs. Scptobasidiales and
Tulasndlales, which ali have basidia subdivided by septa.
I) Order Tremell ales: TIlese are jelly fungi generally found on dead wood. Long
considered harmless saprobes, they have re.:ently been unmasked as vicious mycoparasites
of other woodinhabiting fungi. The basidia (Fig. 5.iOA) aR: often described as 'erueiately
septate: being \'Crtically divided into four compartments. Each of these develops a long
outgrowth that extends to the surlace of the: gelatinous matrix and produces a ballistospore.
The most ro:ent interpretation of these 'basidia' is that the \'ertical septation separates the
nuclei into four cells that can be called basidiospores, and that the long 'epibasidia'
which grow up to the surface of the jelly are actually germ tubes. This would mean that the
'basidiospores' arc actually secondary spores, results of a form of 'germination by repetition: a phenomenon so common in the phragmobas idiomycetes that it is often used as a
diagnostic character.
The basidiomataofTremel/a areoften irregularly shaped (fig. 5. lOA). Otherrepresent:u;\"e genera are Ph/ogioris, the rather attractive scoop-shaped 'apricot jelly,' and
Tremel/adon. But in Pseudohydnum, convergent evolution has produced a form reminiscent of certain holobasid iomycetes. Pseudohydnum has its hymenium on downward
pointing teeth like those of the Hydnaceae (AphyIJophorales). but the rubbery tel<.ture of
its b~idiotna. and the cruciately septate basidia, give the game away - it is undoubtedly
a membt:r of the Tremellales.
(2) Order Au ricula ria les: j genera. 16 species. Members of this Ordcr are easi ly
identified by their gelatinous. ear- like basidiomata arising from wood (Fig. S.IO B). The
e longated basidia an:: di vided by transverse septa. and each of the four compartments
dC"clops a slender tubular outgrowth that produces a basidiospore when it reaches the
surface of the gelatinous matrix. The Chinese call members of the genus Aurit'ularia
'cloud ears' or 'tree ears,' and use them in cooking. largely fortheir interesting texture. We
have recently discovercd that th~ y comain a substance which reduces the clotting propensities of blood. and so may offer some protection against heart attacks.
(3) Order S~ pto hasldiales: 2 genera, 175 species. mostly in &pwbasidium (Fig.
5.11 A). This Order also has transverse ly septate basidia, but its basidiomat3 are 110t
gelatinous. and it parasitizes scale insects. These do not die. but become sterile. They are
buri.-d in a weft of fungal hyphae that produces basidia on its surface and provides shelter
for other healthy scales.
(~)
Order Tul as nellales: This small Order is interesting to us mostly because it has
yet another variation on lhe phragmobasidium. In TU/(Isnel/(I the four deve loping sterig
mata swell up and each becomes separated from the body of the basidium by a secondary
septu~ (Fig. 5.11 B)
Class Teliomycetss
1.9. orrf'li}-
This group comprises two distantly related Orders, Uredinales and Ustilaginales,
which produce no basidiomata and have simple septal pores with pulleywhcd occlusions
(Fig, 5.1 D) rather than !he doliporcs chilftlCterislic of most other basidiomycetes.
(I) Order Uredinalcs: 164 genera, 7.000 species (3,000 in one genus - Puccinia) .
The rust fungi are all obligately biotrophic on vascu lar plants and often have very narrow
host ranges. being restricted 10 a single family. a single genus, or c,'cn a single species.
Although they have obviously ~volved with !heir OOslS for millions of years and don't
usually kill them. rust fungi can severely reduce yields of our domesticated plants, par
ticularly the cereals on which wc are so dependent. The rust fungi produce basidia from
overwintering spores (teliospores), so they don't form basidiomata. But they do produce
no fewer than five different kinds of spore, each specialized for a particular step or phase
in the life cycle, And they often alternate between two hoStS , which lend to be from
tu}(onomically distant groups, This is important information, because as you will sce in
chapter 12. our efforts to control many diseases of our food crops depend on our knowl
_m
.,...
. . -\1
Fig, 5, 10
Phragmoba5kliom~etes,
A: Tremelales; 6: miculariales.
'u"".
?-":i'l,
'.''?" - ."",,,,...
fj::!; :::
~
- --
PlicciniG graminiJ subspecies Ir/tici. the fungus causing black Stem ruSt of wheat ,
can e)(emplify mllcFOCyclic, heteroecio us rust:; (those produci ng all five spore fonn> and
moving back and forward between two differ"'nt hostS). The different stages of the li fe
c>'cle are shown in Fi g. 5.12. Basidiospores, ....-hi eh are of + an d - m ari ng types. land on a
young leaf of barberry (BtrberiJ) in spring. and initialc localized monokaryOlic infectio ns. The hyphae arc intercellul ar. but they seo d haustoria into host cells to absorb food_
Soon. these monokaryotic mycelia develop tiny flask-shaped spe rmagoniA (stage 0) in
the upper lay ers of the lea f. They produce only small brown spots and don ' t do any
si gnificant damage to the barberry. Each sperm~gon;um forms innumerable liny spcrm D.tla which ooze OU I in a sweet-smelling neclllJ. A tuft of rec:tpth t hr ph ne also grows out
from the oeck of each spennagonium. Insects are attracted by the nectar. amI walk or fly
from o ne ~penn agonium to another. unwittingly transferring spe-rmatia o f each mating
type 10 recepl;~'e hyph ae of the Olher type. This process, wh ich is somewhat analogous to
pollination. initiates Ihe di karyoph ase . The dikaryotilation spreads to the lower ~urfacc
,.
o U$tila;o
E rWe!l.l
a TulUMlla
...,,,,,<atyobC
_
....a>
5";0 IV
5~ .O
Ustilagina lcs
I) Tdiospores terminal
51erigm:ua
3) Spcrmagonia produced ( sex
IN)!
on
organs )
6) Oblig:uely biotrophie
7)
lnfection~
8) To:>liospores in telial
unspcdfic
son, location
tWO
CQrnpatible cells
b) Family Tilletiaceae. Here, events are phys ically more compressed: karyogamy.
rn.:iosis and mitosis all happen inside the leliospore. Wh ~n this germinates, the resulting
basid ium produces a cl uster o f s lender. parallel basidiosporcs from ils apo:>x (Fig. 5.11 El
These soo n copu lmc in pairs to rc~!O rc tho:> dikaryon. Tillnia caries . the cause of ' bunt' or
s:inkin g smut of wheat. is Just as im port ant an eco nomi c problem as ste m rust. btc~use il
has so f~r proved impossible to breed strnins of wheat resistant to this fungus.
No w I' ll wrap this long chapter up wi th a key to the more common Orders ofbasidiomycet~s . If you ' ll read through it. it will hel p you to rec~ p the major characte ristics I
h~ve shown you in the te xt ao.d pictures above.
KEYTO SQ;\IE CQ:\Ii\ ION ORDERS OF BASIDIO;\IYCETES
No basidioma: basidia solitary (free),
o r On ind i"idual hy phae .............................. ......... (see yeasts)
No bnsidiomu: basi di a arisi ng fro m
restio.g sporc..~ (class Te liomycelcs) ...................... 2
;\0 basid ioma: basidia in a layer On
sl,Irfa<:e of host plan t ........_-. .................................. E:l:obasid ialcs
B ~si dioma prod l.lced .. .... ... ...... ..... ,.. .......... ...... .... 3
3
3
4
6
6
7
7
8
8
9
9
10
10
II
12
12
.. ............ Lycoperdales
............. Tulostomatales
UFPE.CCII
OSIBLIOTECA
Everyo ne knows the word 'yeast: but vcry few people have m(II;1I idea what a yeast
really I$. and fewer still are aware thaI the name is applied [0 organ iSIll5 of very different
origins. You arc about to join Ihat eli te group. The word 'yeasf has been wid ely illt~r
preted in terms of morphology alone. but as you will see. th~lt is si mplLuic. and 1 fOnTIS are
develo~ in many di fferent groups of fungi, from Zy~omycele5 to BlISid iomycclcs (with
r... pre~ en tativc fo rms in all three major subgroups - Holobasidiomyceles ,
Phragmobasidiomycetcs and Teliomycetes). Cu rrently. about 700 species of yeast ~ are
knov.-n. distributed IImong about 100 genera.
Y~ast> arc moslly (b ut not all) unicellular orga nism s. some Qf which arc useful to us
bec;\u,e they 'r~i5C' bre:ld, put the alcohol in beer (left) and wine . and are~, high-protein
food supplement as ..... ell a~ a rich source o f B vitamins. But the re is much more to them
than th;).t. ;md th~y have a darker side: some are implicated in food spoi lage. A few yeasts.
such a5. Candida Illbicans (Fig. 6.2 C). cause potcntiall y s('rious disease.~ of humans .
i\!lh<.Juh )e~sts;).rc still oft~n characterited as si ngle -celled fungi that \11.1 not produce
hyphae. C(Jndida und qu ite a few o ther yeaS ts cl early produce hyph ae. as well as what we
call 'yeast ' cellS. The yeasl cells of Candid" are !>.asicall y ooni\lia. and develop in what we
"o uid call bh ~ticacropctal' branche\l chai ns.
B<'tause o f their economic and med ical importance. there was a need to identify
micro>copitally simil:tr but physiologic~lly different yeast~. So zymologim (yeast C;<p.?rts) ~cveloped a ta>;.onom ic scheme based on physiological lests such as the ability o f
)CaSb to ferment or assimilate D. "ariety of sugars, thei r nitrogen and " itumin requirements. antibiotic resistan!;e. elC. More recently. sophisti cat<,d tcchniques stich as magnet ic r~son ance analysis o f ce ll wall compone nts. elec trophoretic enlymc analysis . eyto
chrome ~pectrophotometric analy~is. serologic:!l tests. DNA reassociation. and O;":A!>.aM:
compo 'itio n. have all ix:cn pressed into .>ervice in the <;e ar~h fnr u~cfu l t~>;.ono rn i c cl1 aw~
ters in YCJSIl;.
One as.sumption underlying much of this activity wa ~ th~t yeaSts had relativdy few
morph olog ical characters to wurk on. It W~<; thought that yeil~ts reproduced by one o f two
proce~,es. which " <'re s.implistica ll y called 'budding or ' fission: But yeasts do in fact
exhibit morphologica] and d-:ve]opmcntal f<'atures whosc significance hus o oly rece ntly
bee n appre ciated. Th ese chawc ters cven offer clu ~s to !h~ un de rlY1fl;,! phylogenetic
di'"Crsit~ or the group. We now think of <Issimilati,e yellSt cells as essentially conid ia. and
have identified sc"nal diff~re nt kiTld" llf co nidi ogcncsis amo ng thcm. as Fig 6.1 .~ h ows.
:>.bny yeast s (about 600 species in 22 genera) nc"er d.:vdop a telcomorph. and aTe es~n
tially conidial fungi.
,\l u ltiblCr~1 budding )e asts bud from many d iftercnt points on the cell. produci ng
only one daught er cell (conidium) from each site. and 1<'~l'ing many scars (Sllccharomy-
112
YEASTS' 113
ce" -
Fig 6.1 A), What havc commonly been called apiculate , bipolar buddin g ycnsts
have lon g cells Ihtu bud re~aledly f.om each end. c~tending percuuently in the proc~s.s
(e.g. Sacclraromycodel - Fig, 6.1 C. lower di~gram). Cells or what ha\'e been inaccuTOtely tcrmed ' fission' yeastS also extcnd percurrenlly. but 011 a much broader base (e.g.
Sci1izCJS(lcchar<)nl),Ctl - Fig. 6.1 C. upper diagram), Sume hyphal yea.m produce !hallienrthric conidia (Geolrichmn - Fig. 6.1 E). 3a~idiom}ce!oos yeasts may be blaslie-s)'mpodial (Cryptococcus - Fig, 6.1 B) or bla~tic-phial idic (Rhodll/onda :md Sporob%mycts
- Fig. 6.1 D). Somc of these unicel]ular nnamorplls can switch in to the tekom orphic
mode , and produce stnlcrures that would appear 10 place them among the Dikary ornycotn.
though sine<: sex invoh'es fusion of individual cells to form a zygote. thcre is no d ikaryon .
Yeast phases of smu l fungi do, howeyer. have a dikaryopha sc.
Some yeasts form endogenous me iospores inside meiosp orUlIg ia Ihul arc
karyologietilly exactly compal'1lble with asci (scverol such meio~porangia, most comaining foor spores. are visible in Fig. 6.2 A). Ihoogh the wall chemistry (a good indicator of
OCDC iiDCD
'CO~J-)
v ~E?
(~
)::l
114 C HAPTER S IX
UI'PE.CC<l
@818'.!!)TECA
phylogeny) is somewhat different from that of Ascomycetes, and they are never produced
on or in a fruit body (ascoma).
The ability of some yeasts to produce hyphae is emphasized in Fig. 6.2.
S(lccharomycopsis (Fig. 6.2 A) produces Candida anamorpbs. Dipoda.lcus (Fig. 6.2 B)
produces a Geotric!lIlm anamol1lh. shown here beside the meiosporangium.
Other yeasts are Basidiomycetes. Some of these (e.g. Spvrob%mycu - Fig. 6.2 F)
even produce exogenous spores borne asynunctrically on poinled outgrowths ofthe cell:
these spores are forcibly discharged, and the mechanism involved is obviously that of the
basidium. Some, which produce hyphae, even make clamp connections (Fig. 6.2 D).
Others, such as Cryptococcus, produce blastic-phialidic (Fig.6.l D - ccntre) or blasticsympodial (Fig. 6. I B) conidia.
Tooutlinc the full taxonomic diversity of yeasts. I must also add that when members
of the Ustilaginales (Tcliomycetes) or Taphril\3les (Ascomycetes) are grown in axenic
culture, they become yeast-like. Basidios~ of Tremdlales germinate 10 produce a
haploid yeast phase. Sever.u fungal pathogens of humans. while filamentous in culture.
ace yeast- like when growing inside 1.1$ (e.g. HiSlOpiasm(l capsula/um . Blastomyces
demtati/idis - see chapter 23). Finally, a few fu ngi such as Mucor roJlxii (Zygomycetes)
can be changed from a hyphal to a yeast-like morphology. oc vice versa. by varying levels
of carbon dioxide Of" of various nutrients.
So 'yeast' morphology is sometimes a response to environmental factors such as
osmotic stress. a response that has evolved many times in different groups (just as the
lichenization process [chapter 7] and the change from agaric to sequestrate derivative
[chapter 51 have occurred many times). As a final twist to this tale, mycologists have
discovercd that some fungi which consistently produce hyphae (e.g. Arlh f(xucus, AxhbY(J,
Candida, Crtbrolhuium , Dipodascus, Erem olhuium. Gu illiulllonditlla.
S(lcclulromycopsix). are closely related to the unicellular yeasts. This conclusion is based
on four kind s of evidence: ( I) even in hyphal fomt>. there is n~ver a dikaryophase; (2)
they produce a~cus-like meiosporangi~ in isolation, or singly, in clusters. Or in chains, on
individuJI somatic hyphae. but never in any ):;jnd of ascoma; (2) their cell walls contain
l ~ss chitin and more mannan than those of regular ascomycetes; (3) some of them produce
yeast-like anamol1lhs; (4) some ofthem have many extremely narrow mlc ropores piere
ing each septu m. rather than a single central pore. These features. among others. argue for
the recognition of the 'ascus'-fonning yeasts as a group distinct from the ascomycctes
pro~r. J (reat them as a separate class.
Class Saccharomycctcs. Representative genera are DipodascHs with GeOfrichwl1
anamorphs. Hallstniosporu with Kloeckera anamol1lhs. and Sacchorom)'copsis with C(Jn
dida anamorphs. CUlldida a/hicuns. ",hieh produces aerial hyphae (fig. 6.2 C). and whose
teloomol1lh (if any exists) is unknown, causes ca ndidiasis. a disease ",'hich affects mucouS
membranes in various parts of the body. or may evcn become systemic. This is more ful1y
discussed in chapter 23.
The Geo/richum anamorph of Dipod<lsCliS produces hyphae whi ch break up into
thaUic-arthric conidia. but since this is a yeast. there arc subtle differe nces between th is
a nd, for e.>;amplc, the many basidiomycetous anamorphs that abo produce thaUie-anhric
conidia. Wall chemistry is diffe~nt and the septa have many micropores rather than the
single. central septal pore of most othe r hyphal fungi.
Class Holob:l~idiom ycetes (in part). A second. very different group of yeasts have
chitinmannan walls which also contain some xylose or fucose (both absent from the
Saccharomycetes). The anamorpbs in this group also lIave two modes of con idiogenesis.
Mosl are blaslie-sympodiaJ (e.g. the Cf)ptoco<:cus anamorphs of Filobasfdiellu). Others
YEASTS 11 5
are blastic-phialidic (e.g. Cryptococcus anamorphs of Filobruidillm). The teleomorphs,
where these are known. produce clamp connections and basidium-like strucrures. The
holomorphs are placed in the family Filobasidiaceae, and reg:ll'ded as belonging to the
holobasidiomycetous order Aphyllophorales. Cryptococcus lleojOntlOIlS, the anamorph
of Filobosidiello Ileofomums, causes a potentially serious lung disease, cryplococcosis,
which is further discussed in chapter 23. Some other genera, such as Pha/fia and Bul/era,
are known only as anamorpbs. And although the tdcomorph of Trichosporon. if one
exists. is unknown, this anamorphic yeast probably belongs here, because iUl hyphae
have dolipore septa (Fig. 6.2 E). As the diagram shows. this genus forms conidia
sympodially, and the hyphae also tend to break up into thallic-arthrk conidia.
Clllss Thliomycetes (in part). The third group are called the red yeasts, because they
cootain carOtenoid.> (though some spedes of Cryptococcus and Phaffia al so produce
these compounds). Rhod%ru/a, which produces pinkish or reddish colonies, forms blaslic-phialidic conidia from the attenuated ends of the yeast cells. SptJrobolomyce.t cells
(Fig. 6.2 F) devclop sterigmata from which asymmetrically borne s?Ores are forcibly
ejected. A se ries of such balliSlospores is formed by sympodiaJ extension of the sterigma.
Note that although the spore-shooting technique being employed here is that of the
basidium. the spores being formed are asexual mitospOles (conidia). Yeasts of this group
sometimes produce a teleomorph: a chlamydospore-like teliospore, which genninalcs to
--
,hlr"'ortl>rlc """"""' m
II"
E:
TrlctlQ_'~
F.
S~,.j>(r l omyc..
FIS. 6.2 Some I.IlI.ISUiII ~asts. AC: Saccharornycetes; D.E: HoIobasi<ion:etes; F: Teiomycetes.
HdomOlllh
An:lInorph
Dipodascaceae
Dipoda.scus
Gtotrich/lm
A.>COideaccae
5accl1(! rom)"copsis
Candida
Soccharom)"cet~ae
Succ1raromyct..
Torulopsis
Filobas idiaeeae
Filob(I!Jidimll
Cryptococcus
Filobasidiaceac
Filo b(lsididl(l
Cryp l(JCOccus
Aesso.lporOIi
SporolMll)l>!yas
Ustilaginaks
Sporidiobolll~
SpIJrobl>lomyces
Ustilaginales
Rhodosporidiw/I
Rlrodo/lJnria
i\lajor group
SacCh llTOm}cetes
Endom)cetales
Holoh:lSidiomycctCli
Aphyllophorales
Tdiomycctcs
Bnam.
Kurtzman, c.P. and 1.W. Fell (Eds.) (1997) The Yeasts -9 Ta'\:onomic S tudy. 4th Edn.
Elsevier Stience Inc., New York andAmSlerdnm. fA comprchen,i\'e treatment by 38
authors]
Sumson, R.A ., E,S. van Rec:nen- Hoekstra (wi th 12 others) (1988) In trodu ction 10 Food Borne Fungi. 3rd Edn. Centraalbureau voor Schimmeicullures, 8 :1am.
Skinner, F.A., S.M. Passmore and R.R. Davenport (Eds.) (1980) Biology a nd Acthilles
of Yeasts. Academic Press, New York.
UFPECCB
i!5BIBLIOTECA
Habitats
Lichens are among the toughes t macroscopic organisms: What other group can
grow on bare roc k:, in exposed silUations subjected 10 extremes of temperature. radiat ion
and desiccation, from hot deserts to the arctic, from the seashore to the highest mou ntains
(lichens are found at over 7,000 metres on Mount Everest)? As you can sec on the CDROM versiOn of thi s IC.tl, the rocky cliffs along the nonh shore of Lake Superior are
covered with lichens. So is the ground in tbe forest near Scheffcrville in northern Quebec.
So is the bark of a tree at Dingo Beach in Quecnsbnd, Australia. The intertidal lOne is
another tough neighbou rhood, and the rocks just above high tide are ex posed to desiccation, salt sproy, rain, sun and frost, often in rapid succession. Yet many rocks along the east
and WC:>I cOOSLSofNorth America are cooted with a black lichen called Vurucaria. Simple
lichen associations also grow beneath the surfaces of rocks in the Nam ib desert of south
em Afric a. Thcy wi!! grow wherever the air is clean.
Alga(e)
W11 at is thc lichens' secret? They are dual organis ms. Each lichen combines the
talents and strengths of a fungus (the mycohi ont) with those o f at Ieasl one kind of alga
(the phycobiont). The fungus obtains water and minerals. builds a complex thallus. and
produces sexual and asexual reproductive st ructures. TIle alga lives a nd photosynthe
si ~es within the fun gal thall us, and although algae constitute only 5- 10% of the total
biomass of lichens, usu:llly conce ntrated in 0. zone just below the upper surface of the
thallus. they supply energyrich carbon compounds to the entire organism.
In nature. nO{ one of the 15.00020.000 (ully lidtcnized fungi (almost a fifth of all
known fungi. and 40% of all ascomycetes) is ever found without its domesticuted alga.
though mOSt of th e algae can lead indepe ndent existences, and many of the fung i ha ve
bee n grown in a.'l:enic culture. The degree to which the association has led to physical, as
opposed to physiological, integration varies. In the si mplest case. that o f the amazing
cryptocndolitbic associations of fungi and alg!}C recently discovered beneath the surface
of sandstone in the dcserts of Antarcti ca and of Namibia. there are no speci al dual Stro,
tures. There are a few 'filamentous' lichens. in which the algal fi laments de tennine the
form of the association. BUI almost all lichens are at least 95% fungus. and so the fungus
dctermines the shape of the emire organisllL
Figure 7.1 M shows a section through part of a lichen thallus. Jl,1ost of the thallus is
clearly made up of fungal hyph ae. Those composing the uppe r and lower surface are
dcnsely aggregated. forming protective cortical laycl"$. Inside the thallus there is more
room. and the rollnd algal cells sit j ust below the upper cortex, surrounded by fungal
11 8
LI CHENS 119
hyphae. In fac t. the fungus has effectively ,\:aptured' the alga. and the relationship is one
of c)Ilptoitation or balanced parasitism rather than of mutualistie symbiosis. since about
5O'ib of the food synthesized by the alga is pirated by the fungal hyphae. which fonn tight
little cages around the algal cells (Fig. 7.1 L).
The photobionts
Althwgh there are about 500 genera of lichens and up to 20.000 species, these are
al! associated with only 25 genera of eUKaryotic green algae and 15 genera of prokaryotic
blue-green algae (Cyanobacteria). About 80% of lichens contain unicellular green alga~
(most of them contain the unicellular green alga Trebollxia, which has nOt been found
free -livi ng). about 10% cenlain filamentous green algae, and about 10% contain
cyanobac teria. The phycobionts of more than 90% of all lichens are drawn from only
three genera: two green algae. the unicellular Trebow:ia and the filamentous Tnmlepohlia,
and tnc filamentous cyanobacterium, N05tOC. So lichen taxonomy has little to do with
--
Figure 7.1 Lichens. A,B cruslose thali; C,D fOOse thalli; E squamulose thalus: F-H fruticose
thali, note5qJarTllJles at base of podetio..rn inH; I thalus reieasng5OTe<ia; J coraloid isicia; K
cymical isicia; l idlen synthesis, rrebouxiJ being enveloped by its mycobiol'lt; M \I.S.
d:scoichen tlYough apotllCcial <&oma.
120
C I L~PTRSEVEN
algae - it is essentiolly fungal ta:<.onomy. and the names given to lichens are always
those of the funltal component. or mycobiont.
About 500 lichens with green phycobionts have ar~as on or in their thu!li which
comain blue-green algae instead. These anomalous. often wun-like. areas are c.:llled
cephalodia. Three-pan lichens are found in such common genera as l.obaria, Pe!ligera.
Pu:nlocyph ellaria and Sricia. In lichens cOllloining green algae, the carbohydrates
(pholOsynthates) that mO~'e ii:om alga to fungus are sugar alcohols: in lichens containing
cyanobacteria, glucose migrates to the fungus. We do not yet know how the fungus
control5 this transfer. Cyanobacteria have the usefu l ability 10 fi:<. almospheric nitrogen,
and some ofthis is also IXlSscd on to Ihe fungus.
LICHENS 12 1
Sexual reproduction
Althou~h
the mOSt common accC5sQry struc tures are the podet ia of such squamulose
genera as Cladollill. Thesc arc large. upright. often branched Structures which generally
ha,-e onc or more apothecium like cups at the top. These may in fad become s ingl ~ red
apotheda, as in Cindonj" COCci/em , or they may bear smaller. variously col()ufcd apot h~
~cia around the rim. or they may ha"e tiny anamorphic, flaskshap.:d pycnidill.l e<>nidiomat:t
arouad the edge, as in CladO/Iia p,I'xidafll. The surface of the podetium may also be
covered with powdt:ry sorcdia.
Taxonomic groupings
Although thae arc twelve almost entirely li chenized orders of ascomycete s. ond
four more with some hchenized members. I 3m goin g: to men tion only eight of the !;Irg(f
or more common orders.
122 C HAPTERSEVEN
( I) Order Arthoniales: 17 genera, 650 species. with green algae as phycobionts.
Thalli mostly crustose. with apolhecioid or lirellate (long and narrow) ascomata, producing bitunie~te asci.
(2) Orde r Graprudales: 30 genera. 1,700 species, with green phyeobionts. Thalli
crustose, with apotbecioid or lirellate ascomala. containing unitunicate-inoperculate asci
y,. ith a thickened apex rather like that of the Clavicipitalcs.
(3) Order Leeanorales: 300 genera, 5.700 species. with green phycobionts. Crus
lose, squamulose, foliose or frulicose Ih:l.lli. with apothecioid ascomata producing
archaellSceous asci (primitively bitunicate?) This huge order is home to many of our
commonest lichen genera - Ciadonia (includ ing 'reindeer moss; C. rangiferina. and
'British soldier: C. coccinea), H)pogymnia. I.etharia . Panne/io, and Umbilica r/a ('rock
tripe').
(4) Order Opegraphales: 35 gencra, 900 species. with green phycobionts. Thalli
are crustose or fruticose, with apothecioid or lirellate asc:ornala, and bilunicate asc i.
(5) Order Peltigerales: 18 genero, 600 species. usually with blue-green phycobionts.
Foliose malli wim apothecioid ascoma!a producing archaeasccous asci.
(6) Order Pyrenul<lIes: 35 genera, !.ISO species. with green phycobion!s. r-,'Iainly
crustos.e, wilh pseudothecial ascomata containing bitunicate asci.
(7) Orde r Teloschislales: ! I genera, 600 sJ)C'cies. with green phycobionls. The
thalli are of all four main types, bearing apothedoid a~omala with Z1rchaeasceous asci.
and also producing pycnidial anamorphs.
(8) Order Vcrrucariales: 25 gener~, 700 species, with green phycobionts. Usually
crustose. rock-inhabiting lichens wi th pseudothecial ascomata and bitunicate asci.
The discipline of !ichenology has until fairly recently been conducted OUlside the
mainstream of mycology, because the dual organisms vcereconsidered so radically different from non-licheni zed fungi in nutrition. ecology and li fespan. Bm it is being increasingly ~alized that me life processes of lichens. including their biotrophic nu uition. ue
nOt rellily alie n to those of many other fungi. and we can anticipate increased integration
of this large minority group. as specialistS in Ii chenized and non-1icnenizcd fungi exchange infommtion and ideas. At least OfIe important refcTence work, the Dictionary of
tile Fungi. now covers both groups.
Identification of lichens
Lichens produce abolll230 unique compou nds which arc called 'lichen substanccs:
These are mainly weak phenolic acids. derivatives of orcinol or bela-orcinol. They include depsides, depsidones. and dibenzonfuran derivati\es such as usnic acid, which has
antibio tic properties. The indicalor, litmus, is obtained from depside-containing lichens.
Some of these unique lichen substances are routinely used to identify the genera ::md
species that produce them. KC)'s 10 lichens often call forchemicalteslS with 10% aqueous
potassium hydroxide (KOH). chlorhle bleach (el) and 5% alcoholic pa raphe nylenedi
amine (PPD). These. when applied in various sequences. combine with depsides and
dep.idones to gh'e characteristic yellow. orange or red colour reactions. Professional
lichenologi,ls can't stop al this level: accurate identification of many Hchens calls for
more refined techniques. ( I) RecrystaUilDti on of lichen substances: these are first leached
out of the thalli by aceton<:. th<:n redissolved in 3 glyceri ne/alcohol mix with some water.
orthoto!uidinc, anilinc or quinoline added. Heating causes recrystallizntion. gene rating
characteristic shapes, and colours observed under UN. More precise identification can be
anained by resorting to: (2) paper chro"!:l.lography, or (3) thin layer thrnmatogr:l.phy
(These procedures are necessitated by the existence of a5 many as six 'chemica! stra.ins
LICHENS 123
within some lichen spedes. These may look ell3ctly alike, hut their chemistry diffcrs, and
though they often have different distributions, these frequcntly over!~p), (4) DNA analysis, of various types.
lichen synthesis
The very exiStence of the slowly developing lichen ascospores is something of a
puzzlc. because when they are eventually released, no algal cells go with them . This
means that if the ascoslX'res are to establish a new generation of lich ells, they must
encounter an appropriate alga, and this in turn implies that lichens must be constantly
resynthesized in nature. The only problem with th is was that for many yean; all our best
effortS to synthesizc lichens from their component fungi and algae failed. Only relatively
recently was the trick finally mastered. It involvcs having each of the prospective partne rs
in a thoroughly debilitated condi tion. Only then. it seems, will the fungus literally embrace the alga, and only then will the alga permit itself to be co-opted without making the
ultimate prOl:est.
In a successful synthesis, the fungal hyph ae grow around each algal eel! and produce a ppressoria on its surface. Ii appears that, once the alga is in this situation, its
physiology is subtly altered. While it metaboliz.es more or less normally, it becomes very
'leaky: losing large quant itie s of soluble carbohydrates. Trebou:Iio leaks ribitol.
Tnnrepohfio leaks erythritol. and Nostoc leaks glucose. All of these are quickly absorbed
by the fungus, and convened into typical fungal carbohydrates such as trehalose. This is
interesting in vicw of recellt work sugge >ri ng that high levels of this sugar are one of t):le
sccrets o f surviving cxtreme desiccation
lichenometry
After taking colony mcasurements on many gravestones. which were, of course,
dated, Iichenologists were able to calculate past growth rates. This enabled them. for
example. to help glaciologists determine how long it has been sin~ panicular rock faces
emerged from under the ice of retreating glaciers.
124 CHAPTERSEYEN
li chens: all are like the canaries that miners used to take down the pit - ultra,en,iliye
indicators of dangers 10 our, elves and to the entire biosphere.
As a footnote to this chapter. I Fed I must mention the case of the bitunicate ascomycete. Mycosphaerella ascopfJyl/i and its host. the brown marine alga, Ascophyllum
11odOSllm (an inhabitant of the Atlantic ocean). Aseomata of Mycosphaerella are invariably found embedd~d in the tha llus of Ascophyllum. Since th~ fungus is always present.
this may indicate a kind of reversed lichenization, with the alga providing the thallu,. and
the fungus some ki nd of growth substances (or perhaps it is just a universally d istributed
pnmsite - no one has yet done the research necessary 10 establish the facts) .
B.W., M.S. Baddeley and D.L. Hawksworth (1 973 ) Air Pollu tion and Lichens.
Athlone Press, Un iversity of Lond on. London.
FrieJllnnn. E.!. (1982) Endolith ic microorganisms in the Antarcti ~ cold desert. Science
215: 1045-1053.
Hak . I\I.E. (1983) The Biolog,Y of Lichens. 3n:1 Edn. Edward Arnold. London.
Hale. \I.E . ( 1979) Ho w to Kn Oll" the Lichens. 2nd &In. Wm . Brown. Dubuque.
Ha\\ksworth. D.L. and OJ. Hill (1984) Th e Lichen-Forming Fungi. Blackie, G lasgow.
Ha\\ksworth. D.L. and F. Rose (1976) Lich ens as Pollution i\-1onitors. Studies in Biolog)
1\0. 66. Edw~rd Arnold. London.
Hawk,v,orth. D.L. (1988) The variety of fungal -algal symbioses. their evolutio nary significance. and the nature o f lichens. Botanical Journal of the Linnaean Society
96: 3-20
Hawksworth. D.L. (1988) Coevolution of fungi with algae and cyanobacteria in liche n
symbioses. pp. 125-148 (in) Coevolution or Fuog i with Plan ts and Animals. (Eds.)
K.A. Pirozynski and D.L. Hnwksworth. Academic Press, Lon don.
LICHENS' 125
Kendrick. B. (1991) Fungal symbiosis and evolutionary innovations. pp. 249261 (in)
Symbiosis :is II Source of Evolutionary Inno vati on. (Eds.) L. Margulis and R.
Fester. MIT hess. Cambridge.
Richardson. D.H.S. (1975) The Vanishing Lichens. Their history. biology and importance. David & Charles. Newton Abbot.
Richardson. D.H-S. (1992) Pollution Monitoring with Li<:hens. Naturalists' Handbook
19. Richmond PubL Co.. Slough.
Seaward, M.RD. (1977) Lichen Ecol ogy. Academic Press, London.
Smith, D.C. (1973) The Lichen Symb iosis. Oxford University Press, OXford.
Smith, D.C. (1978) \Vhat can lichens tell us abuut real fungi') i'lIycologia 70: 9 15-934.
Viu. D.H .. J.E. Marsh and RB. Bovey (1 988 ) Mosses, Lichens an d Fe rns of Northwest
North America. 296 pp. Lone Pine, Edmonton.
Vobis. G. and D.L. Hawksworth (1981) Conidial Lichen -Fomlin g Fung i. Pp. 245-273 (in)
Biology of Conidial Fungi (Vol 1). (Eds.) G.T. Cole and B. Kendrick. Academic
Press, New York.
hltp:llwww.lichen.com is a co mprehensiyc and beautifully illustrated web sile
explores many aspects of lichens and thcir ecology.
whi~h
l!
UI'I'ECCB
~8\B\.\OlEC"
Introduction
Fungi cannot walk or run, but some can swim, most can soar, a few can jump, and
some must be carried. From your rcading of the taxonomic survey in this book, you can
probably put a few names in each of the categories I have just mentioned. At the beginning of the book, when I was defining the word 'fungus' I concentrated on the unusual
somatic morphology and the heterotrophic, osmotrophic nutrition shared by most fungi.
But P<'rhaps I did not place enough emphasis on one of the main rcaSDns for Ihe success of
the fungi: their abili ty to produce and disperse vaS! numbers of tiny, but often highly
characteristic and spec ialized, spores. By sheer fecundity the fungi make sure Ihm, whenever and wherever a new food substrate becomes available. they will be on hand to exploit
it. "'Ian y fungi are cosmopolitan - you could find them almost anywhere in the world.
Thc air we bre athe sometimes contains more Ihan 10,000 spores per cubic metre. The soil
contains astronomical numbers of spores, wait ing for food. Why are there so many? How
did they get there? What significance do these numbers hold for us? This chapler will try
to answer those questions.
126
,~
Fig. 8.1 Spread of Phytophthora inicstans. A: in eastern North America 1843-1845. B: m Europe
during 1845.
128 C HAPTEREIGIIT
easily disloosed by wind or rain. Landing by chance on an other leaf. those of mo~t
spedes re,-en to their ancestral behaviour. and require the pn:sence of a film of free water
so thaI they can release motile, bifiageUate zoo.pores which swim off to infect the plant.
usually entering through the Stomales. In a few of the most highly evolved oomycetes.
members offarnily Peronosporoceae. the airborne sponlngia produce a germ rube . The;e
fungi appear to be cutting their last link with the aqUJtic life of their ancestors.
As I mentiono:<i in chapter 2, the human species is probably the most impon:ml
vector for many fungi. One imponant example of this is the oomycete Phyrophlhr)f(l
ilifes/(Jl1s, which causes late blight of potato. Human tran<,QCe::mic commerce inadvertently carried Ihis Central American fungus to nonheastern Nonh America in 1843, and to
Europe in 1845. I say 'inadvertently' because at that time no one even knew the fungus
existed. or what it was capable of. The maps reproduced here (Fig. 8.1) show how, after
th:se introductions, it~ natural spread proceeded. Airborne sporallgia were obviously a
successful invention.
The structures associated with selmaJ reproduction in :lYgomy~tes are very conser'ative. Zygosporangia are basically tiny, look-alike. thick-walled, resistant capsule, designed to survive hard times. But in a few case, they may also ha"e some adaptltions for
dispersaL The antler-like outgrowth s of the suspensors in Ph)"com)"cts blakesleeal!llS
mlke the "Whole structure a 'micro-bulT' that could be unknowingly picked up and carried
lway by a passing arthropod.
Non-motile Sporangiospores
Zygomycetous Anamorphs
When wc look at the lMmorphs of zygomycet~ s. we find a bewildering diversity of
form and function. We can di stinguish four mai n kinds of di spersal mechanism. and
s~\~r.ll sub-categories.
(I) Large. spherical , columellatc rnitosporungia each containing hundreds or thous.::.nds of spores (Fig. 3.4 A). But the generally similar form of these spor.mgia is not
rdkc\~d in their dispersal techniques. (A) In some c)(umplcs the spores are produced in a
slimy malri.~ . This may be SUlTQunded (i) by a thin but persistent membranc (peridium). as
in Phycr)mYCt.f l1il<:IIS. or (ii) by an equally thin membrane that dissol \'es and e:c.poscs the
~pore drop. In many J//lcor species Ihe e.\ posed mucilage imbi~s water and swells to
S<!'eral tillle~ its origir.a1 silc, often supported by a collar-like remnant of the peridium.
Thi. is a mlkcd spor~ drop. and is often an adaptation for di,persal by small animal
\C Cto~. (B) In othe rcas ~s th e ~po re ~ are dry. so th:\t when the pcridium rupture s. they can
blo ..... awuy on the wind. e.g. Rhhopru siolorlifer. (e ) In the third group, the spore m:lloS is
"iolentl}" d ischarged. This technique has been evolved by onl y on~ gentlS of Z)'gom;.cctes, Pilo/m/m (Fig. 3.6 A-C). a specialized inhabitant of the dung of herb ivorous
m~;nmals. In order to sur. ive, (his fungus mUSt gel its spares away from the dung and 01110
th~ prospective diet of the animal concerned. The subsporanginl vesicle of this fun gus
ruplllre<; when internal pressure rc~ches about seven atmospheres. and e~pds th~ spore
mas~ to adislanceofup to two metres - far eoollgh to gct it away from e\'cn an elephant's
hug~ <J~posi\.
ti,d> intermediale genera as Thumnidium (Fig. 3.4 D) Io.rge and small ~porangia coc .~ist.
The ~ m:\ll sporangi a ofte n break off und are wind dispersed. wh Ile the large sporangia
remain in place and act as slimy spore drops. T/!Qlflllidium is unusual in this two-pronged
allocation of reprodocth'e resources. Hdicoslylum produces mul!ipl~ sporan gia with red~ced spore Illlmbc:rs. Other genera like B/akt.!leu. produce ~porangia wilh very few spores
(Fig. 3A 8),
A; Syncep~ JIi~
{lygomy<:o~~)
B PiprQ~,pn.lIs
{2ygo'T1y~o\a)
"
..
,,~
c:
~-.
co~spot9d .~..,myeola~
spo'a~ I <>!.
D. DI~"" ~mY<:Olan
COJIidium
r
I
13{) CHAPTER E IG HT
ooe-spom:! sporangia or Cwmillghamtlfa are dry and wind.dispersed . (8) The umbellate
sporocl adia of Kick.ul/(I produce their sporangioles in a drop of slime. (C) The sporangiophores of some dung-inhabiting genera are very tall. and elaborately branched or
coiled, as in Spirodact)"lon (Fig. 3.4 F). I think these stroccures play an important part in
spore dispernll. becoming tangled in the haiTof thesedenlar)' rodents on whose dung tbey
grow, and being ingested during grooming acti vities,
In the Entoffiophthorales, one-spored mitosporangia are actively sbot away by three
different mecbanisms: (A) In EnfOmophrMra muscat(Fig. 3.6 E), the apex of the sporangiophore ruptures to expel the sporangium. Cytoplasm from the sporangiophore goes with the
propagule, and may help it to stick to the substrate when il lands. (8) Species of BasidioOOlus
have aline of weakness around the sporangiophore just below the apex,At maturity, the wall
spli lS there, and the spore flies away with part of the sporangiophore attached. As in a twostage rocket, the sporangiophore fragment falls away during flight. (e) In some species of
EmomcphlMra, and in ConidWbolus, the mitosporangium is projected by the release o f
pressure built up between the sporangium and a tiny. intrusi~"ll columella.
ttI1 Ul'1>E.CCB
91SLIOTECA
/
c
o
Fig. 8.3 Adl-entll"e5 of Pllyllactinia ([rysphales) (see text\.
1&45
,li
,
1c
,
p - ... -
v
,;;'..,
r,C
-C
-'Ie
':
136 CHAPTEREIGIIT
the cem.re. The se:gments thus fonned open by bending backward. and a~ they reflex
further and further. they lift th~ gleba above the sUlTOunding leaf litter. exposing it to the
rain and wind. My riostoma has several evenly spaced ostioies.
In the biT(rs~nest fungi (Nidulariales), the basidiospores of most gener.! fonn inside
several small se:edlike packts called peridiolcs or. more colloquially. eggs. These: sit in
a deeply funnel shaped splash-cup receptacle. Which focuses and reflects the kinetic
energy of falling raindrop~. Some of that energy is transferred to the peridi oles. which are
thrown for some distance.
[n the earthballs (Scl<,rodermatales), a group otherv.'ise e:memdy passive in its
spore dispersal. there is one ahertanl family. the Sphacrobolaceae, which has rather SUTprisingly evolved a new kind of active spore dispersal. The positively phototropic
basidioma of Sphauobolm stellmu.f is only 2mm in diameter, but can catapult its gleba
- I mm in diameter - up to 7 metres, The peridium in this fungus has se veral different
layers, AI malllOty. the top splits and reflexes to expose the spherical gleba. The lower p:ut
of the ~ridium s.cp.1rate5 into two nesting cups which lOuch each O\her only al the rims.
Glycogen in Ihe cells of the inner cup is converted to glucose. and turgor pressure builds
up until the inner cup abruptly turns inside out and flmgs the gleba into space.
Sphaerobc/Il,\ often occurs on old dung. and tile evolutionary rationale for its explosive
spore dispersal is clearly similar to those for the very different mechlnisms we e)(amined
earlier in Pi/oOO/uI, SaCCobo!UI and Ptxlolpom.
The stinkhoms (Phallak;;) are perhaps th~ mOSt bi zarre members of this strange
menagerie. Thc youn g fruit body is cal led an egg. In Pha/ilrs (Fig. 5.7). the soft sllell splits
in the morning. as a d~nse mass of specialiled ti!>Sue inside tlkes up water from the
mucilage that sUlTOunds the embryonic basidioma, and elongates quickly to produce a
tall. spongy stalk. At the lOp is a receptacle. cO\'ered with a sugary but eYil-smelling
greenbh sli me in which the ba.,idiMpores are embedded. Th~ smell attracts a procession
of tlying insects, plrticularly dipteran fl ies. which gorge e.~citedly on the sl ime, llnd also
carry spores away on their feet. By evening, the green slim ~ is gone. ili m ission accomplished. The most highly e\'oh"ed phalloids seem to be those which. like Aserol. have
ba>idiomata wilh long, brighl red. r:adiating r.!ys Ihat can only be intended 10 supplement
their olfactory messag~ with a visull on~. As a plssin g vector (prob~bly a tlying an hropod) Illig ht say: "It's II flower. ;";0. it' s rotting meat. No. it's facce s !" Slr~ nge fungi i nd~ed .
that in the name of di spersal combine the qualities of flowers and eXL'rement.
problem with spor~s is the same as th~l with pol1~n. Both lock any motive
po"er or navigalion~1 equipment. To make sure thai al kast a fe'" spores land in places
where Ihey will find food (c<;pt.'Cially if they are picky). fungi must liberate Ihem in
a.tronomical numbers. Some fungi are making and releasing spores from early spring
until late fall. Somc will c\'en release them in winter whe nen:r the tempcralf.lre ri:;es above
frcezin g poi nt (OC) ,
"'>cologi sts have described nearly IOO,O(X) fungi. and there is lillie doubt that
hundreds Ofloousand, more remain to be ~i5CO\crcd. Let's see just how many spores a few
Funga l a ll ergies
The p rime SUSpe1:ts in respiratory allergics provoked by airborne particles were
originally the pollen gmins of plants. and mgweed (Ambrosia ~pp.. Asteraceae ). became
the villain of the piece (e\'en though most people ha"e no idea what the plants look like).
causing what is widely and inaccurately known as 'hay fe,er.' But po:oplc tended to forget
that allerge nic pollen is ac tuall y only a summ er proble m. while many respiratory allergics
persist in fall and winter. So scientists had to look elsewhere for o ther less sca$()nal
causath'e agents. and found them in the fonn of fungal spores. Skin teSl~ proved that such
spores can indeed be aliergenic.About 20% of me population is alopie, and e:tsily sensi li1-Cd by normal spore concentration. (up to 10' spores/m'). These proplc may react by
developing 'hay fever' or asthma. and may become se ns itized to a number of common
allergens. The other 80% of the popul~tion do nOI deve lop allcrgie~ so easily. The)" would
require exposure 10 higher spore concentrations ( 10' - lit spores/mi) such as occur only
during such cvents as haymaking. harvesting or grain handling. These eoncelltralions
may then produce allergic a!veoliti s (hypersen.itivity pn eumoniti s) resulting in breathlessness. Such sensitivily is usually restricted to (I single all ergen. and the condition is
u~uall)' re lated to the person's occupation (famler, grain -handler.) Many common fungi
are IlOW known to be allergellic. and more allergens 3re being recogni:ted as time goes on.
So all fungal spon:s should be regardcd as potentially allergenic. Sufferers from alkrgies
induced by fungal Spores could gain some relief by moving to hot orcold desertS. or to the
mountnins. or by tak ing an ocean cruise.Very high local con centrntions of spores can be
enCOUIHcr~d during epid<:mics of fungal plant diseases such as wheat rust. and the spore
concentrations to which fann worke rs handling mouldy hay are eXpoM:d can eventually
cause a ~erious and sometimes fatal allergic diseaseeaUcd "Farmer's lung' (Rippon 1974).
Here, repea!~ expo~urc to high concenl,Jtions of ~pores from a number of different
a ll ~rgenic fungi (oft~n spccies of p/!l1i/."illi1lm ~nd Aspergillus) can lead to ~ensiti7.~lion.
and produce acute or ~hronic symptoms. The acule stage is u$u~llr found in haryest<:rs
and threshers. who are brieny exposed to o"emhclming spore loads. They experience
chills, fever and generally fccl un\\,ell. but thcy will rceo,'er. The chronic stage is found
~mong ,ilo and mill workers who have low-level but constant e~posure to the allergens .
This is much more serio us. because it causes dcgcncru tive changes in the res pi ratory tract
which lead to obstruction of the airway. Patients become breathless after exertion. cough
constantly. and fe~l weak. The chronic stage may be a progressive cause of emphysema_
and may eventually be fatal. This disease was firsl described in Canada (Cad ham 192..;)
and is commonest in temperate regions where high rainfall encourages moulding of hay.
A simib r complaint has been seen in some ofiice workers when hidden air-conditioning
systems have. supported massive gro" th of similor moulds. Bronchial asthma is also
frequently provoked by airborne fungal spores_ usually belonging to the mould gene ..!
A/Unlaria. Aspergillus, Drechslera ("He/mimhosporil.m') and Penicillium. These spores
reach their highest numbers in fall. with anoth~r lower peak in spring.
UFPE.CCB
/a>BIBLIOTECA
--4
The air inside buildings tends to reflel.:t the cond ition of the outside air, thou gh , pore
counts arc usually lower indoors becau~ there is no wind effect. Howe\lCr, if rooms are
d:unp, or if there is soil orpl.lOt material present, these may represent new spore sources and
counts may increase and become more diverse. Bathrooms are damp. ami moulds are often
found sporulating around windows. Kitchens have refrigerators and garbage conl.tiners.
both of which m:ly bespore sources. Living rooms often contain house pl.lOts. and both soil
and plllJ1ls may be spore sources. Air conditionin g systems, whjeh involve condensation of
moiscure, may become major sources of fung~l spores or bacteria. Activities such as house
cleaning (especially vacuuming, e.>:ccpt in the case of acentral V3!;uum system exhausted 10
[he e;(terior) and food preparation are known 10 increase airborne spore counts. The effecls
of su~h ~hange5 on the development of allerg ic symptoms are being researched, and though
there are :IS yet few proven connections betwee n individual fungal ta"\a and the onset of
respiralory allergies, properly designed epidemiological studies will, in my o pinion. lead to
the confirmation of current suspici ons. and the unma'lking of many fungal culprits.
Poll en~
nnd
,~ UI'i>E.6es
@ BIBLIOTECA
Fungal Physiology
Cell components
Proteins are large. complex molecules. made up of various mixtures and configurations of20 different am ino a dds. held together by peptide bonds. Because of the essentially infi nite number of structural possibilities that the building of a protein molecul e
preserus, most organisms make many uni que proteins. Fungal proteins are unique. yet
function just like those of other organ isms. Some are enzymes and struct ural components, others are associated with nucleic acids to fonn nucl eop roteins, and a third group
are conjugated with carbohydrates to fonn glrcoprote ins, which arc fou nd in membrane s
and the cell wall, as wcll as being secreted as ex~lluler enzymes.
Nu cleic ac ids are o f two kinds, commonly known as DNA and RNA. DNA is the
ccntral reposilOry of genetic information. DNA incorporates the gene tic code, in whic h
sequences of three bases (codons) code for individual aminoacids, and thus spedfy the
order in which these will be join~d together 10 fonn the variou s prote ins. DNA replicates
itself. an.d al so transcribes encoded in.formation inlO RNA. Some R..t"\l"A is associated with
proleins in ribosomes. some occurs as messenger R.t~A. and some as transfer R..t~A .
Ribosomes move alon g messenge r RNA strands , reading the succession of3-b~sc codons.
~nd Wingin g together ami no acids brought in by transfer R..t"A. [n this way, protei ns are
assembled.
DNA and RNA both have a sugarphosphate sp ine. w!th p uri nes and py rimidines
anaclled to the sugars. The sugar in DN A is Zdeoxyribose. that in RNA is ri bose. One or
the pyrimidines of DNA. th ymIne. is replaced by u racil in RNA. DNA molecules are
usually in pairs, helically inten wined: RNA is singlestranded. DNA is concentrated in
the nucle i of cuk:uyotic cells, though some is also associalCd " 'ith the mitochondria (thi s
is because these: organelles were originall y independent prokaryotes). One way of categorizi ng DNA is by its base r:llio (percent guanine -+ cytosine). In the Eumycotan fu ngi.
142
Metabolism
Metabolism may be defined as the sum total of all chemical reactions that support
life. These may be divided into an abolic and catabolic functions. Anabolic metabolism
convens food substrmes into fungal biomass, c.alaholic meta bolism extracts energy from
various substrotes, producing a denosine triphosphate (ATP). red uced nicotinamide-adenine dinucleotide (NAD H) and NADPH, as well as intermediates used in various anabo lic proc esses.
All important reactions in biological systems are initiated and controlled by en
zymes. In the absence of enzymes ffiOSl reactions would go on 100 slowly (if they pro-ceeded at all) to sustain life. Enzymes increase r:l!es of reaction dramatically, by factors up
to 10' . An enzyme consists of a prote in. often with a coenzyme such as a vitamin. and an
activator such as Mg ions. Enzymes often work in sequence, each catalyzing a particular
stcp in a melabolic pathway. Many fungi can produce enzymes that are rarely found in
other organisms, e.g. ligninases and cellulases.
Glycolysis. Of the three pathways by which glucose can be convcned to PYnJ valc
before it is oxidized in the citric acid cycle. mOSt fungi usc two: the Embd en-i\-Jeye rhof
(EM) aud the hexose monophosphate (ID,I). The EM pathway yields ATP and pyru"ale.
The HM pathway yield s NA DPH. the main reducing agent in the biosynthesis of fatty
add s and sugar alcoh ols, and ribose, used to make RNA . DNA and other nucleotides.
Fungi respire aerobically, regenerating NAD by transfer of electrons from NA DH to an
external acceptor, oxygen. Fungal fermentation in' o\ve.'; the regeneration of NAD by
transfer of clecirons to pyru vate. which is produced while the subs trate is being metabolized. This kin d of fcrm~ntatio n can produce IIlcohol or lactic acid. Everyone knows
Growth
Growth is often defined as irreversible increase in volume, but usually implies some
other kinds of change as well: changes in components, metabolism. sha~, function. A
mycelial fungus will extend in all direction$ as its hyphae grow at their tips. The hyphae
become longer, they often branch repeatedly, a lot of wall materinl is laid down, the
amount of protoplasm and the number of nuclei in the colony increase. If the fungus is
ll.lcky. it will find more food than it uses l.lp in the search. so it can both grow and accuml.llate reserves that will enable it to sporulate. Fungal growth is usually measure d as increase
in fresh weight (unreliable because of variations in wate r content), or in dry mass (whi ch
for obvious reasons can be measured only once for any particular colony), or by increase
in the diameter or radius of the colony (which can be measured re~atedly). In unicellular
yeasts, growth is measured by counting cells, or by measuring the increase in turbid ity of
the cul ture medium. If we were trying to produce conidial inoculum for use in a program
of biological control (see chapter 14). we might express the success or the organism in
terms of the numbers ofpropagules it formed in a certain time. at a certain tem~rature , or
on a particular substrate. A mushroom-grower would be interested only in the mass of
basidiomata produced.
Beginning from the spore, growth proceeds in stages, which can be catcgorized as
germination. assimilati,'c growth, and s porulatio n. Each stage may require conditions
very different from the others. I wi\! examine them in tum. Much of OUf information about
,
,
I SO C H APTE RNlNE
at lOOOC but OOes not solidify until it lOIs 10 45C, and is not metabolized by most fungi.
As linle:lS 1-2% agar solidifies most medifLAgar media are usually used to fonn thin layers
c;overing the bottom of petri plates, or to fin the bottom third or so of test rubes (called
<i1anlS' beCause mey are placed at an angle while the agar is setting). Plates are used to grow
culrures for idcntificatiOll. Typically, a small inoculum will be placed in the middle of the
plate. then incubated. The colony which develops. growing partly abo\'e me surface of !he
medium . and partly below it. will often show diagnostic features (colour, Ie~rure, sporula
tion, etc.) Living cultures are oflen stored in slants, or may be Iyophilixed (freezedried and
sealed in a high vacuum) for longterm storage.
If the culture ;s to be axeni c (or as we say, uncontam inated), the medium. which is
attractive and accessible to many microorganisms. must first be sterilized. This has usuall y involved pressure-cooking the medium in an autoclave at a steam pressure of 15
pounds/square ioch (2 aunospheres) for 15 minutes . The tempernrure reaches 120C,
effectively killing all microorganisms. But it also tends to caramelize sugan. and to
destroy thennolabile substances like miamin (a vitamin) and some antibiotics. Autodaving is acceptable for routine work. bill for critical physiological srudies, it is better 10 filler
the medium through membrane filten lhat effe<:iively remove bacteria and fungal spores.
Nutritional Requirements
C arbon nutrition. One of the principal distinguishing features of mOSt fungi is lheir
inability to fi ~ inorganic carbon. The simplest co mpound most fungi can usc as a source
of energy is the monosacch aride glu cose. Unlike most olher carbon sources, this doesn ' t
need to be enzymicall y brohn dow n to anything simpler beforc it can be absorbed.
Vinually all fungi are ready to met~bolize glucose at a moment's notice: they alre ady
have all the necessary enzymes, which are thus dcscribed as const ituti ve. Fructose. mannose and galactose are also readily used, but there is often a delay before assimilation
begins. This is bec-ause the enzymes in\"Olved in processing these sugars aren't necessarily ready and waiting. The fungus takeS a liule while to recogni~e lhe nature of the
substr.ltc. and to s)"mhesizc the proper enzymes. This process is called ind uction . and
produces ada pt i.-e enzymes_ If a 101: of glucose is present. it may actually suppress the
production of the enzymes that deal with other substrates: the fungus takes the easy route.
A little glucosc. on lhe other hand. may fuel the inductioo process, and shon en the lag
phase on many substrates.
Although many experiments have been done to compare the ability of fungi to use
differem single carbon sources, these may nOt tell the whole story. In nature. fungi usually
havc to deal with mixtures, and their behaviour in this situation can 't always be forecast
from single-substrate tests. We've already seen that the presence of glucose can suppress the
utili7.atiOll of other substrates. Perhaps the most impon:mt example of the mill.ed substrate
situation in\"OI\"CS lignin. Although the ability to degrade lignin (0 carbon dioll.ide is Olle of
lhe things for which many basidiom~'cetes (the white rot fungi) are most nOl:orious, they
can't usc lignin as soli!carbon source, and will break it down onl y in the presence of another
accessible carboo source, such as cellulose. cellobiose or glucose. Fungi may deal wilh
lignin only to gain h.>uer access to the cellu lose, or in order to release available nitrogen.
Culture medi a must also contain 3 source o f nit rogen . No fungus (in fact. no eukaryote) can fix atmospheric nitrogen. Many fu ngi can usc: nitrale, lhough ammonium nitrogen is even more universally metaboliZed. Ure~. amino acids, and various polypeptidcs
and proteins are accessible to some, but not all, fungi. A good nitrogen source for many
fungi is hydrolysed case in, a mixture of amino-acids . Sulph u r requirements can almost
always be met by incorporating sulphate in the medium, though some chytridiomycetes
require sulphur.containing amino-acids such as methionine.
,,
Cllions such as: potassium. ammonium. m.lgnesium. calcium. manganese and iron
arc all accumu!:ued against high concemnltion gro.dienls. sho""ing that .lctivc. carriermediatcd transport mo:hanisms arc in'olvect. If a fungus is loaded with ,;()dium. then
supplied with potassium. sodium wilt be cxpelled as potassium is taken up, This kind or
bt'haviour is ca ll ed countenrilnsport. The dival ent c~ l ions. 1\Ig0. Ca~ nnd Mn " . will be
tak~n up only if phosphate is ~lso a\~ilable. and Fe-is chelatcd with siderochromcs
before being transported. The transport of ions such as phosphate and sulphate is also
carricr-mediated. Once phosphate i$ in.id.., the cell. it is con\eIted 10 polyphosphate. und
internal concentrations of orthophosphate dOn't ~hange. The study of nitrate UplJk.e h~s
bt'~n hindered by the lack of a Te,1\ly se n_, iti v;: meu suri ng Icchn iq ue , so it isn' t cc nai n th~1
~~ITjer, arc invohed.
Glucose and other sugar.; mow across the piasmakmma of fungi by fncditated
diffusion. or by nctive tr.msport, or by 2 combin~tion of the 1.... 0. A sin;lc fungus may hu\e
S<!\"(~ral different meeh~nisms. Somc 01 the aC11- e mechanisms are constitutive (always
present and read, whik some are in~ucible. Amino acids are also lr.mspofled actively.
NfI.rtupora cnLISt! has been shown to havc al 1~3~\ live differ<: lu amino acid tran ,port
syskms: one carries only m~lhiomn~: anothcr. on ly aciJic amino ~citls: a thirJ. only
basic umino adds: the fourtll. aroma!j,' ;md 31iph~tic umino 3cid.~: the fifth. aromatic.
aliphatic and b:J~ic amino acids. AminO:lcid I mn~port syslemsdiffer from those for sugars
and ions in thal no countertransport h:!5 !xen detected.
Cetl ulosc lind L ignin Decompositio n_ Fungi produce an extraordinary spe<:lrum of
enzymes. and can Jegrade just about Jn~' organk sub;;trat~ _ Perh:lps the mo,t import~nt of
these ,Ub,tr:ltcs are \.C ellulose and lignin B inion s of \on nes of cellulose i, produced by the
high~ r plants every year. It fonlls tht gr~atcr part of their cell walls. and, being apparently
enable 10 re<:yc le it themselves, lhey dis:::ard it in \'ast quantities every year. Autumnshcd
!eaves. the entire bioTffi15s of annual plants. and el'er.tually the corpses of the much longerlived lr~es: all ar.., beq ue~lhed to Ih.., fungi. beCause no Olh~r organisms c~n initintly
Environmental Effects
Pb ysical parame ters like t~mpcratl.lre, lig ht, and gravi ty have profound effce ts o n
many fungi, but generalizations are dangerous. Some psychrophihc fungi grow at temperatures below OC: some thcnnoph iles can function at temperatures aoo\'e 50'C. Some
fungi need light in orde r to fruit: othn:; seem indifferent to illumination. ~hny manofu ngi
are extrclllely sensitive to gravity: ru nny microfUllgi are totally oblivious to it
It is helpfu l to tnow thc cardinal tem pera tures of any fungus we want to work
with. These are its minimum. opti mum ~nd maximum temperatures for gro\\lh, Most
rcs~ an;h ers find it co nveni en t 10 grow a fung us at its optimum tem peratur~. but this
ignores the fluctuating and often t:xtrcmc temperatures the organ ism mUSt face in much of
KonhArnt:rica. I have already pointed oUi that falling temperatures in autumn may induc.:
fru iting in some fungi (such as Coprinus Co"w tljS), donnancy in others: that [<',Img stages
o f m~ny fungi (such as M mlilitlia) mUSt be chilled be fore they will erminate; and that
heat treatment produces the same effect in others. From srudy oftheir assimilative grov..th.
fungi can generally be categori zcd as psy chrophilic, meso philic or thermophilic.
Psychroplliles have minimum growth temperatures bel ow ooe, maxima below 20C. an d
optima in the nmge 0"-1
Mesophiles (the great majority of fungi) have minima above
O"C. maxima below 5ifC, and optima between IS and 4O'C. Thell1l()philes h:wc minima
above 20C. maxima above 50' c' and opti ma between 35 and 5WC. Establ ishing true
optima may not be si mple, as Fig. 9.1 shows_If 11 complete growth curve is not ploued al
re.
~ 100
Time (00)
Frg. 9. 1Effect of lime and tC!"r'lpefature on grQI.Vlh of Phycomyces i1 a defoed medOn (Robbins
artdKav;magh,1944).
~ UFPECCB
~BIBLIOTECA
Although many fungi fruit only after exposure to light. the actual amount of light
energy needed can be very small. Initiation of Coprinus /ugopus basidiomata is triggered
by only 8 jouks (J) per square metre (5 second, atO.l foot candle). To induce pseudothecial
ascomata of LeptosphlU:ru/ina requires even less light (0.64 J m,). Most fungal responses
need only 0.5-20 J m"; remarkably little, considering the magnitude of the induced effect.
The development of reproductive structures obviously necessitates changes in
morphology ami development. but the nature of the physiological and biochemical
changes involved is not immediately apparent. Detailed comparisons of the mycelia and
conidia of the Chrysonilia anamorph of Neu.rospora crassa show th at some substances
such as trehalose, glutamic acid, glutathione. carotenoids and phospholipid. which are
present at low levels in mycelium, are round at much higher le vels in conidia. Others, such
as arginine. omithine, and adenine nucleotides, are more plentiful in mycelium.
The conjugation of yeast cells is governed by diffusible hormones. and by agglutination factors that ~ bound to the cell wa1!s. ElIch mating type of Saccharomyu5 ceTuiJine
has it.'; own hormone . One consists of oligopeptides of 12 and 13 amino acids. The other
has a molecular weight of about 600.000, an d comains protein and polysaccMnde. Though
they are so different. these substa nces have similar effects on the appropriate matin g type:
they inhibit the initiation of DNA synthesi" effectively locking the ce ll imo interpha.><:.
Budding stops, and cells of opposite mating type become mutually adhesive. Since isolated prolOplast~ won't stick together unless they manage 10 regenerate walls. the agglutination factor must be wall-bound. Cells of oppositc mating type have distinct but compkmentary peptidopolysaccharide agglut ination fac tors. Conjugation follows agglutina_
tio n. Sometimes the zygo te multiplies to form a generation of diploid cells, so metim es it
develops into an ascus- like meiosporan giulll.
Amo ng the ascomycetes proper, sex homtones have been par1i~lly purified for Nell.
rospom (Sordariales), and there is evidence for the existence of comparable hormones in
A5cobolu5 ( Pezi zales) and Bombardia (So rdariales). T he well-known mycotoxin
zearalenone, prodoced by the hyphomycete FU5arium gramintarum. apparently stimu
lates the developme nt of pcrithecial ascomat3 of its tcleomorph. Gibbudl" ~e"e
(Hypocrea!es).
Among the basidiomycetes, it has been shown that oppo.~ite mating types of Tremel/a
(Ph ragmoba sidiomyeetes) have indi vidual. constitutive sex hormones. One of them h~,
been panially characterized: Tremerogen. as it is call ed. is a l2-amino acid li popcplide
with an isoprenoid conjugated to the sulphur of the cysteine at Olle en d. When the yea,tlike basidiospores are exposed to Ihis, they SlOp bodding and produce a conjugation'tu~ .
The red yeast Rhodo(()m/" has simil:rr hormones. Om." of these. nJm~ rhodotorucinc.
inhibits budding and induces formation of conj ugation tubes in the opposite mating
type. The resultant tcleomorph i~ RhodospDridillln (Uslilaginale$).
The situatio n in many basidiomycetes is co mplicated by the fact that although the
fim prerequ isi te fo r sex ual reprod"ctiOl1 - the bringing tog~th er of compatible nucleihappens a t the momc nt of dikaryotization. the ultimate sexu31 fusion of nucle i may b~
long delay~d. aod happens only to distllnt descendants of the original nuclear pair. Al_
though sex hormones may facilitate the meeting of Olonokaryotic myceli~l. other factors.
nutntional and environmental. probably determine the timing ofnude-ar fusion and meioSIS.
Although "cry few fungi h3vt bt;~n investigated for the prescnce of SO:.\ honnones,
it seems li kely that the ir sec retion is the norm rather th on the e.\ ception. [f ascomycete and
b;ls idiomycctc sex hormones arc show n to have some uniformi ty of structtJre and action.
it would be fJsdn~ti1\S to apply the m to the vast number of dikarYOlll>'cOlan anam orphs
for which no teleomorph is known, to see if sex ual dcvdopm~nt eQuid ~ initi:l.!cd, ~nd
1ll3ny lungstanding mYSteries solved.
Antifungal Compounds
The chemical industry
synlh~siles
\'ariou~
Further Reading
Aronson, J. M . (1981) Cell waH chemistry, ullrastnJ~ture and metabolism, pp, 459-507 (in)
Biology of Co nidia l Fungi. Vol. 2. (Eds.) G ,T. Cole and S, Kendrick. Academic
Press, New York.
Bannic ki-G arcia. S. ( 1966) Cell wall chemistry, morphogenesis. and taxonomy of fungi.
Annual ReYlew of l\'1ierobiology 22: 87- 108.
Ikrry. D_H. ( 1975) The en\'ironmental control of the physiology of filamentOUS fungi. pp. 1632 (in) 'fh(: rilamentous Fungi. '.hl I (&Is.) J.E. Smith and DR Berry. Arnold. London.
Burnett, J.H. (1976) Fundamentals ofl\lycology. Arnold, London.
Carlile. M.1. (19 70) The photort:sponscs of fungi. pp. 309-344 (in) Photobiology of Microorganisms. (Ed, ) P. Halldal. Wiley. New York.
Cochr.me. V.w. (1958) Physiology of Fu ngI. Wiley, New York.
Griffin. D.H. (1981 ) Fungal Physiology_Wiley, New York .
Holl. R. (1981) Physiologyofconidi al fungi. pp. 417-457 (in) Biology of Conidial Fungi.
Vol. 2. (Eds.) G.T. Cole and B. Kendri(k . Academic Press, NcwYork .
H3",ker. L.E. (1957) Th e Physiology of Rep r oduction in Fungi. Cambridge University
Press, London.
Lowe, D ,A. and R.P. Elander (1983) Contribution o f mycology to the antibiotic industry.
l\Iycologia 75: 361-373.
Mueller. E. ( 1971) Imperfett-perfcct conne<:tions in ascomycetes. pp. 184-201 (in) Taxonomy of Fungi Imperfecti. (Ed. 8 . Kendrick). UniVl:rsity ofToronto Press, Toronto.
Robinson. P.M_ ( 1978) Practical Fungal Physiol ogy. Wiley. New York.
Smitll. J.E. and O. R. Berry (Eds.)(1975. 1976, 1978) The Filamentous FungI. Vots. 1-3.
Arnold, London.
Smith, J .E., D.R. Berry and 8. Kristiansen (Eds.) (1983) Tile Filamentous Fungi. Vol. 4.
Arnold. l ondon.
Turi3n. G. (1966) Morpllogcnesis in ascomycetes, pp. 339-385 (in) The Fun;:i. Vol. 2(Eck) G.c. Ainsworth and A.S. Sus~man. AC(l(icmie Press. New York_
T urian. G . ( 1969) Dirrerenciat ion Fongique_Masson. Paris.
~ U~PE.eC2
~.$8iBLIOTEC A
10
Introduction
Genetics is the discipline that seeks to understand the ways in wh.ich the information needed 10 reproduce an organism is slored within iI, and how that information may
change and be reassorted before it is passed on to th e next generation. In recent ycars .we
have also become oonccmed with how this informat ion can be c hanged in a directed way
by human int<,rvemion. This chapter anempts to show how fungi are useful lools in some
areas of both Mendelian and molet:ular genelics. If yOUT background in this area is sparse.
you will find some useful introductory infOf1ll.ltion in chapters 1 and 9. If you still have
trouble \\!th what follows, I recommend th at you consult an e lementary gem: tics tell!
before trying agai n ..
In the simplest ternlS, genetic infonnation (the genome) is maintained in the ,eU as
1000g.linear sequences ofnudeotide base p:lin whi, h make up DN A molecules. Theorderin
whi,h these bases ocrur constitutes the gencti, code. and this 'ode specifies the sequences
of amino acids required to build all the proteins necessary for the construction and operation of the living organism. DNA molecules can be very long. incorporming many thousands of base pairs, and are ,alled'hromosomes. The genome of prokaryotes is contained in
a single. usually ciro::ular chromosome found in the cytoplasm. The genome of eukary()(es is
contained in twoocmore(often many more)chromosomc:s.. whkhare contained in a nudeus,
a special command module separated from the c)'1oplasm by tWO membranes.
The cukary01ic plants and animals differ from ea,h other in many ways, but both 3re
basically diploid. This means that their nuclei contain two matched sets of ' hromosomes:
(usuall y one set orig inally derived from a male g3mete, one set from a female gam ete). So
each chromosome has a 'double: Most genes on ea,h chromosome have a counterp~rt ,
,alled an allele, on the 'double: This ~Ilele affects the same ,h3f3.,rers, thou gh nOt
nC(.:es.sarily in the same way. FOf e:.;ample. one allele of a particular gene makes pea pl~nts
tall, while Lhe orner allele makes them dwarf. If ~ tall plant is crossed with a dwarf pl~nt,
the re will be more tall offspring than dwarf offspring. Plants will be dwarf only if both
alleles are of lhe dwarfin g kind. This shows that one allele can mask another: we say that
the 'tall' allele is d ominan t. the 'dwarl' allele rtces.sh-e. Th is makes genetic analysis
diffi,ull. and also makes il hard to bcud pure lines of many diploid organisms, because it
is almost impossible 10 eradicate recessive genes. since you ,an't tell whether they are
159
160 CH A PTE R T EN
presem or not (though it is easy 10 pure-breed for reccss ivc colour gClles. su(;h as those
expressed In white ratS and mice.)
The vast m~jorily of fungi are h~ploid. which means th~t their nuclei contain only
a single set of ctLromosomes. This gi~-es thcm ccnain advantages over diploid o.-ganisrns
for genetic studies. since there are no competing aUeles. and c"ery gene is potcntially
capable ofbcing expressed in the phenotype (the physical manifestation Or incarnation of
the organism). This .,bsence of maski ng makes gcnetic analysis much easier. The advanI~ges of using fungi in genetic studies are as follows:
(I) The mycelia of almOst all fun gi are populated wilh haploid nuclei
(oomyeetes, be ing chrornislan rather than cumycOtan. are atypically diploid), and many
fungi form large numbers of uninucleate. haploid s]lQres_ Th~se can be used 10 study
natuut]y occurring or induced mutations.
(2) The hyphae of closely related eum}'cotun fungi can fuse with one another
(anastomose) locally during nOffilal assimilative growth, exchanging ntlclei and thereby
producing heterokaryons (m ycelia containing genetically different nudei). The heteroknr}otic eondition confers great flexibility on many conidial fungi, helping them to
cope with different substrat~s and conditi ons. Heterokaryons can be investigated tinder
corumned conditions by isolating spor~s or hyphal fragments. and arc used by geneticists
in the complementation t~st (see below). The production of heieroknryons may also be an
essential step toward a long -delayed sexual fusion. as when basidiomycetes init iate
dikar)'otization by an astomosis between sexually compati ble mycelia.
(3) Hypha l fusions also lend to exchange of cytoplasm, producing
hetcroplasmons. These make it possible to Study extr.lnuc\ear genetic phenom~na . and
fungi ~re panieularly vuluable for !he investigation of cytoplasmic inheritance.
(4) The phenomenon of crossi ng-ove r. a vital part of the process of genetic
recombination, can be most degantly studied in ascomycctes like Neurospora or Sardaria.
The>e fungi havc very sho!llife cycles, Qlld eom'eniellt]y arrange the eight nuclei ~sulting
from m.:iosis and the subsequ.:'nt mitosis ill a linear sequence within the ascus. One nucleus
goe~ into each uscospore, nnd the nSCQSpores are arranged in single filt within Ihe n:umwly
cylindrical ascus. The a~ospor.:s in th is 'ordered tetrad' can be individunlly cultured and
ICS1<'d in various ways. Using appropri:ue marker genes: (a) first-division segregation can be
distinguished from sccond-dhision segregation; (b) reciprocal and non-reciprocal chromosomal exchanges can be det.:'cled; (c) chromosomes can be mapped; (d) interferen~ can be
;lUdic<J. (All the terms JUSt m~ntioned are di sc ussed in more detail below).
(5) The phenomenon of somatic crossing-ovcr was fir;t seen in the fruit fly
Orosopliila, but it can be much more easil y studied in fungi. Somali<; nudcar ftL~ions
occur. with low but predictable frequcncy in fung~1 helcroknryon s. The resulti ng d iploid
nudei occasionally undergo mitotic cross(wer. Somt: ofllie somatic diploid nuclei which
h:we undagonc mitotic cross-over cnn revert to the hapl oid condition through irregular
forms of mitosis. These haploid nuclei ha"e thus undergone genetic recombinmion without benef,t of sex , The process is called p,trastxual ity. Thanks to their production of
large numbers of uninuclcat~ ;;pores expressing specific genetic markers (t.g_ CO!Qur. or
nutritional deficiencics), conidial fun gi such as Aspergillus nidI/fans are espedally well
suited for investigations of this ph<!nom~non.
(6) Fungi can be handled rather like bacteria - many pure cultures can be
SlOte\1 in a small spact, and th~ generation timc is shon - yet fUngi ore eukaryotic, SO
resullS arc much more applicable 10 Ihe oth.:'r major kingdoms, ani mal s and plants.
Fung~1 genetics is not without its difficulti.:s. Fungal nuelei are often very small,
and we cannot do the kind of analysis .of chromosomal arrangement at the mewphase
stag.: of nuclear division that is possible in mlmy plants and animals. The drawings in Fig.
(se:c)
o
INTERPHASE
20
PROPHASE
METAPHASE
ANAPHASE A
ANAPHASE B
.r_".,__' f .
UlV ........ 't'I ISIS',
32'0'"
Ci(,_
INTERPHASE
.-'.1,
a
~
~
/'"
n~n
n~~n
i r/'"r ("V
( r ( 1 (1 (r iii i
('r
A A
r! Tr
) 00
00 )
0000
1\
....
1\
Fig. 10.2 (a) no crossing-over - f..5t division segregation pattern; (b) ~rossing-over between ascospore
~OIOUr gene and ~entrOl1lre - s.econd civision segregation pattern (see text).
,,
1
i
ways. and so remain physiologically flexible. Crossing--over is one of the main mechanisms
involved in providing the pool of variability on which natural selection a<:ts.
If we have appropriate marker genes, like the ascospore colour gene just mentioned.
we can use the incidence of crossing-over to find out roughly whcre these genes are in
relation to the cent romere (the point at which the chromatids are functionally joined. and
the last thing to separate at mitosis). How can we do this? We begin by assuming that a
chromosome is equally likely to break anywhere along its length. IT this is !rue, then the
further away from the centromere a marker gene is, the more likely it is 10 be in,"Olved in
a crossover. Also, if we have two linked marker genes, the funher apart they are on a
chromosome, the more likely they are to be separated by acrossover. This kind of information allow5 us to make chromosome maps showing the relative (though not the absolute)
locations of our marlcer genes.
Our map-making rests on the assumption that we can keep track of the products of
meiosis. In most organisms we simply cannot recover and analyze all the nuclei arising
from one meiosis. Bm amazingly enough. we can do it in some ascomycetes, because their
meiosis takes place in a long, narrow rube called an ascus. Figure 10.2 shows how the
products of the divisions lie in a straight line. SO that their exac t origin can be traced. The
example I gave above involving light and dar:\;: coloured asoospores is in fact a real one. In
Sordariafimicola. ascospore colour is detennined by a single gene. Wild-type ascospores
are dark. but there is a mlllant strain with pale spores. Since Sordariajimicoia is heterothallic (olllbreeding). the maling of a nonnal dar:\;:-spored Sirain with a mutant pale-spored
strain can be used to demonstrate some features of crossing-over. In this panicular mating.
if no crossover involving the ascospore colour gene has happened. there will be four dark
ascospores at one end of the ascus. four light oncs at the other end. as in Fig. 10.2 a. But if
the segment of chromosome bearing tb.!colour gene has been cros~d-o,cr. then each half
of the 3iiCUS wi11 contain a pair of light spores and a pair of dark Ones, as shown in Fig.
10.2 b. These pairs can appear in ~veral different ~quences, depending on which of the
chromatids undergo crossi ng.over. Crossovers c~n take place between any two of the
homologous chromatids. 50 there are four possibilities for single crossovers: 1-3. 1.4.23.
2-4.
In fact, crossing-over can be e\'en more complex than I have just described, because
it can happen twice between a particular pair of chromatids; or one chromatid can ex
change ~gments with both of its hornologues. Some of these possibilities are shown in
Fig. 10.4. Of cou rse. we can't watch these events. but we can explain the ascospore
arrangements resulting from crosses between strains with two marker genes by diagrams
~ UFPECCB
1~.
8mLI')TECA
< .
t~
CHAPTER T EN
SllCh as those in Fig. 10.4_ Not all gencs epress thcmsdvcs so immediately and un
cqui\'ocaUy as thai determining ascospore colour, bm the proce>s of segregation werks
just the same for any gene. In order to analY7.e other kinds of markers which don't express
thermelves visibly in the ascospore, we have to physically pick OUi the IIscospores (this
calls for great dexterity and lots of practice), and grow th<:m individually in culture. The
sequence of the spores inside the ascus is recorded. lind helps in the interpretation of the
subsequent genetic analysis.
As we have already seen. ifn o crossing-over happens between a particular gene and
the centromere. the four a"'t!OSpores atone end of the ascus will all be of one genotype, and
the four 01 the other end will all be of the other genotype. This arrangement is called the
'first division segregation pattern' he>;ause the tWO versions of the gene separate at first
division mciosis (see Fig. 10.2 a), But if crossingover has happened bel"'ecn the gene
and the centromere. the two different versions of the ge ne are not separated until the
second division of meiosis. This arrangement is called a 'SCl;ond di"ision segregation
,
rcz- ,
,'-' ._.
, -.
'.
-_.
~/
- . -- I -~:J
_:yj!'- J
B
)
Fig. 10.4
C~s ol
.a._
(
__L
--
-,
- ...----
~
...
=--
-~
-~
C)
.l --")
C--, -L
I . 1
:c"""t ,,= .
- --....
C
-r, -
C -
---
'..l
B
,
--
and there can be four such panems ...... hich occur with about equal frequenc~. Any
particu lar gene wi!! show a definite fr... quency of crossi ng-over, which nalu"lIly increases
as its distance from the centromere increases, The recombination frequency for any gene
will equal half of its freque ncy of crossing-over. Th is is be.::ause only two of the four
chromatids arc involvcd in any particular c rossover. If we obsel"\.'c a squashed pcrith
ecium, and find that of 20 asci. 8 show evidence o f crossing-over in the ascospore oolour
gene. we can say that the frequency of crossing-over for our marker gene is 40%, and the
recombination frequency is 20%. That figure is also a useful way of placing the marker
gene on a chromosome map. One map unit is arbitrarily defined as the disl.:lnce between
linked genes (genes on the same chromatid) that will give 1% rewmbination. The gene
mentioned above is 20 map units from the cent romere. If a second marker gene has a
reco mbination frequency of 30%, this mea[lS that it is 10 m:ip units further from the
centromere than the first marker, It CDuld be only 10 map units from that firSt marker. but
it cou ld also be 50 mllp unit~ away, on thc other side of the centromere_
With patience and de~ terity, a two-faClOf cross can be done with the ascomycete,
N tll rosp om crass(/. (Sordarialcs)_ using two linked marker g,mes (with all eles A and a. B
and b). lllree mai n ascospore pntterns will emerge.
( I) The parental ditypc , AB AS AB AB ab ab ab ab: if there is no crossing-oyer
between the two marker genes. the two tetrads of 3SCOSpores wilt reflecllhecharacteristics
of the respective parents.
(2) The tetraty~ pattern. e.g. AB AB Ab Ab aB aB ab ab: when a si ng le crossover
happen s so mewhere between the two marker ge nes. four kinds of ascospore res ult. two
paremal types and two recombinants.
as as
The rdative frequencies o f these three pntte rn s can be used to calculate the linkage
dist:mce between the Iwo marker genes, and to deduce their positions relati\'e to each
other and the centromere.
It c an also be used to discover which of the two markers is closer to the ccmro mere,
~nd whether the m:,rkers are on the sa me or opposite sidcs of the cen tromt:re. For e:o;amp!e.
we an;llyze the ascospore arrangements resulting from a two-factor cross. and find that
there are 56 p,an:ntal ditypc asci. 44 tetrntype asci, and 0 non-parental ditypc asci. What
can we deduce from these data? tr tho: marker genes were unlinked (i. e. nOt on the same
chromosome). the frequency of pare ntal ditypc and non-parental ditypc asci would be
expected to be the same. Since no non-parental ditype asd are recorded. we can ass ume
that the two m~rkers afC linked (i,e .. on the same chromosome). In order to be able to pla~e
the markers in tbeir correct relationship to eac h other and the CC[llfomere. \\1(.' need to
aoalYle the 44 t<::trJtype asci fun her. Wc note that there arc lhree arrangements:
(i) 24 are AS AB Ab Ab as ~ S nb ab
(i i) 19 arc AS AB ab abAB AS ab ab
(iii) I hAS AS
aB Ab Ab ab ab
The marker genc~ could theoretically be arranged in one of three ways with respect
to the centromere:
as
(f) Centromere -
Aa - Bb
(If) C~ntromcre - Bb-A>
(II/) Aa - Centromcre - Bb
168 C H APTER TE N
mycelia may be morph.ologically indistinguishable, yet invisible incompatibility factors
can prevent their mating. Incompatibility can prcvent anastomosis. or prevent karyogamy. In fungi like the ascomyce tes. wherc fusion of assimilati\'e hyphae does not initiate
the sexual process, vegetative incompatibility is not a barrier to sexual reproduction. and
is often determined. by entirely separate genes, so that a sin gle speci~s may be divided up
into a number of vegetati ve compatibility groups (VCGs). Such ascomycetous taxa as
Crypiwneclria parasitica (Diaporthales). NeJ<T()spora CT{Jna (Sorelariaies). and Fusarillnl
mOllilif()~(anamorphic Hypocreales). contain manyVCGs. In the basidiomycetes, where
fusion of ordinary, und ifferentiated assimilative hyphae is a prerequisite to the estahlishment of the dikaryophase, and dikaryotilmion a prerequ isite of karyoga my, vegetative
incompatibiJiry can effectively pre"ent sexual reproduction.
Basically, heterothallism implies that a haploid nu<:leus can complete the life cycle
only if it mates with another haploid nucleus carrying a different mating-type factor.
Heterotha ll ism is the fungal eq ui valent of the separate sexes found in many philltS and
animals. As we shall sec, the fungi. despite their restricted genome and relatively eonsistent organization. have evolved many and complex variatioM on this sexual theme.
The simplest kind of genetic system that can ensure olllbreeding consists of twO
"'iITerent alleles, which weean label 'A' and 'a: at the same locus. Pairs of mycelia carrying
the same allele will be incompatible (A ..... ith A. Of a wilh a), while pairs of mycelia with
different alleles (A and a) will be compat ible. This system effecti\'cly divides a population into two catcgories. and has the same eIT.eet as d ivision into two sexes . This two-allele
system is found in all groups of fungi other than the most highl y evolved basidiomycetes.
Examples or.: the zygomycetes Rhizopus and Phycom)"ces . species of the ascomycete
genera Nl'ltros(HJro, /umbo/us and SclerQlilliu. and species of the tdiomycete gellCra
Puccillia anq VS Ii/ago.
It has been found thai the genes at the 1111'0 loci often control different pans of the
dikaryOlizatiOll process. In the basidiomywes Coprinus /og~ and Schiz.op/lyllum commime, clamp connections de,-elop only if the dikaryoo is heterozygous (has different andes)
fOf the A locus. For e;.:ample. AI B I A2 B I would h.we hyphae with d amps, A l BI A I 6 2
""Ould nOi. Nuclear migmtion is controlled by the B locus, and would fail in A I BI A2 B I.
Of 230 species of Aphyllophorales. Agaricales and gasteromycetes examined. 1015% were homoth allic. about 35% were bipolar hel~rothal!ic . and about 55% tetrapolar
heterothallic.1t has been esti mated thut Schi!ophyllllm communI! probably has about 340
+ 120 different A Jlleles. and 64 + 12 different B alleles. Estimates in some other basidi
omycetes are of the ord~ r of 100 different al leles for eJch locus. thollgh the bird 's-nest
fun gi. Cye/hllI .Ilriallls and Crllcibu/um vulgare. nre be lieved 10 have on ly about 10
alleles for each locus _
Second3ry homolhalli~m can occur in heterothullic fungi. If an ascus conta ins only
four spores, as in Nellrospora lelrasperma. instead. of eight. there can be a compatible pair
of nuclei in each spore. Similarly, if a basidium bears only two spores. as in AgariClIs
bnuUlucellS, each of these may also contain two compatible nucle i. Homothallism is
possible. ewn in species with fourspored basidia. If an extra mitosis happens in the
basidia, two compati ble nucld may find their way into some of the basid iospores.
Homothallis m can also be introduced in what would otherwise be a heterothallic
fungus by mating-type switching . In addition to the fu nctional mating type aUele at the
uct ive loc us, SaccharumyC(s cuev[.riee has 's ilent' copic, of mJting-type :lUcks at two
o lher loci. A site_specific endonuclease cuts the double stranded DNA at th e active locu S.
The resull ing gap is the n r~ pajred by sp licing in DNA from one of the loc i at which the
silent copies resi de. This often means that onc all dc is replaced by the other. .~ the
mating-type of the organism is sw itched. Similar swi tchi ng occurs in another yeas t.
SchiW$Occharomyces pombe. and in the filamentous ascomycetcs. SclerOlinialrifoliomm.
Chromocrea spiJ1l1fosa. and Gfomueffa cin.~lIfa/a. though the mechanism is still obscure
in those fungi. The switching in ChromOCftfl and Sderorinia happens in only one direction. If the mechanisms in,-ol\"ed are like that found in Saccharomyces, it is likely that
only one of the mating-trpc alleles is present in a silent form. We do nOI yet know ho .....
much fungal homotha ll i:im can be accounted for by mating -type switching. In some
fungi. se lf-sterile spores with a single nllelCUS, and self-fertile spores with two nuclei. are
both de ve loped in the same fruit body. This kind of mating behavi our is cuBed
umphithallism.
Recognizing the e~istence or compatibility genes is one thing. understanding how
they work is another_ The best-documented compatibility system is (hat of the yeast.
Sacch(lromyces c"ft,'isiaf _l"kr~ ttlc re is a single locus with two alleles. Each m~ting type
sec reteS a constilUtivc polypeptide pheromone wh ich causes cdls or the opposite mating
Interster ilit y
Compatible mating-types are not always enough to ensure successful sex. Sometimes. mnting fai ls despite apparent co mpatibili ty. There is therefore another genetic
system, which we can call an intersterility system. that can override the usual incom(Xltibiliry system. Unfortunately. weOOn't know nearly as much about the basis orthis sy$lem
as we do about incompatibility. The ki nds of barri crs invol ved are eithcr llrezygotic.
preventing ferti lization, or postzygQlic. res ulting in hybrids of reduced fertility or meiot ic offspring less fit than the parents.
Pretygotic barriers exist bet ...'ce n closely related populations of many well-known
basidiomycetes, including Amlillaria, Callybht. Capri/lwi. w ccari(l. Pnxillus. Pieuroflls.
Gtmoof!Tma and Hettrobusidion. Since intersterility is usually complete, particularly in
sympatric populations. the intersterile groups are equivalent to biological specic.~. In
some of these fungi, DNA reassoci3tionor DNA restriction fragment patte rns have shown
th~t the intersteri le groups 3re Jlso genomically divergent. Sometimes two enti rely intersterile sympatric popu lations are partly interfcrtile with a third population from anotller
arca. We do not yet know whether this thin! population could aCt as bridge between the
other two soli tudes. In Usrilago c),nodol1li$, intersterile popul Jtions and partly interfcrtile 'bridging' strains coexist within what appears to be a single complex species.
Posl7.ygotic barriers are present when malingoccurs, but mOSt of the resul!ing spores
are not viable. In closely related hetewthallic Ne tlrospora species. the reproductive barricrs appear to be mostly postzygotic. Intraspo..'Cific cross~s yield viable ascospores. but
interspecific crosses produce largely non-\iable ascospores.
Parasexuality
Ascomycetes and basidiomycetes can be easily di stinguished when they reproduce
sexually. In this phase (the teleomorph) they form characteristic frttiting bodics (ascomata
and basid iomata) bearing unique me iosporang ia (asci and basidia) fro m wh ich, as we
h31'e seen, the products of a single meiotic event can ~ isolated and anJlp.ed. Many of
these fungi repmduce asexually as welL producing what are called anamorphs. which
form mitospores called conidia, and often occur wen separated in time and space from the
telcomorph. In fuct. we know thousands of anamorphs which have nOl yet been persuadcd
to metamorphose into a telcomorph. :"Iany of these go on. generation after gcneration. in
the 3sexual condition. and it now appears highly probable that many of them have entirely lost the ability to produce a telcomorph. thus becoming anamorphic holomo rphs .
We know th3t one of thc most vital functions performed by the tc leomorph is
genetic recombination. This rea.~s.onment of the gene pool during meiosis broadens the
ability of the population to cope wi(jt the stresses imposed by changing environments.
Conidial fungi, which are often highly opportunistic. and grow on a wide range of sub-
ru
UFPE-CCB
~ BIBLIOTECA
means that linkage analysis is mueh easier. The original diploids arc heterozygous for the
various marker genes. Those in which crossi ng_over sub,equenily occurs will become
homozygous for any marter genes that are distal to the point of crossover. The relative
frequencies with which such markcrs become homozygous ~ an indkation of their relative distance.~ from the centromere.
Extranuclear Inheritan ce
Some genetic phenomena can't be explained by reference 10 nuclear or chromosomal events. The logical corollary of lhis is thlltthe determinants may be tnlnsmined in
cytoplasm rather than in nudei. In some helerothallic fungi, the volume of cytoplasm Ihat
ae<:omp;mies one of the nuclei during a sexual fusion may be muth greater than that
associated with th e other nucleus. Al ternatively, iF one side of the fusion involves a
microconidium or a spermatium. this must inevitably bring much less cytoplasm to the
union than does the receiving panner. This sometimes results in tnc offspring resembling
the parent that contributed more cytoplasm, and implies the existeoce of cytoplasmit
gen es. It has been shown that in Aspergillus glaucIIs, attributes such as spore germination,
growth rate, pigmentation, and dens ity of perithecia ore under cytoplasmic control. A
well-known example of cytoplasmic control is the 'poky' mutam of Neurospora Crtlssu.
This grows more slowly than the wild-type, and cannot be speeded up by dietary supplements. If 'poky' is crossed with the wild-type, the 'poky' CQlldition is transmitted only
when the 'poky' str:lin forms the perithecium initial. which means thai it is essentially the
matcma l parent.
Another well-known example of extranuclear inheritance is the <petite' strain of
Sacc1raromyasurtvisiae. which ari~ with a frequency of abotH I etll in 50ll SuchccUs
give rise to smaller than normal colonies. which can respire only anaerobically, even
when oxygen is prescnt. This deficiency is due to Ihe absen<;e of impor!ant respiratory
enzymes such as cytochro me oxidase and sucdllie dehydrogenase. The mitochondria are
defective. Whole colonies can be com'cned to 'peli te' cells by growing them on medium
containing 3 ppm atriflavine. Di ploid "petite' cells don', R:produee sexually, but diploid
hybrid s derived from 'pctite' and normal haploid cells respire aerobically and can form
a.scus-Iike mciosporangia. If the meiospores are cultured. all are nonnal, and 'pctite' cells
ari ~ among their offspring only in the ominory 1:500 rolio. Normol yeast cells co ntain
cytoplasmic genes (in mitochondria) tontrolling the synthesis of respiratory cnzymes_
'Pctitc~' arise by mutations in the mitochondrial DN A. When a cell containing this tytoplasmic mut:lnt fuses with a nomlal haploid cell, the cxtranuclear genes from the normal
~ell rende r the resulting diploid normal again, and nornla! mitochondria find their way
into any r~su l tant haploid cells, which will all therefore be nonua!.
carry none, one, tv.'O, or all three of these genes. With the ai d of these hoSt varietie~. eight
races o f CladQsporillmjulVlun cao be discriminated. TIl.! most efficient way to differentiate these races is with three tomato varieties which ha\c. re,pectively, resistance genes I,
2 and 3, as can be seen from Table 10.1. 1 you examine me ei ght columns which give the
responses of the three tomato varieties to the different fungal races, you will see thnt each
column diffcrs from all the others. This means tha t ilny of the eight races Ciln b<l identified
by tes ti ng it against only three tomato variet ies.
Thble 10. 1
Clado.!porium roces
1+2
1+3
2+3
1+2+3
!~ liFP E-CCilil \
,,>
j-.
175
facilitates subsequent digestion of the cell wail. (2) The wall is digested by mixtures of
glucanases derived from snails or bacteria. (3) The resulting p rotoplasts (oflen called
spheroplasts) are washed and suspended in a stabilizing solution (0.6 M KCl or 0.8 M
sorbitol) to which is added the foreign DNA (vector incorporating the desired sequences).
(4 ) Uptake of the plasmid DNA during protoplast fusion is promoted by adding polyethylene glycol. (5) The tmnsfonned protoplasts are then allowed to regenerate a wall, and
are grown on a selecth'e medium (one containing a specific antibiotic, o r with a panicular
food substrate. depending on which marke r genes were used) which will allow only
appropriately transfonned cells to grow (because only they carry the appropriate marker
gene, which came with the vector and confers resistance to that antibiotic or the ability tu
metabolize that particular substrate).
The alkali s.aJ.t method permitS transfonn:uion of intact cells. Cells are incubated in
lithium acetate to make them competent. i.e. receptive to exogenous DNA. 1bc: DNA is
then incOl'pOrated in the presence of polyetheylene glycol 4000. Although transfonnation is less efficient than with protoplasts, the procedure is simple and quick. cells can be
stored for weeks without loss of co mpetence. and the problem of diploid fonnatioll during
protoplast fu sion is avoided.
The first demonstration that yeast could be transfonned with ell.oge nous DNA was
made in 1978, using a recombinant bacterial plasmid carrying the Saccharomyces Cl!"I'isiae
gene for an enzyme needed in the synthesis of leucine (LEU 2). This ge ne had earlier been
recognized in E. coli because it complemented a mutation in the bac terium that had
caused the loss of (he same enzyme. Several other yeast genes have now been clotlcd in .
wll by complementation of other bacterial mutants. These are useful marke rs which ca n
be inrorpornted in the ell.oge nous DNA along with the desired gent: their uptake an d
subsequent expression in yeast cells allows recognition and selection of yeast cells .... hich
have been appropri ately transformed: that is, which now carry the desired donor gene.
Most strains of Saccharomyces Cl!Tevisiae contain up to a hundred '211m pla s mid~'
per cell. Ench plasmid has about 6.300 base pairs. Hybrid plas mids made up of the entire
l!1m sequence. plus the LEU 2 yeast gene, plus a bacterial vector sequence, efficiently
transfonn )east celli that lac k the LEU 2 gene (As a consequence of the bacterial vector
sequence DNA having been repl icated in a baCteriuru. the 211m plasmid also works in .
coli, so it can serve as a 'shuule vector'). The complementatioll of the LEU 2 gene means
that those cells which have been properly transfonned can be selec tively isolated un
leucine-free medium, and subseq uently multipli cd. It has also been demonstrated th nt the
hybrid plasm id replicates in transformed cells. However. it appears that smaller plasmid s
containing only a fragment of 211m DNA are more versatile, gi\i ng higher frequencies of
transformation. and more copies of the plasmid in each transformed edl (up to 300). All
stages of gene-cloning can be carried OUt in yeast. but it is usually more efficient to
amplify recombinant plasmids in E. coli. The most important aim of the cloning exercise
may be to obtain gene products. but cloning also lets us produce a lot of homogeneous
DNA, which can then be used in the sequencing of ge nes.
1
!
Translation
Initiation
11gnals
TranslaUon
control region
(promot&f)
DNA encodIng
signal peptlcla
lor secretion
Fig. 10.5 Components of a fungal gene.
Polyadenylatlon
and transer!ptlon
termina-tloll 11g:nals
PSI I
IPA cDNA
Xba I
IpiA lerminalor
tpiA promOIer
Psi I
pM159
Xba I [PuvlIJ
arg8
BamH I
Xba I [PuvllJ
theexpres~iooof
180 CHAPTER T EN
mose. nuclei migrate but mitochondria do not. so the resulting mycelium is uniform in its
nuclear component. but has at least twO seclOrs with different mitochond.rial genotype,.
Therefore. an examination of mitochondrial DNA polymorph isms can now help us disCO"cr the history of those clones.
The uses of molecular technique~ in mycol og y are multiplying. and I must begin by
warning my readers that it is almost impossible for any publication to keep pace with the
lntest developments in thi s field. However. the attempt must be made!
DNA sequencin g. usually after amplification by PCR (the polymerase chain reaction). is now being used to idemify important fi.mSi . such as commercially grown specie,
or serious plam pathogens. or to find the appropriate talonomic niche for fungi whose
ta.wnomic position is problematic. A small r",gio n oftbe genome of several individuals in
one species is compnred to the DNA .~eq uence of the eql.livaJent region in other taxa_
Currently the region being sequenced and compared most commonly is the rRNA (ribosomal RN A) operon. This operon consists of three genes under the control of a single
promoter. The genes are: (1) the small subunit gene (SSU). (2) the 5.85 gene. and (3) Ihe
lars~ subunit gene(lSU). Fortu nalely. in most fungi these genes are alT'.mged in Ihat order.
and so CJn be located and compared. The fiTht gene transcribed is the SSU. After this comes
an irllergenie Spacer Region (IGS) which contains an intem3ltranscribed spacer region
(ITS I). the 5.8S gene . and a sc<:ond transc ribed spacer region (ITS region 2). At the Olher
end of me IGS is the LSU.
The rRNA operon is pan of a mUlti -gene family consist ing of repeated array~ of
operons. Different genes arid reg ions in the rRNA operon have differem degn.""Cs o f $Cquem:e conservation (the likelihood that changes will enter the sequence of base pairs
01 er time). Th: vnt)'ing pres,ure for sequence conservation is due to the differing degre es
of importance of the different sequences: areas th at are less imponant in the function of
the genes tend to vary more than areas that arc crucial. This is beeause Jny ch ~nges in
th ,"c crucial areas might wreck the gene's ability to make its product. The rather mySleri au. Internal Transcribed Spacer regions (ITS). since they do nO{ themselves code for a
g~ll~ produc t. are fnr more variable than the genes. The ITS regions have pwved most
suitabk for comparisons between rdated species. T he 5.8S gene is small. highly consef\~d and w o f liule value for phylogenetic comparison. The SSU is also conserved. b ut
~in,c it is larger than the 5.85 gene. more variation has crept in. and it has hccn used for
cumpmsons among genera and higher la:ta. 1bc LS U is the Icast conSCf\\!d of the threee
gene> and hJo; allowed comparisons within nnd bctWtCll 5pecie~_
0:-<.-'1. s~quencing after PCR amplificJlion has been used to idemify speck'~ of
Am:i!/"ri(l (an d m,my other fun gi). But these technique s are 110t rest ricted to identification of known species. Th~y c,m also be used to conm:ct or compare previously unidentifiabk mycelial (nen-sporulating ) cultures with fungi that have been identified using thdr
sporulating st rucltlrcs (whether sex ual ltelc mnolllhic 1or ns.:::t ual {annmorphic1). The ON A
protlk, of non -fruiting eultures havc been comp;=d with the profiles from D;.YA iwlnl<!d
from (ruit hodi<,s of Amlil/a n". nnll with thi, evidence in hand. new species of Armillaria
ha\c b.!~ f1 described. This raises some problems. such as how the ne w t3J\n could be
idcntif;~d without reso!1tO e~pcnsi'-e and time-c(>n'>uming molecular techniques. but the
da: (of a handheld sequencer sure ly e;mnot lie more thnn a decade in the futllre!
At present. 1!ouC\er. sequencing e"ery fungJI isolate to identify it is far too tim\!"'on.l~ming and e.~pensive. Thcr~ fore. a quicker and simpler technique based on the po!ym~r.I"~ ch3in ~;'\(.tjon (PCR) and the specificit)' of restriction enzymes (ReStriction Fragmem Length Polymorphisms Of RFLPs) has ~ Il d<,vi scd. This is the "PCRfRFLP" tech
nique. It invol\"es the ampliiicatioo of a specific gene or region of the senorne by PCR. The
amphfi~d fragmentofOi'OA is then cut" ith oneer more restriction enzyll1CS. and the resu lt-
I
I
1
I
Genome Projects
...l ost people are aware that a large number of laboratories are ~"()lI~lbornling in the
!>Cquencing of the tlllin:: human geoome. This is 3 hugc projcct and is nOt eXpo:1:led to be
completed for some time. But the entire geoo/l"lC5 of some othcr org3nism) have 3lready
been sequen~d: these include many viruses. some bacteria andonc fungus. SIIct;hllrQm)"Ce)'
ctrr-.isille (ba.l;:ers and brewer' s yeast). The genome of SacdwromYCt:$ ha.<; been founelto
contain nbollt l2 milliDn base pairs w\th about 6,000 recognizable g~nes. divld~d among
16 chromosomes. The SaccharomY"fS genome is the first fungal genome to ha\'~ been
completely seqLlenced. bu t other genome proj~cts are under construction for such mainSlays of genetics as NnnQ;pOI"ll era.lsn and As,nrgillll;' nidlilims. All of these projects will
make it easier 10 place any sequcnced fragment. and thus to know where specific genes are.
Dnd ""h;!llheir funclioflS are. The future of fungal genelics looks c:<.citing.
:i
182 C HAPTER TE N
Mycoviruses
Hypovirulence or reduced virulence associated with the presence of dsRt'\'A has
become a well recognized phenomenon in some fungal pathogens. The first of these
mycoviruses to be well characterized was the so-called "hypovirus," so named because it
causes hypovirulence (reduced pa thogenicity) in the chestnut blight fungus,
CT)'phollcclTia parasilica. This virus apparen tly has no coat protein, and can' t exist
outside the fungal celL It is transmitted from one strain of the fungus to the next during
anastomosis (the fusion of somatic hyphae). Fungal mycelia are capable of anastomosis
only when they belong to the same vcgetative compatibility group (VeG). Diverse fungal
populations with many d ifferent VeGs will tend to inhibit the spread of the virus. So,
while mycoviruses are potentially [Xllent biocontrol agents for fungal pathogens. they are
likely to be more effective in pathogen populations wi th low genetic diversity. A growing
number of mycoviruses have been found in fungi. Some, like the Crypholleclriaparasilica
hypovirus , are associated with symptoms such as reduced virulence of the pathogen
(similar viruses have been found in other ascomycetes such as Ophiostoma ulmi and
Diaporthe ambigua). Other myc oviruses are cryptic. The best known of the more cr)'ptic
mycoviruses are found in the well studied yeast. Saccharomyces cerevisiae. These viruses
are a%ociated with the killer yeast phenomenon , where one of the viral genomes codc~
only for a protein toxin. The other genomes code only for a coat protein and an RNAdependent RNA [Xllymerase. Neither of these last two genomes have any apparent negative effect on their host. Most mycoviruses do not appear to be closely related. and a
number are based on DNA sequences rather similar to those of some plant viruses.
Further Reading
Beggs, J.D. (1981) Gene cloning in yeast. pp. 175203 (in) Genetic Enginee ri ng 2. (cd.)
R. Williamson. Ac~demic Press, New York.
Bennett. J .W. an d L.L. Lasure (Eds. ) (1985) Gene Manipulations in Fungi. Academi c
Press. Orlando.
Bennen. L\V. and L.L. L~sure (1991) M ore Gen e Man ipulations in Fungi. Academi c
Press. New York.
Berka. R.M. and C C Barnett (\989) The development of gene expression systems for
ti lamentOlls fllngi _ Biotechnology Advances 7: 127- 154.
Blum. H . H. Beier ~[1{1 H J . Gross (1987) Improved silver staini ng of plant protcins, RNA
and DNA in polyacrylamide gels. Electro pho resis 8: 93-99.
Brasier. C!-.l. (1987) The dynamics offungal speciation (in) E ~'olu tionary Biology ofl he
Fungi. (Eds) A.D.t.1. Rayner. CM. B r~sier and D. Moore. Cambridge University
Press. Cambridge.
Bruns. T.D .. T.J. White and J. W. Taylor (1991) Fung~1 molecu lar systematics. Ann. Rey.
Ecol. Sys l. 22: 525-564.
Bruns. T.D .. R. Fogel, TJ. White and 1.0. Palmer (1989) Accelerated evolution of a falsetrumc from a mushroom ancestor. Na ture 339: 140- 142.
Bruns. T.D. and 1.0. Palmer (! 989) Evolution of mushroom mitochondrial DNA: Suilh,s
and rdated genera. Journal of Molecu la r E ~'ol utio n 28: 349362.
Burnett. 1.H. (1975) j\lycogenetics. Wiley, London.
Burnie. J.P.. R.C Matthews, I. Clark and L.LR. Milne (1989) Immunoblot tingerprinting
of Aspergilfus/umigaws. Journal of Immunological !-.let ho ds 118: 179-186.
I
,
UFPECCB '
~ 'B''- 1 i.)
r-. -:!": ...
~ vf"'A
1J1
Fungal Ecology
11
Ecology is the study of organisms as lh~y relate to each other and their enviJo[\
ment. II must be 3pparenl lhat el'en in the taxonomic chapters I &a\'c a lot of ecological
infonnation. Think of the effects that fungi ha\"e had on people: the potato famine, the
downy mildew of ttlc French grope \ines. the blue mould of Canadian tobacco. the way
chestnut blight removed an important species from Ihe forests of eastern North America,
and the more recent loss of the beautiful American elm trees to Dutch elm disease. Fungi
may aller tbe
e~ology
175 gcneraofascomyceles are largely or aclusivdy found on dung. The extremely advanced
anctsuccessfuJ agaric genus Cuprinus hlS many specico; Ih:ltoccurexclushely on dung. Tht.--re
are also many ~peci:ilizcd dunginm.biting lygom~eetes. among which Piluboills and 50mc
184
And finally the BasidiomyceteS, main ly small (but profuse) species of the agaric
genus Coprinlls with liny caps, black spores, ~nd autolysing gills.
It has he<:n suggested that Ihis is a true ecological succession. albeit a miniature and
condensed one. Initially it was poStu lated thllthe seqllcnce wa~ a nutritional on e. Zygomycd es "111 generally a,similate only fairly access ibk carbon sources. such as sugars.
Their fast growth was assumed \0 give them an advan tage in findin!! the~e. and the ir early
dis.appearanCe was thought 10 be due to the e",h:tu5tion afthis substrate. The ascomycetes
and C1)nidinl anamarphs mat appeared nex t were assumed to bc able to as.<>imilatc m~
comple)( caroon sources such as hemicellulose and cellulose; while the basidiomycetes.
appearing last and persisting longest, were able to exploit both cellulose and lignin.
But when this hypothesis was scrutinized more carefully and tested by experiment
and Ilmher observation, it did not hold up. The growth rates of the various fungi were
found to be relatively similar, and the various carbon sources were not exhausted as
quickly il$ had been assumed, So a second hypothesi s was advanced. This one was based
on the time it took for each kind offungus 10 accumu late enough food reserves to pennit
it to fruit. It was argued that the simple sporangiophores of the zygomycetes cou ld be
developed after only a short period, whil e the more elaborate fruit bodies of tho: ascomycetes would require a longer build-up, and the even larger basidiomata of the coprini
wou ld need the longest preparation of aiL TI)is is a more reasonahle hypothesis, because
if wo: grow some of the dUllg fungi on laboratory media, we find that it takes Mucor
hielno/is 2-3 days to sporulme, while Sordaria fimicola needs 9-10 days, and Coprinus
Ireptemerus 7-13 days,
Some of the KickAeliales, zygomycetes often found on the dung of sedentary mJmmals (those with a defined home base, a small territory, and habitually used paths), produce eXlrt:mely complex and convoluted anamorphs_ Spimdactylon, possibly the most
complex of all. produces tall, branched sporangiophores that bear liny coil s w ithin whieh
develop innumerable one-spored sporangia (Fig, 3.4 F), The whole structure must be
dcsigned to catch on the hairs orthe rat or mouse as it passes by. This is made possible by
the habit;; 0[" the animal which. although it doesn't eat its own dung_ at least deposits it
somewhere along one of the trails it follows every day in its journeys to and from its den
or burrow. The final step, the ingestion of the spores, is presumably taken when the animal
grooms itself. JS mammals (other than human children) habitually do, Some coprophiloU!;
hyphomycetes (e.g., Graphillm) produce slimy droplets of conidia at the top of tJIl conidiophol\'$ or synnemaml conidiomala, Thcse spores are presumably dispersed by arthropods
which may Ihemsel ves specialize in seeking out dung, and may thus act as spec ifi c, and
very efficknt, "ectors for the slimy -spored fungi.
So we can assume that an assortment of spores of coprophilous fungi will be present
in dung wh~n it b deposited, and th at these will all have been triggered to germinnte by
some as!X'ct of passage through the mammalian gut. Whik Pi/obo/us is producing its
miniaturc artillcry c)(travaganza, the other fungi are growing and assimilating steadily
within the dung, preparing for their own appearance at the surface. The new hypothesis
had oeg\ecl~d only one imporwnt fa<:lor: antagonbm, After a few weeks , almost the only
fungi still sporu lati ng on the dung will be species of Coprillus, Th~se CJn go on producing J sequence of ephe meral basidiomata for months_ We now know that the various
compon~m5 of the substrate are far from e)(hausled after the initial flushes of growth and
sporulation_ What has l\'aU)' happened is that Coprinus ha> seized contro l by supprc ssing
most of the other fungi. Hyphae of Coprimls are actually extremely antagonistic to those
of many oth~r coprophilou$ fungi. If a Coprinus hypha touches Olle belonging to
Ascoliolll'i, the Aswboilis hypha collupses within minutes, We don 'I understand exactly
how this trick is done, but it is e~treme l y effective. and turns out to be a fJirly common
strntagem among the fung i, whose main competi tors for many subslrntes are other fungi_
Another intercsting and important gamhit used by Coprinu.1 involves repeated
3nastomoses_ Spores are more or less evcnly dispersed throughout the dung when it is
d~posited (Fig, 11.1 A), ~nd they all germinate more or less simuitJneously, producing
, mall mycelia wilhin the dung (Fig, 11.1 R C). When compatible mycelia meet, they will
~ nastomose. and soon the entire dung deposit is permeated by what is now essen tinll y a
sin gle mycel ium (Fig, 11 . 1 D), which can then pool its re,ources and produce more and
larger basidiomata , Cooperation pays off for Coprillus.
am
UFPE-CCB
~BIB L IOTECA
And don.'t forget the Interesting subplot.> that run concurrently with the mmn story
Several of the zYg<lmycc!cs that usually appear (e,g., Piptocephalis) are actually parasitic
on other zygomycetes, One common zygomyccte. Rhopalomyces eiegmls, parasitizes
nematode eggs. Nematode-trapping fungi such as ArrhrobOirys often sporulate, and devdop their characteristic rings and nets (see chapter 15). Keratinolytic hyphomycctcs
such as Microsporwn may appear on hair thm the animal has acridcmally eaten during
grooming.
Occasionally, an undescribed species of fungus may be seen. For many years the
third year mycology class at Waterloo followed the dung succession as a laboratory
exercise . These undergraduates saw the zygomycete Stylopage allOmaia 011 horse dUllg
several years before it was formally described ill 1983. They also found an undescribed
species of Podospora (Ascomycetes). which is perhaps the 102nd species of this genus.
They also found the rare zygomycete, Helicocepha/um, which I had never seen before.
(Who says your students can't teach you anything?)
Horsedung is easy to obtain in most areas, comes in discrete units, andcan be handled
and observed without creating much personal distress . As many as 40 species of fungi
representing most major groups of eumycotan fungi arc commonly recorded from a single
collection of horse dung. Most of them can be identified fairly easily 10 genus with the help
of the specialized taxonomic literature that is now readily available (and by looking at the
pictures on the CD-ROM version), tbough , admit that some of tbe zygomycetes are not
easily recognized as such by beginners. Many of th~ fungi can be isolated in pure culture
without too much difficulty, and with a linle imagination. interesting experiments can be
devised to investigate various aspects of their behaviour. Perhaps now you can understand
why I and many other teaching mycologists ask OUf classes to put their culturally determined attitudes on hold, adopl an objective scientific approach. and study the Sf.lccession or
fungi on horse dung. then think about the biological mechanisms and manoeuvring that lie
Fig. 11 .1 Behaviour of Coprinus in dung. A:spores present when dung is deposited; B; spores
germinate synchronously; C: mycelia anastomose; 0: c:omposite mycel"lUITI c:an exploit the entir<:
substrate and produce large basiO!OfTlata.
a mi
cromanipulator and giving them a variety o f delicious media. But they refused to grow. so
I eventually decided Ihat most of them must be dead. and that they had perha ps grown at
some other time and in some other place. I looked in the organic horizon above the
mineral soil. and found there a thrivit1g community of lillerdecomposing fungi. which I
proceeded to investigate (I did not realize it at tnc time. but this is fairly typical of PhD
projects, which 1IfC often changed in mid-course by unfol"C5eet1 events).
The pille needles making up the litter unde("\\-'ent a gradual transition from L- Fl -FlH layers oflhe organic horizon of the soil. I then decided to examine as many needlcs from
each layer and sub-layer as I CQuld process each month (the number turned out to be 300).
Living needles from lhe tree rcpresemed stage Olle it1 fungal colonization. Recemly dead
ncedlesconstilUted the L layer(pale brown). below which lay the upper FI (needles much
darker. but still tough ), then the lower Fl (needles blackish and softer). and finally the F2
(neeules greyish and fragmenting). By the time liner material entcred the H layer. it was no
longer w:ognizable as individual needles. Needle were treated in \'arious ways . (I) Some
........ ....".1....
c.... , ,;
,.,;
"
....... ...
'-~"'''.
. ..... .
~"
,~
...,..
'.... ,..
1,
,, ,
,
,,
,...... ,....."".
".
.......' ..,."....
Fig 11 .2 Gener<olized scheme of the foxogal successionn Pinus sy/vesfrls ~ shoo.vng the
1O""(.lOf:t1 and ;pollial relatiOnsl"Vps oi the f~i mainly coocerned in the breakdown process
T.able ll.l
Provisional biomass estimates and arulUalliner production for
Meathop Wood soil (after Satchell 1970)
Group
Bacteria
7.3
Actinomycetes
0.2
Fungi
454.0
Protozoa
1.0
Ncmatodes
2.0
Earthwonns
12.0
Enchytraeidae
4.0
Molluscs
5.0
Acari
1.0
CoUembola
2.0
Dipiero
3.0
Other arthropods
6.0
TOIal biomass
497.5
Annuallittcr production
7640.0
were washed repeatedly to remove loose surface spores and plated out in segments to
isol:ue fungi on and in the needles. (2) Some were surface steri1i7.l'<i before plating out. to
select fO intemll coloni1.ers. (J) Some were Walt-embedded and sectioned. (4) Some were
obser..ed directly over a period of incubation in damp chambers.
One of the first dramatic changes is the development of numerous ascomata of
Lophodennilllll pil1(/$/ri. which apparently often ~olonizes the interior of living needles
without producing ovcrt symptoms - in fact . it may be in~olved in deterring herbivores
from eati ng the living needles. The death and fall of the needle stimul ates this fungus to
fruit. The large number of lenticular black ascomata of Lophodermi/ll/l that can occur in a
single needle indicutes that it is a dominant colonizer. Other fungi fruit in Other needlesindividual needles may thus travel along several dccompositionll paths. though the
average time it takes a needle to become humified is about nine years. One pathway
begins with WpllQdumium. anothcr with p),cnidial conidiomat:l of l coelomycetous
anamorph. Fusic{)CL-UIil (holomorph probably BOIT)"mphaeria). The interior of the needle
b<gins to brenk down under the auacks of the fungi.
Meanwhile, on the surface of the needle. networks of dnrk hyphae develop. But
whm fungi do they represent? Mycelium without sporulntlng suucturcs is not very helpful unless one has access 10 moiccui.u- techniques. Fortunately. several of Ihese fungi
fruited either in nature or in damp chambers. The rU"S1 of these w3S SIiItl(lCOIII)"Ce$ monosporu
(which I mistlkenly described in 1958 as a species of /leUcoma). A sel'Ond major surface
~ UFPECCll
~1l\B110"!i.CA
~ ,-,
. dikaryomycolan fungi. However, if you collect some stream foom and examine it under
the microscope. you will see that the bubbles"have uapped a rather unusual kind of multi~
armed spore (this is simply a physical phenomenon - a surface tCl15ion effect _ and theTe
is no other relationship between the bubbles and the spo.-es). In fact. the water contains
what we call tetraradiate spores of many Sile.~. Pass a litre of stream water through a filler,
then stain the filter in conon blue and examine it through the microscope. and you win
see morc of these often large and strikingly shaped tetraradiate fungal spores (Fig. 1\ .3).
Other spores will be unbranched, long, thin and arc-shaped, sinllate or sigmoid (s-shaped),
All are produced by conidial anamorphs tho! are specially adapted for living in Streams.
Where do these spores come from. and how do the fungi that produce them make a Jiving?
The first due came when limnologists (biologists specializing in freshwBt~r systems) began to examine the energy budg~tsof streams. Because some Streams now through
forests. th~y are heavily shaded during the growing season. This mc:ms that few green
plants (primary producers) can grow in them. It was found that more th:m half, and SOillCtimes nearly all. of the energy supponing organisms that live in streams comes from
.lulUmn-shed leaves of trees that grow over the Streams. This source of energy is de~cri~
as 'alloc hthonous' (which means ',,:oming from somewhere else').
When they flnt fall into the water, these: leaves are extremely unpalatable to Stream
invertebrates. but as they are colonized and 'conditioned' by microorganisms, they apparently be<:ome tastier. Ex perimentS in which batches of leaves were trellted with eithcr
anti fungal or antibacterial amihiotics sllowed that the fungi were ehiefly instrumental in
making leaves palatahle to animals such as Gammam_1 pselldolimnat lls. a numerous
amphipod crustacean living in the Stream (another amphipod lives on the beach below
my house in millions. eating decayin g tidal jctsam, mostly seaweeds and, no doubt. the
fungi growi ng on and in them). In a feeding experimcm. Gammarus chose to cat fu ngal
mycelium rather than unconditioned leaf discs. Later experiments with l eavc~ conditioned by indi vidual stream fungi showed that not only were some of the fungi that
produce tetraradiale or sigmoid conidia most active in conditioning leaves, but their
mycelia and sporu lating structures were also highly numtioos food for dctritivorous
stream anim.als such as Gammarus. An imponant ecological role had been established for
these fungi.
But many qucstions remai ned, Were those fungi with letraradiate sporcs related to
one anOther? Did they ha\'e telcomorphs'? (which would help to answer the firsl question).
Since stn:a!IlS alo.,,'llys tlowthe same way. and have a natur",1 tendency to carry small things
like spores downstream , where diclthe inoculum for the upper rcaches come from? What
were the advantages of the tetraradiate and sigmo id spore shapes? The informati on we
needed was gradually accumulated ove r several years of experimcnts. until eventu~l1y we
wen: in a position to givc some Urlswcrs .
.\Iany of the tetraradiate (fOlic-armed) spores, though similar in configufllfion at
maturity. developed in rathcr different wayS. I will describe just two of these. In some.
three armsrew upward and outward from the toporth<! rlJ';t-formcd am} (e.g. TtmKh(l~tllm
in Fig. 11.3). In others. one arm grew upward. the other!hrce or four outward and downward al the same time from a cenlm! cell (e.g. um()fln;aa in Fig. 11.3). Somc of these
conidia ...'ere thallic. some blastic. A few had clamp con~c{ions; most didn' t. This impression of di\'Crsity wasconfinned when some of thc telcomorphs were.disco~ered . Some
wen: unitunicate ascomycetes. both opereulate and inoperculate, producing apothecial
~nd ~rithecial ascom ata. Some wcre bitunicate asromycetes. Some were basidiomycet~s.
II became clear that the morphologically similar anamorphs were actually n mi"l:~d
bunch: fun gi of vcry different origins th aI had undergone comergcm evol lllion. mo lded
by selecti on prcssurc imo similar shapes. The teleomorphs also provided one nnswer to
the qu~stion of how these fungi got upstream: ascomata and hasidi omatll.. unlike the
anamorphs, were not submerged in streams. and they liberated airborne ascospores or
oosidi05pores. The group has been christened the amphibious fungi. beeause of it~ immet>Cd anamorph.i and emergenllekomorphs.
But "hy d id so many of these taxonom ically d iverse amphibious fungi evolve
conidia with similar shapes? It was found that as they w~re carried along by the WateT.
tetraradiate spores somclimes entered the layer of still Watef JUSt above the sulface of
subm<:rged !eo\'cs. and then made three-point landings on these leaves. We know thai a
tripod IS the most stable config uration. able to .tand firm o n irregular surfaces. The spore.
fomlcd microscopic tripods that gavc thcm a foothold <,In the dead leaves for long enough
to gcmlinatc from the ends oflhc lhr~ arms. and attach themselves to the substrate before
being swe pt away. The n:ason for the sigmoid shape has not yet been fully estab lished.
After coloniZing the leaves. the amphibious fungi sporulate again, and it was found
th:u they wOllld do this only in highly oxygenated conditions. and with the phySical
stimulus provided by nOVo'ing water.
FU~GA L
ECOLOG Y 193
If the ~pore numbers are charted over the entire ye ar. it will be seen that their
numbers peak in fall and spring. In !he first place. the massive new input of autumn-shed
leaves pru,-ides the necessary substrate. In the second C3SC. spring run-orr will also carry
plant d~bris into the stream. The entire process is diagrammatically summarized below,
showing mal the fungi are vital intermediaries of energy flow in streams, providing 3 link
between dead leaves 3nd troUi (Fig, 11.4).
1,,
,\,,
,
"
l"
\
,,
I
,,
Ii,
I, '
I
I' I
196' CHAPTERELEVEt\
related. Again. convergent ~volution has bc~n Ilt work. the sekction pressure applied by
irnperati-e.
We finnUy disco\"~rt:d whm thi~ was. It wos the need to be frnt on the sc~n~ when
new substrate appears. \\I"h~n Il dead l~af falls into a pond. it docs not sink immediately. II
may actually fallon top of $Orne of [he floating propagules, or the propagules may be
drawn to the floating leaves by surface tension. In either case. these fungi will be the first
pond-adapted species to enter this new substrate. The leaves soon sink to the bouom of
the pond. carrying their new colonizers - hyphomycete or gasteromycele - with them.
These fungi also have the abiliry 10 grow at low oxygen levels. and to survive the virtually anaerobic conditions thnt prevail at the bottom of a pond for extended periods during
the winter. Sporulation wi]] happen again wheo the pond begins to dry out during thc
follo"'ing summer. and the water level subsides until the colonized leaves are once more
JUSt below the surface. We found til~lthese aero-nq uatic hyphom)'cctes play an ecolog ical role parallel to thai ofthc amphibious fungi in streams: conditioning the deoo 1ea\"(:~.
and making them palntablc to the detrilUs-ealing in"crtebrates such as snails; and venebrates such as frog s. whose tadpoles live in the pond and ~ke1etonize leaves after the fungi
have 'conditioned' them. e'entually metamorph()!;ing into tree frogs which represent the
apex of the pyramid of life in the pond.
$Om~ ~cologica!
'.
Other Habitats
The biosphere has myriads of othtr habitats. each unique in various ways. and each
making spedal dcm~nds of the organisms that live in it. The roots of plan IS creale special
conditions around themselves, and have establish<ed especially intimate relation~ with
hundreds of endotrophic and thousands of ectotrophic mycorrhizal fungi (which have
chapter 17 10 themselves). Other rather less specialized saprobic and parasitic fungi also
abound on and near rOOts. The su rface of living leaves is inhabited by a spedalized
mycota. while dead and decaying leaves are subMr.lteS for a succession of other species.
The soil, into which most leaf remains are incorpor.ued, is itself a mass of microhabitats,
and is the richest resc(VQiroffungal diversity. And of course the leaves of di fferent pl~nts.
and the various soil types, will have different subsets of the total mycota. Julict Frankland.
in her 1998 Presidential address to the British Mycological Society, gave a nice overview
of the problems and progress in our study of fungal succession, exemplifying them with
an aute<:ological study of the agaric, Jlyuna ga/opus.
!\Ol all fungi can be parcelled om neatly into successi~'e steps of a succe~~ion.
Often, fungi compete for access 10 ~ sub,trate. Sometimes a natutnl phenomenon will give
us an unexpected insight into this struggle. Wood is often colonized by many different
mycelia. The boundaries be't"een the 'territories' of different mycelia can often be clearly
seen as black lines or zones, and the wood is described as 'spalted: (Fig. 11.7) The black
materia l is melanin-like, oxidiled and polymerized phenolics deposit~d by wood-rotting
fungi. and although the biological fl,lnClion of the zones isn't entirely clear. melanins arc
the precursor> of the hl,lmic acids. which are longliled and important detennjn~ntS of soil
fcrtilit).
What's an ATBI ?
Of course. you can't do fungal ecology unless you know what fungi are present.
There is almost certainly no habi tat in the world whose fungi have been fully enumerated.
A group of 22 mycologists gathered in Costa Rica in 1995 and came up with a strotegy for
isolating and identifying all of the fungi (an estimated 50.000) in a particular hahit:u (the
Guanacaste Conservation Area) - an All-Taxa Biodiver,it)" Inventory for fungi (Rossman
et al. [Eds.J 1998 - see reference below). This ambitious plan called for a staff of a
hundred , 51 million wonh of agar media and 1.8 million slants to isola te the e ndophytic
fungi alone. Unfortunatel y alllhis would have cost about US52S million. so it hasn't
been done. BUI the need remains. and the ge nernllack of kno wledge about fungi means
that they are not usually considered when conser"mion issues are raised , Perhaps you ca n
hclp to chunge all that. A less ambitious ATBI is now und!f way in Great Smoky Mountains National Park, blll it is a long-term ende ~vou r - visit the " 'eb site at
http://w"w.disco\.e rli rC.o rgj
And baving outlined th at cunemly unsatisfactory stale of affairs. we must tum the
page to another. completely different aspect of mycology whi ch came to promi nence in
the middle of the nineteenth ce ntury. an d has remained ffOot and ce ntre ever since .. ,
~ UFPECCB
/5SISl.I OTECA
12
Introduction
We nre utlerly dependent on plants. Directly or indirectly they supply all OUT food .
So it is an ex tremely serious maner if something prevents our domes ticated plaTHs from
Hvi ng up to the ir g~netic potential in terms of growth and yield. Outside influences that
do this nrc said to cause dise~se. and are deal! with by (I broad collection of disdplines
grouped und~r the heading of Plant Pothology. At many universitic~. whole academic
dCJXlrtmenlS are devoted to it; enlire government iabor:!tories do nOlhing clse. This is
bccaul.C OUTCrops, in fidd or forest arc threatened by thouo;ands of disca~s, Plant P3lhol.
o;~
noninfectiou~
such as mineral deficienc ies, climate or pollutants, and with infectious diseasoes caused by
a horde of different organisms: n~mat()(ks, bacteria. myCQplasmas, viruses _ and fungi.
This ch~pter, as you might expect. ""ill ~ concerned only with dise~ses causcd by fungi .
Although insects are our chief competitors for food. fungi are a good second. Crops
in Ohio ~re attackcd by ahout 50 bac terial diseases, I 00 \"ir~l diseases. and 1.000 fungal
di.s.:ases. AboUl 60% of all pl ant disease li terature concerns fung~1 diseases. You h~ve
already read about some of these in tile ta~onomic chapter, at the beginning of this book'
ruSt" smuts. bhghts. down y mildews, powduy mildews. ctc. I am not going to repeat
myself: you should refres h your memory of the org~ni~ms im'olved by lOOking back into
that section. You could nen glance throuSh it now, before)'011 go on with the rest of this
chapter. (That's thc- great thing about a book: it's a wry fie.\ ible te~C"hing machine.) But I
will mention somc additional diseasoes here. just to b["()2.d~n your perspect ive.
E\'cr since Jlt'opk ~ame i:umers, thc) lIave had problems with fungal diseases of
plants. These dis~ases we~(fl ,i.ited upon them by Ih~ gods. as the ancient Romans
thougllt. but were a natur:tl consequence of growing plants in extensil'c pure stands. or
monoculturcs. Whether the fungi grow. swim. fioat. ride or blow from one ho~t plant to
the ne)(t. they w ill find a new home much more readil y in a monoculture th~n in most
n3.tur~\ plant communities. This is bc<:au~e most plant disease fungi hJve a limited host
range. and the very diversity of the comm unity means that ind ividuals of a panicular host
spedes are ofle n well separated. so may escapc in fection em~nating from their relatives.
Although fungal diseases ha\ e beel\ rccogni7.cd for thousands of years, III~y w~re
not conn.xted with the organisms that caused them until the mid nineteentll century.
Fonunatcly.the scientific re,'oluTion was in fuU swing when the pomo famine caw.cd by
]00
$10%
41-60%
~~
> 90%
Fig. 12.1 Progressive attack of Phytophthora infestans on potato plarlt$.
:1t~
UF o;:-C!:\'!
~ Sr&U OTEC.~
extreme, some fungi evolved diffusible lollins that killed host cells at long range. and
circumvented the problems inherent in expl oiting living cells. At the othe r extreme, some
fungi be<:ame so intimate with their hosts that they ultimately beeame dependent upon
the living host c~'!oplasm for many things: not just food, but also 11 variety of vital
enzymes. or even whole biochemical pathways. Some fungi produced p lant growth regulatoi"S that either increased or de<:reased the ability o f host cells 10 grow and divide.
In this way, three different kinds of pathogcn cvolved (I) Some are racu fUl ti>'e
parasi tfS: mese versatilc organi.~ms can Ih'c cither saprobically or parasitical ly. Many of
mese are pathogens o f annual herbaceous crop plants. and must survive betwecn growing
seasons as members of Ihe normal soil mycola. This ability make s them particularly
difficult 10 control. and virtually impossible to er~dicate: Fusarillltl oxyspo rum var.
cubense. which causes Panama disease of bananas. can survive in the soil for at least forty
years in the absence of the host. (2) Other fungi are nenot r ophs: basicall y saprobic, but
producing toxins specific 10 su>ceptible host cells. The Monilia anamorphs of Monilinia
species, causing brown rot of peaches and ocher stone fruits. belong to mis category. (3)
The last group are caned obligate parasites or obligate bi otrop hs, ~ause they have
long since iostthcir independence. and cannot grow al all except on or in a suitable hosl.
In fact . me dependence is oflen so complel~ that onl y one host species. or a fcw cultivar.;
of that species, will support a particular race of such a pathogen. The rust fungi. for
example the genus Pllccinia . are good examples of this third category.
Life cycle st udies. Often we can' t decide on the best wa y to tackle a fungal disease
until we know a greal deal abou t the li fe c ycle of Ihe fungus. For example. many o f the
obligaldy biol.rophic rust fungi hale cvolved complex panerns of existence m:u require
IWO hosts (such ru~t fungi are called heteroecious). with an obligatory an nual migfiltion
from one to Ihe other. We may be able to control the fungus hy eradicating one o f the hosts
(~ssu ming that it is neitherof economic imponance. nor rare, of course) wherever il grow~
too cl ose to the other. Perhaps the best- known example of this practice is th e widespread
eradicat ion of barberry (Berberis spp.) in NOTlh America 10 break the life cycle of Ihe
wheat rust fungus, Pliccinia graminis (Teliomycctes, Uredinales), or at least reduce its
opportunities for genetic recombination, since dikar),otization happens on the barberry.
The Spilococo anamorph of \~ntllria inaeqllo/is (Ascom ycetes'. Bi tunicatae) is a
virulent para~ite which attacks me italICS and fruit of apple trees and causes the unsighlly
scab disease. BUI il can also li~e saprobically. because the ascomala of me te\eomorph
develop in the dead apple leaves over the winter, releasing ascospores (the primary inocu
lum) in spring. To control the anamorph requires repe3led spraying throughout the growing season and , as the chapter on fungicide s c learly shows, the fungus quickly del'elops
resistance to e~ch new fungiCide. Removal of dead leaves from the orchard floor, and
sprayi ng with disinfectants while the trees are dom1:tnl. are valuable w:tys of reducing the
amoum of ascospore inoculum released in spring.
PhylOphfhoro infts/Ofl$ (Oomyoota. Peronosporale.s) produces easily detachcd and
subsequently airborne mitospofilogia; but when mese land on a new POUliO plant, they
still release swimm in g spores. The5e are delicate, shon-livcd, and can functi on only when
free water is pre~e nt on the potato leaf. Thi s st:tgc might be described as the Achilles' heel
of the fungus, since minute quantities of fun gicide in the water will kill th e zoospores. BUI
once the fungus i~ inside me host plant, control becomes much more difficult (Fig. 12.1).
II is clear {hal we must ha,e detailed knowledge of the life cycles of pathogcnic fungi if
we want 10 develop optimal disease control str.lIegics.
ultimately replace il with thdrown reproductive Structures . U we grew com and rye as we
do lettuce. just for the leaves, these diseases wou ldn' t be so serious. And if carrot leaf
blight didn ' t reduce the efficiency of the harvesting machinery (the leaves are weakened.
and break off. leaving the carrot in the ground). it might nOI be taken nearly so seriously
by the growers, since it doesn't drastically reduce the actual carrot crop.
H ost organ s attacked. Discases can be described as root rots, vascular wilts. leaf
spotS. etc. When a disease is first noticed. the fungu s cau sing it will not usually be
producing diagnostic structures. Symptoms may well develop in parts of the plant Ihnl
aren't being direcily attacked: symptoms of root disease will oflen manifest themselvcs in
the shoot system. ConsequeDily. many plant di sease manuals concentrate on describing
and illustrating setS o f symptoms by which diseases can be diagnosed early. Although
positive iden tification of the fungus may not be possible until it eventually fruits. or is
isolated and identifie d in pure culture. treatment must begin as early as possible. to
prevent the build-up of an epidemic. It is easy to lalk about such d isease.') as Allemaria
blight and Cercospora blight of carrots. as if these were easily recognizable entities like
mushrooms or mice. but th e truth is that the early symptoms are often very ineonspicl.lou >.
that they change continuous ly as the condi tion develops. and thut it takeS a very prac tised eye to make an early diagnosis of most diseases. Plam diseases can be class ified
according to the symptoms Ihey elicit:
(I) Necr osis. i<'neralized cell death . is the most extreme reaction. It can affect the
base o f the shoot. as in damping-orr (caused by PYlhium species: Oomycota,
PCrOtlosporales)~ or the lea ves, as in late blight o f potato (Phylophlhora infi"suUls:
Oomycota. Peronosporules): or storage tir.~;ues, as in soft rot of peach<:s. Necros is go.:s by
many names: anthracnose . blight. canker. scab. leaf Spol. shot-hole.
(2) Permanent wilt ing. caused by blockage of the xylem by hyphae or as a reaction
to a fungal toxin . as in wilt oft01llato (caused by \'1micil/iwtl: Hypho mycctes). Panama
disease of banana (Fusarium oxysponjm f.sp. Cljbens~: Hyphomycetes). and Dutch elm
di sease (Ophio5tomu ulmi; Ascomycetes. Ophiostomat:lles).
(3) H ypert rophYOI""hype rphlsia . caused by growth hormones (auxins ) liber~ted by
the pathogen. as in white rust of crucifers (cau.ed by Albugo Cilndida: ()Qmycota.
Peronoo;poral es). ,om smut (Usli!(lgo maydis: T<,liomycetes. Ustilaginales). and peach
leuf ,uri (Taphrina dejornums: Ascomycetes. Taphrinales).
(.4) Lea f abscission . caused by hormones produeed or sti mulated by the pathogen.
as in powdery mildC"<of gooseberry (Sphal'rolheca: Ascomycetes. Erysiphales). and cofft'.: rost (Hemile;(l "asla/rix: Teliomyeetes. Uredin ales) .
(5) Et iolatiun. excessive extension growth. caused by a growth hOffilone (glbb<:re llie acid) produced by the pathog~n. as in 'foolish seedling ' dbease of rice (eaus~d by
GibbtrtllaJuji!':'IITOi: Ascomycetes. Hypocreales).
(6) Pre\'entiun orreproducli on , cau>cd in various ways: Choke of gnls>cs (Epichlo
I)"philw: Ascomycetes, Clavicipilales) prevents flowering: ergot of grasses (C/OI'icep.r
purp/lfea : Ascolll yc~te~ . Clavicipitales) replaces the grain with a fungal scl"rotium: and
anther smut (Uslil(l80 vio/acea: Teliomycete.5. Vstilaginales) replaces the pollen with
fungal spores.
Irrespective of how we classify and diagnose fungal pb.nt diseases. the prime objective of plant path nlogy i~ to thwart the game plan of the pa thogens. and many disc iplines
now contribute to thL, end. The meteorologis t provides data whiCh will allow the plant
pathologist to forecast outbreaks of eenain diseases, lind prescribe appropriate pre\"enti ~e
measures: this teChnique is panicularly valuabl.: in dealing with btl' blight of potato.
Some plan! pathologists have delved into micromcteorology and aerodynamics to prone
,
the way conditions within the canopy of a forest or of II field crop affect spore dispersal
and germination. The chemis t sYflthesizes new and e"er 11lQfC: sophisticated fungicides.
1be plan t brewer produces o;ulti vars with built-in resistance to specific diseases.
The plant pathologist is dealing. not simply with an isolated interadion between II
fungus and II plant. but with the overriding effects of climate and microclima te on how
that interaction develops through time. MOSt imponderable of all is the fungus itself
which. with itS endless genetic flexibility. is never more than one j ump behind the plant
breeders and the fungicide formulators. Sometimes there are other complicating factors:
the mysteriou~ wanderings of animal vectors such as the bark bee tle that carries DUlch
elm disease from tree to tree; and since Dutch elm disease: was brought, albeit acciden
tally, by people: from Europe to North America. the control of an plant imports assumes
tremendous importance_ Although some diseases are almost Ubiquitous, many are still
relatively localized. and governmentS try, with mue<! success, to exclude exotic pathogens by quarontine regul ations, employing plant pathologists to inspect incoming shipments of plant products. Much of what we know about long-range dispersal of fungi (see
chapter 8) concerns the spread of crop diseases, which will make themselves fdt, and
hence be docume nted, wherever they appear. Jt must be clear by now that there is no
simple formula for dealing with plant diseases. Each is a special o;ase; and each outbreak
will differ from all others in various ways. Plan! pathologists wil! never put themselves
o ut of a job.
Establishment of Disease
_When pathogen meets plant, a number of factors detennine whether disease will
de'elop. The plant may be entirely w.;isLlnt. extremely susceptible. or somewhere between those extremes. Thc fungu s may be enre mely viml ent. almost avil1llent, or somewhere between the two. The stage of development of the host may be important: damping.
off attacks only young seedlings; ergot ascospores can infect only grasses in flower. The
weather may be critical: many downy mi ldews have an absolu te requirement for free
water.
Pemaps the most crucial phase in the deve lopment of any disease is the initia l
pene tration of the host. A microscopic spore \One in a hundred? One in a million?), lands
"
F.g. 12_2 Penetration of host by flXlgUS. A: sca~ electronmicrograph; B: iransrrission
eIec~ 01 . ,icrograph.
Epidemiology
Epidemics of different dise:l..'\CS develop in different Wll}S. The inc idence OfSmUiS is
predetermined by the level of infection or spore contamination of the seed when the crop
is planted. But the severity of most Other d iseases depends on their success. not only in
producing primary infection. but in multiplying their sc(;ondary inocu lu m during the
growing season. This success. of course, is a product of the inler-olction of many faetors:
virulence in the fungus. susceptibility in the host. fa"ourable weather. lack of action by
laissez-faire farmers. Contlitions for th~ development of major epidemics of many dise~ses do nOl h~ppen every year. but some crops are always threatened. For example. if
apple growers did nol spray 820 ti mes per season to control apple scab (the Spilocaea
po",i anamorph of Venturia i"a~l]llGlis). between. 70% and 100% of their crop would be
unsaleahle. If peanut growers didn't spray 8-10 times ~ season for foliar diseases. they
""ould looe 10-75% of their crop. Peaches need foliar and post-harvest treatments if 80%
~'-~ "'::I
<;)-:,
~ V l.,.
_,
of the crop is not to be 10SI. Strawberry growers stand 10 lo;e 70% of their crop if it is not
sprayed severaitimes. Gr.lins, on the other hand, can often be protected against their worst
diseases by a single seed treatment. which preve nts losscs of up to 35%.
Let"s see how some of those diseases develop. Apple scab begins the :season with
asco.o;poteS. primary inoculum shot into the air from 3scom3ta dc\'Cloped in last year's
dead leaves. But it immediately swi tche s into anamorph mode: each infection dcriv~d
from a single ascospore soon produces many conidia on the cumnt season's leaves. These
spread the infection to new leaves. and the new infections soon prod uce even more
conidia. The number of conidia increases in a geometric progression, an d unless this
cycle of infection and conidium production is interrupted. the outlook is bad_ You will
find a detailed diSl.:ussion of the difficulties invoh'ed in oontrolli ng apple scab in chapter
13. It is an interesting SlOry, wilh no end in sight.
Other crops are threatened by more than one se rious disease. Potatoes. for example,
suffer from an early blight caused by Allernaria (H yphom~-cetc.~), then from late blight
caused by Phyrop/uh()ra (Oomyeetts). No single fungicide wi!! effectively control both
fu ngi. Mancozeb is commonly used for the Allemaril'. and Ridomil for the PhJlophthora,
and aclose watch is kept on the weather to determine wilen it is necessary to spray for late
blight.
Experienced plant pathologist~ perfoml an invnluJble ~ervice when they go OIIt
into a (,eld and d iagnose a disease, but Ihey cannot keep Imck of every diSt!asc on every
crop. And if the development of epidemics. ond the resu lts of control measures. are to b<:
documented. we need so me objectivt ways or decid ing how much disease is preScnt, and
how serious it is. Sometimes these take tile form of dtscriptions. as in Ihe following
excef1'llS from a ke)' for asscssing powo blight: ' Up to 10 SpolS pe r plant'" I % of crop
diseascd: 'Eve ry plant affected an d about one- half of leaf Jrea destroyed by blight: field
looks green flecked with brown'" 50% of crop diseased'. In other cases, visual aids are
pTO\'ided , which allo w farmers to assess the severity of JUnek for Ihem~el ves. Figur~ 12. 1
I,
I'
~,
,
,
,
,',
".,
I~J
(;\
..,
I L rJ".
,
"
' ,
,
,
"
".
1"'"
,,,
('1
'.
&
Fig. 12.3 Diagrams uS<!d to assess severity of disease. A: Septoria gluIDe blntch of wheat; B:
Erysiphe pcr.Ydery mildev. of cereals.
cenain thai anything will be done about it. Economic considerations ~ re a.sain paramount
in rT\3uers of disease rontrol. Some diseases arc ensy and cheap to controL Ie would be
possible to suppress many others " 'jth an appropriate regime of sani tation and prophy,
laxis, but the return in increased yield would not cover {he cost of the progrom. This is
particularly true of many forest diseases. At the Olher end of the scale. greenhouse crops
are often so valuable that e~penshe control programs (from soil fumigation to repe~ted
applications of fungicide) are routine,
Onio ns are attacked by: ( I) purple blotch (Allemliria porri: Hyphomycetes): (2)
neck T()t and grey mould rot (BolTyti! allii. 8mr)"tis squallwsa and Bmrylis cil!er~a:
Hyphomyce tes); (3) leaf bli ght (Borryti! !quam(}Sa). (4) smudge or anthracnose
(Collero/ric/rwn circinans: Coelomycetes); (5) Fusarium bulb rot (Fu.wrium oxyspor"m
f.sp. ((PC~: Hyphomycetes ): (6) downy mildew (P~TOtl{)s{J()ra des/fllelor: OomycOla): (7)
pink rOOt (pY'l:t1ociUlela laTes/ris: Coclomycetc~); (8) white rot (Sclerotillm cepiv()I"lIm:
steril e ana morphs); (9) smut (Uroc),stis magiC(;: Tc liomycetes). Of course. a givel\ crop
will not develop all ofthcse discases at once. but the co ntrol strategies used by farmers are
sufliciently diverse to be wonh outlining.
Fou r main strategies are adopted: (lJ C rop sanitat ion. Since many p~thogens overwinte r and complete thei r life cycle on the dec~ying remains of Iheir host ptant. il make~
se nse to destroy crop debris by burning it or ploughing it under. (2) C rop ro ta tion.
AnOlh<'t "'ay of reducing the populations of pathogcnic organisms is to alternate ~usce p
lible "ith non-susceptible crops. The length of T()lalion depends on how 1000g the pathogen can survive without the host. Sometimes a tWI)- or three-year rotation will do, but
since Scltrorirtln, Colletotric/rum, Prn:nt)Chlleril. and Uroc)"stis can survive in the soil for
~ long lime, rotations of at least five years would be neceSS:lf)' to reduce their inoculum
potential to a reason~bk leve l. Such long rotations are often impract ical. (3 ) ""u ngidd~
trea tments. Seeds are treated with fungicides to prevent dampi ng-ofr and smut. because
the inocu lum for these diseases is seed-born.:. Leaf diseases are difficult to lreat once they
have appeared. and require repeated. and thereforc e~pensive, sprayings. So a protcctant
spray is often applied before any di sease symptoms appear. Preventive spraying may be
repealed if weather conditions or disease forecasts call for it. (4) Res istant c ulth'arlO are
under constant de"e!opment by plant breeders. When available. they arc the most effec_
tive and the cheapest way of avoiding losses.
r-,Iorc spKifically. in onion fields. purple blotch. neck rot and leaf blight are controlled during the growing season by fungicides, and thei r inocu lum potential reduced
after harvest by removing and Qestr()ying pJ:mt residucs. Neck rot is basically a storage
rot. and can be minimi.1;ed by harvcsting the onions in dry wcatllcr, air-dry ing them before
Slori ng. then keepi ng them at OC and a relative humidity CR.H.) below 70%. Smudge
occurs at harvest time and in storage, so drying onions properly, and keeping them at OC
and 70% R.H., is recommended. Fuwrillm bulb rot is difficuil loeliminate.since Fusarium
species commonly survive in the soil as chlamydospores. or grow saprobicaJly on crop
residues. A ~-yearrotation is required to keep this disease in check. and use of resist ant
cultivars isreconunendcd. To become established. tnedowny mildew fungus Perol1Qsporo
needs cool temperutu res and rain or dew on the leaves Gust like potato blight, and for thc
same reasons). A few hoors of dry. sunny wcather will slow Pero"ospora down considerably. The fanner can hdp by avoiding mildew-contaminated sets, practising a two-year
rotation. spraying regularly with fungicide, and destroying infected Crop debris. If pink
root becomes :1 problem. a long rotation will be necessary. White rot also necessitates a
long rotation. though soil treatment with fungicide may deal with small problem areas.
Control of smut is achieved by cQJ.ting the onion seed with a systemic fungicidc. practising rotation, an d using onion transplants if the wi l i!i already contaminated: established
plants will not to.! affected by the disease.
It is instT\lcti ve to co mpare the fungal diseases attacking onions with those found
on ca rrots. Carrots are prone to Alternaria blight (Alternaria daad: Hyphomycetcs);
Cen;:ospora blight (Cercospoffl caralal:: Hyphomycetes); rosty root (PYfhium spp.:
OomycoCl); violet root rot (/?hiZOCfonia CTOCOntm anamorph of HdkoMsidium purpWl!Um:
Basidiomycetcs 1: Rhi.1;octoniacrown rot (Rhiwcwni/! folalli anamorph of Thanatephoru.1
cllcumeris: Ba ~i diomycctes): Sclerotinia rot (sclerotial anamorph of Sclerofinia
.clerotiomm: A.;.comycetcs); and black rot (Slemphy/iw" radicinum: Hyphomycetcs). Are
any genera conunon to both li!itS? Only Alternaria: this gives you some hint of the
diversity of patl:::ogenic fungi. and the difficulties faced. by the plant ~thologist . Which
group of fungi is most prominent in both lists? Dikaryomycotan anamorphs. mainly those
we call Hyphom:. cetes. This is a generalizatio n that holds across the entire spectru m of
plant disease t'unp. Of course. the diseases vary in distribution and in their economic
impact. CefCo,pora blight is favoured by hot. humid wcather. and develops in high summer. while Alternaria blight and Sc1crotioia rot like it cooler. and develop later. RUSty root
is mosl ~\'ere in wet soils, Rhitoctonia crown rot in organic soils after repeated carrot
crops. Sclerotir.ia rot prooobly causes the greatest losses_
Since the r.lnge of control measures avail able to us is much more restri ct<:d tha n the
variety of fungi innJlved. I don'l need to elaborate on Ihis exceptIO say that the measurcs
used will reflect sUI:h fcatures of the fungus as its longevi ty in the soil, the part orthe plant
it attacks. and e.;conomics. In the case of th~ two Rhi:oclOnia diseases, no effective co ntrol
is possible at pre;..:nt, SO the only possible recoursc is to grow carrots in uninfccted. soil. II
is hoped that resiitant varie ties I'il1 C\'entually be developed.
212 CH APTER-TWELVE
spraying to pre ve nt late blight. Simpler programs call for the grower to usc a
hygrothennograph and a plastic rain gauge to keep track of the daily m:llI:imum, minimum
and mean temperature. and dai ly r.linfall on a standardized record sheeLA blightfavoorable
day is recoroed as a . +', and the first spray is dictated by ten successive '+' days. E"ery
seven days afte r Ihis, the need fOf spraying is reassessed, using hu midity, temperature and
rainfall data ,
A weather-timed spray program has been dcvized to keepAlll'maria and Cercospora
leaf blights of carrot from kiBing more than 15% of the leaf area. Jfthis level is exceeded.
har..esting machinery tends to leaT off the weakened leaves, leaving the carrot in the
ground. No fungicide is applied until the bligh t covers 1%2% of the le;U' area. Then
fungicidc is applied before thc ne.'l.t forecast rain, or before the next night with a forecast
minimum temperature of 16cC or high er. At lcast 7-10 days are allowed betwee n subsequen t sprays, which are applied in conditions similar to those for t~ first spraying. Sprays
are not needed before forecast rains when the night temperature will be below 9C, because the fungal spores infect the leaves only when these are both wann and WCI for an
e.'l.tended period.
Although wetness is vital for the suc~essful establish ment of most leaf di sease~. the
.'I.erotolerant powdery mildew fungi are less affected by moisture, and more by the aV3ilability of inoculum: levels of airborne conidia. A thi rd f~clor is the in~reas ing sus ~eptibil
ity of some crops as they age. Programs have now been worked out to detennine the
critieal date for a single application of fu ngicide to forestall powdery mildew of barlcy.
the date of the fi rst spray to cont ro l powdery mildt:w of rubber, and the timing of suc!':essive sprays against powdery mildew of apple.
The value of plant discase forccaSting is, as one migh t e.'l.pect, economic. In the
carrot blight situation. an average of 2-5 sprayings were sa ved by following the program.
The saving resulted from delaying the first spraying. and making subsequent spraying
cOluingent upon the existence of conditions favourabl e to infection. rather than ritually
spraying every so many da ys_ Each program muSI be designed or modified to take into
aCCQunt conditions prevailing in the area where it will be applied _
Forest Pathology
The Americun sweet chestnut, Castane(. dentata. once grew from M;line to Alaoom.1.11 was a fine tree that thrived even in poor seiland on Steep hillsides. Some spedmen~ in the Grcm Smoky Moun tains were 4 melrcs in diam eter and 40 metrcs high.
Chestnut wood was eJucnsh'ely used for fencing and roofing. 10 make furniture and to
build barns. During the burgeoning industrial revolution of the nineteenth century it was
u!>l'd for lining mine shafts and in minc roof suppons, 3., railroad ties. as IclcgrJph poles.
and as fuel. Chestnut trees shared pride of place with elms as street and shade trees.
Appalachiun fanners fau ened th eir hogs on chestnuts. which were also roasted and used in
meat stuffings. The chestnut was the most economically imponant tree in the eastcrn
hardwood forests.
Near the end of the ninetcenth century. chestnut seedlings imported from the Orient
to New York brought with thcm the fungus Cryplwllt'crri(l (Elldotilia) p(lmsirica (Ascomyce t<!~. Dothioro!es). Th is introduction found a defenselcss host in tile American chestnut. The first diseased u-ees were noticed in 19().l in the New York Zoo, and from then on.
the epidemic mounted and sprcad re morsele ssl y. The early issues of Mycologia. thc Jou r
nal of the ~lycological Society of America. contain repeated rather pl.:lintive references to
th e ad\'ancing plague. Despite their agonizing concern. myCtllogists ami foresters could
only watch hdple ssly as millions of chcstnut trees died. and the face of the forests in
eastern North America changed. By the 1940s or 1950s practically all the mature Ameri-
,,
Allemaria so/ani
(Hyphomycctcs)
(Oom)'cetc~)
CeratOL),slis jimhriata
(Ascomycetes)
Cercospvrella hcrpO/richoideJ
(Hyphomyceres)
Clul'iaps purpuna
(Ascomycetes)
Col/etOlriehulI! /indell!urhimwII!
(Coclomycetes)
Dip/ocurpon rosae
(Ascomyccrcs)
Host(s)
Disease
Control
potato. tomuto
early blight
MancOl:eb
forest treeS
bult-rot
lettuce.
tomato,
StrawberTY etc.
grey mould
Captan. BellOmyl
lenure
downy mildew
Dirhiocarb
sweet potato
black rot
wheat. b'lI'ley
eye-spot
cultivar
<="
''8'"
clean seed
t.ID'
amhnlcnosc
clean seed
black spot
Caplan
powlkry mildew
culri\'llr.
Tridcmorph
rocHot. butt-rot
shorten rotation
rye, OI:her
=~,
(Ascomyretes)
(grasso:s)
Hererobasidion wmosum
(Aphy1lophoraJ cs)
conifers
--
can chcstnU1trees had died. rhough living roots are still sending up sprouts that reach a
fairsizc before being killed by the fungus. and some large tIe<:S siill survive. because they
are apparently infected by a hypovirulent strain of the parhogen (apparently the result of
irs becoming infccted by a virus). All that is hislory now, a nd it's too l;llc 10 do much aoout
it, ex cept to slowly reintroduce scions of surviv in:,: trecs to areas in which the species us".d
to grow.
What of current concerns in foreslry? The lumber industry is a m3instay of the
economy in many areas ofNonhArnerica. but until rece nt years forests were 'mine(!' with
liuk tooughtto repl:lccment. since the resource wa~ ao;sumed to be \'inually infinite. or:lt
least entirety self-renewing. In Canada. a combination of depiction of first-growth forests
by clcarcl,!{ting. heavy 11\.'(: monality duc 10 inseclS nod diseases (which togcrhercau>c an
annual loss of almost 130 milliun cubic metres of wood), and ~xtensive forest fires.
~ombined to produce a po lential wood shor\(lgl:I. Even if on ly 20 million cub ic metres
cou ld be saved. this would provide 39.000 jobs. $800 million in wages and salaries. and
forest products wonh 52.9 billion. All this makes fungal discases important. because they
are one of the m3in faclors contributing to the tosses.
2 14 CHAPT ER TWEL\'
Tree diseases are often distirw::t1y unspectacular in appc:araoce. and their effects are
insidi ous rather than dramati<::. Trunk decays and root rots progress steadily. year in. year
out. Oll<::e established in a tree , they cannot be eradicated. In Canada alone, the various
rots cause a combined loss estimated at 30 million cubic metres of wood each year.
Root-rot caused by Phellimu (Porill) wtirii (Basidiomycetes, Aphyllophoraies) is
widespread in West Coast forests. and ise~pecian y destrUCtive in Douglas f1r(Puudmsugll
Intnzil'sil). Despite e:uensivcsrudies, we still have nocost-cffective way of preventing or
eliminating this problem. Nevertheless, it appears that losses could be reduced by earlier
cutting of infec ted stands, selective culling to favour the establishment of less susceptible
tree species. and the use of red alder in rotation to reduce the amount of Phellinus inoculum in the soil. Other silviculrural practices that would be helpful include: stump remo\al. fumigation. prescribed burning, fertilization. interplanting. sanitation, biologkal
eontrol. and host tolerance Of resistaoce.
Heart-rot caused by Foml's pinl (Basidiomycetes. Aphyllophorales) is also a severe
problem in western forests. Trees with signs of internal decay should be cut because
Fomes pini , unlike many other rot fungi. doesn't cause further decay after harvest. Root
rot caused by Hererobasidion annOS/l1IJ (Basidiomyce tes. Aphyllophorales). an aggressive parasite that infects cut stumps. spreads from root system to root system, and kills
many different con ifers. was the subject of nearly 600 publications betwee n 1960 and
1970. ReCQmmended management procedures include; wide spacing in new plantations;
preventing stump infection by applyi ng inoculu m of Peniophora gigallfea (Basidi
omycetes, Aphyllophorales) (biological control by a saprobic competitor): decreasing
the number of th innings per rotation; removing as muc h of the stump and taproot as
possible during logging; regcnerating by seeding instead of planting; and usi ng resistant
species. At present. the single best way to reduce losses caused by decay fungi appears to
be to shorten the rotation time: in the southern U.S., heart-rot losses in pi nes have been
reduced from 30% to below I % simply by decreasing the age at which trees are harvested.
A survey of forest putholog ists across Canada showed that rOOt-rot causcd by
Armillaria mtlltll (Holobasidiomycetes, Agaricales) Wil!; the only disease placed in the
ten most important diseases for all sill. forest regions. and was among the top three for all
ell.cept the Qucbec region. Whi te pine blistcr rust. ca used by Crenar/iu", ribicota
(Tc1iomycctes, Uredinales). was among the top ten diseases in all regions of Canada but
one. This disease produces spre~ding cankers on branches or main trunk that may evcntunlly gird le and kill th e trce. mc:mw hile producing the accial stage of the fungus . Thi ~
fungus. like many others causing rust diseases. has two h[l!;ts. so eradication o f the alternale host. Ribes spp., has be<:n widely practised. Cronllrlium cQmll1,drae, ca use of the
similar Com~ndr;;r. rust on lodgepole pine and other t~o- and three-needled pines. is not
susceptible to this form of control. be<:ause its alternate host is acommon and inconspicuous herbaceous plant.
In the so uthern Un itcd Slates another ~tem rust called fusi form rust. causcd by
Crona rti"", filsiforme. b responsible for losses of about :530 million a year. T his disease is
on the increase as a result of: (I) the use of infected nursery stock; (2) widespread monocuhure of susceptible tree spo.."cies; and (3) an increase in the altcrnate host. red oak. following improved lire prevention. The only practical contrOl measures are the use of fungi
cides in nurseries. and the breeding of resistant tree cultivars.
Gremmeniella ubietina (Agcomy,etes. Leotialcs) cau,es a serious canker of conifers . <especially pincs. in northea stern North America. The fungus has two raccs. The
Am.:rican race is vcry widespread in Ontario north of latitude 45. and kills many young
trees in their flISt decade. Once more than two metres taU, they seem able to survive the
Further Reading
Agrios , G.N . (1978) l' lanl
Carefoot, G.L. and
P~tholo g)" .
E.R. Sprott ( 1%7) Fami ne on the Wind . Rand /".'l cNaJly. New York.
Dickinson, e.H. ~nd 1.A. Lucas ( 1977) Plant Pa thology a nd Pl an! Pathogens. Blac kwell
Scientific Publishel"$, Oxford.
Barley, Bee t. Citrus. Com. COlton. Elm. Grape. Ornamental foliage plants.
Pea, PeanlJt. Potmo, Rhodexkndron & Azale a, Rose, Sorghum, Soybe;m. Straw.
berry. Sweet polnto, Turfgrass. Whcat).
Horsfall. l.G. andA.E. Dimond (Eds.)( 1959I%O) Plant Pathology. Academic Press. New
Yorl<.
James. C. ( 1971) A manual ofassessmenl keys for pla nt diseases. Canada Department of
Agriculture Publ ication No_ I-US. American Phytopathological Society, SI. Paul.
Johnston. A. and C. Booth (Eds.) (1983) Plant Pat hologists' Pocketbook. 2nd Edn. Commonwealth M ycolog icullnstilUt c, Kew,
Kenaga, C.S . E.B. Will iams ~nd R.J. Gree n ( 1971) Plant Disease S)'lllibus. Ball Publish~
els, lafaycuc.
Large. E.e. (1962) The Advallce orthe .,' ungi. Dover. New York
Roane . M .K.. GJ . Griffin and 1.R. Elkins (1986) C hestnut blight, other End othia dis
eases, and the gen us End olhia .APS Press, SI. PauL
Roberts, D _A. and C.W. Boothroyd (1972) Fu ndame ntals o f Pla nt Path ology. Freeman.
San Francisco.
Scopes, N . and Ledieu. 1\\. (Eds.) (l979) Pes t and Disease Control Ha ndbook.
Publishers, Croydon.
UFPECCB
Bepc
Fungicides
13
Introduction
Fungi have ravaged OUf crops ever since we invented agriculture, As soon as \I.'C stan
to grow many of Ihe same kind of plant close together (a mon(l(: ulture), any other organism s
!hal make a living from mal plant "ill find life much casier. since IRe nCX I meal (called iI host)
is siuing right beside the P',"iOO5 one. Bul until about ISO years ago. we had no idea what
caused mOSI plant disea,es. and until we learn ed that pathogenic fungi were actuallycnrane00" spore.dispe~d living organisms. rather than 'humours' or 'cflluvia of the earth. or of
thunder. oror snakes: we couldn'l do anything about it. So, fOr examphl, the destruction of
the Irish pol;\\O crop by Pilyrophthora il1/l!$ta1l5 (OomycOIa) during the 18405 went compkt.:l)" unchecked. for all it5 terrible effects on me human population. lbe fitst practical
fungtcide: "a, n 'I devised until fony years [ater. by a univer;ilY prof<essor in Fr-Jl1Ce.
Even IOday, over a third of al! crop [o,ses are due to fungal diseas ~s, They cost
Anl~rican fanners alone more th an $)5 billion a year. Some pathoge nic fungi (e.g. P"ccinia
gWl/linis: Uredi naJ<::s) can lxst be conlfo[]ed by breeding resistant plant varieties. Hut all
comm~rcin! npple varie ties ar~ Stl5ccptib1e to applt: scab (cause d by the Spill)cnen pomi
conidial anamotph of the bilUnicJte a'IComycele. Venll4rin illneq"alis). The eondilion~
conduei\ e to infection are precisely known. and oceur up 10 20 lime ~ each growing season.
Unprotec ted orchards muy prod uce no s~leabk fru il al all, so fun gicide ffillsllx: applied 615 lillles each year. Over 5 1.5 billion are now spent, worldwide. on fungicides of all ki nds.
Thi ~ chapter is an exploration of our increasingly sophisticatcd effort~ to combat pathogenic fu ngi with chemicals_
blend of copper sulphate and calcium hydroxide (quic ldime), This soon btcamc famous as
Borden ux mi.xtu ~ (in FJench. 'Bouillie Bordclaisc). OIher copper mlphaLe-based fungicides
followed: Burgundy mixture. in which the lime was replaced by sodium carbollUle. and Clle,hun[
miMure, in which it was Il::placed by ammonium carbonate. Although Bordeaux mixture i~:m
efficient. wide-spectrum fungicide. it has !lOW largely bten re-placcd by Comulations of coppo:r
oxide, copper hydroxide. and copper o:l;ychloride.
Bo,deaux mixture. and almost all olher fungicides developed before 1960, are called
p rotecla n l.s: Ihey are toxic to palhogenic fungi. but only if the)' intercepf the fungi outside
the host plant. If !he pL::m t's e ~terior is nOL thoroughly coated witb fungiCide. the fungu s
can slip through the defence. Once inside its host, many pathoge ns can' t be rca.;hed by the
chemical. and have on ly the pla nt's internal defenses to deal wilh. Inorganic fungiCides
al so lend to damage the plant itself(they are phytotoxic as well as fungit oxic), and they can
be washed offby rain. This necessitates repeated spraying during the growing season, and
ultimately leads 10 a build-up of tOllic s ubstances in the soil. Long-leon use of Bordeaull
mi llture on grape vin es has produced con cen trations of up 10 130 ppm C{l pper in the soil.
One early alternative to Bordeaux nUlltuer was su lphur, applied ase1ememal sulph ur
or as lime-sulphur. It is not tmie \0 animals. and is still occasionally used to oonlrol pow.
dery mildews, apple scab and peach leaf curl. but it may 'seorch' leave s, causing them to
drop. and can have a dwarfing effect on planK
M e r curous chl or id e was also found to be an excellent broad-spectrum fungicide
(heavy metals denature a wide range of enzy mes), but its residues can cause both acut e
and chroni c toxicity in animals. Its l D", to rats-the amount OIat will kill halfofthe animals
ellposed to it-is loS mg/kg. and longterm exposurc to even vcry low le"ds of merCury
eventuall y causes sevcre brain d am ~ge (Mi na mata disea>e).
Resistance to Fungicides
As yol.! read through the earlier sections of this chapter. you probably noticed that
the phenomenon of target resistance to fungicides became Lroublesome on ly after the
introduction of the systemic fungicides. It transpired that the resistance was developing,
not because these fungicides were systemic, but because they acted on very specific sites
within the fungus. A broad-spectrum fungicidc li ke mercury poisons so many enzyme
systems- it is a multi-site fungicide-that only an absolutely inconceivable number of
simultaneous genetic alterations could confer resistance on a pathogen. But BCllomyl
operate s by interfering specifically with microtubule assembly in ascomycetes, and it has
become apparent that some target organisms, when repeatedly exposed to Beoomyl, rapidly evolve strains that are resistant to this and other benzimidazole fungicides. This story
has been repeated with each new f~mily of systemics_ Resistaflce has been reported to the
acylalanin es (Metalaxyl), to the carboxamides. and even to some oflhe sterol-i nhibitors.
Dodinc is a pro tectantleradicant (LO", (rat) == 1,000 mg/kg) us~d against apple scab.
Resistance was reported in 1969, after this fungicide had been used exclusively in some
orchards for 10 years. Resistance 10 Benomyl was noted in 1975, after that fun gicide had
been used cxclusively and repeatedly for only 2 years. Orchardists who used Benomyl +
Oodine began to experience resistance to the combination in 1978. We now reali ze that it is
often best to ring the changes: to use mixtures of unrelated fungicides, or to apply a
sequence of different fungicides, as part of an Integrated Pcst Manageme nt scheme. Had
this bt.~n done in itially witll Benomyl, we would probably be expe rienc ing fewer resistance
problems with this fungicide today.
FUNGICIDES 221
industry asked that it he abandoned. MClalaxyl is an excellcnt substiru tc, h lll signs of resistance havc appeared, so this ambimobilc sy~temic is now often mi;I:cd with a protectant such
a, copper oxychloride. Satisfactory control involves using (I) resistant hop cultivars, (2)
sanitation-removing infected matcrial, (3) timely application of fungicidcs.
Many systemic fungicides arc almost insoluble in water, and the plant cuticle heps
water-borne substances out as well as in. So if these fungicid~s are dispensed as wettable
powders (WP), after the spray droplet has dried, most of the fungicide wi!! still be outside
the plant. More fungicide gets in if it is supplied as an emulsifiable concentrate (EC), and if
surfactants (to lower the surface tension of the spray and make it spread O>.lt over the
surface of the plant) and humectants (to slow the drying of the droplets) are incorporated.
These measures allow lower dosages to be used. New sprayers are now being developed
which increase the efficiency of application by dispersing the fungicide in finer droplets
than ever before, and by placing an electrostatic charge on the droplets, so that they will be
drawn dire.::tly to the plant.
The most efficient use of fungicides is ohviou~ly as ~eed dressings. Com is grown
on over40 million h~ctares in the U.S., and over 90% ofth~ seed is treated with fungicide.
Wlthoutthi, treatment, it is estimated that yield would be reduced by 10-12% in most yean.
Seed treatment involves some contamination of the ,oil, but since the newer fungicides are
nOI very peNistent, and the amounts applied per hectare are minute, thi s is not a serious
problem. Seed and root dips are also sometimes employed.
Many crops need more than seed dressings if disease is to be adequately controll ~ d.
COllon receives seed tre~tment. in-furrow treatments, and some foliar sprays for 'cotton
rust. Without fungicides, it is estimated that 20% of the cotton crop would be lost. Peanut
leaf spot (Cercospor(l: Hyphomyce tes) is potentially devastating. No resistant cultivars
exist; crop rotation docsn't help in controlling leaf diseases; and the cond it ions17.."i1Iikclioo (leaves wet for4 -6 hours. or near 100% R.H. at temperatures alxl\'e 22"C) exist almost
e\'ery day in the S.E. United States. Fungicides have to be applied every two weeks. Los,es
due to leaf spot diseases are now 2.5- 15 %. Without fungicide, this figure would soarlO 2075%, and peanuts would not be worth growing.
No discussion of fungicides would be complete without some menlion of several
other techniq u~s for controlling or eradicating fungi. (I) Soil steri lization may invol ve
>t~am or dry heat treatment, or chemicals such a;; formalin, chloropicrin and methyl
bromide. Some of the same chemicals are also used to co ntrol arthropods an d fung i in
stored food. The Canadian Government has recently banned f,ve chemical fumigants,
induding ethylene dibromide, which has been identified as a carcinogcn, and mOSl other
a\'ailable fumig~nts are under inveSligation. (2) Ami -mould compounds are often added \0
paints. fabrics, paper, cosmetics. soaps. etc. Many modcm fungicides are good candidat.:s
for such uses, because they have low solubility in watn, an: non-toxic to mammal s. ~re
biodegradable, and arc not very persistent. (3) Mould inhibitors- weak acids such as
sorbic. benzoic. acetic. or propionic acid , or their esters, which are fungus inhib itors rath~r
th3n fungicides- arc added to some foods. Calcium propionate, for examplc, is added to
bread to extend Its shelf-life.
Further Reading
Canadian Journal of Plant Pathology-recent issues.
Johnston. A. and C Booth (Eds.) (1983) Plant Pathologist's Pocketbook 2nd Edo. Commonwealth Mycological Institute, Kcw.
l"o"larsh, R.W. (Ed.) (1977) Systemic Fungicides. 20d Edn. Longman, London.
PhJ1oputhology-rccelll issues.
UFPE.CCB
DBIBLIOTECA
14
Introduction
In recent years we have begun [0 understand the consequences of the widespread
alld !"(."peated IISC of chemical biocides [0 control the host of organisms. such as insects.
weeds and fungi. that threaten human interests. You probably know that while many pests
became resistant to persistent pesti cides like DDT (:I chlorinated hydrocarbon), predatory
bird~ such as the Peregrille falcon suffered population crashes as a result of the biological
accumul:uion of DDT residues. Since we, too. aTe at the tOP of many food webs, this and
O(~r ellamples could hardly be ignored. We soon phased out the more persistent pesticides. at least in North America. and imensified the search for replacements.
;-:ewer generatio ns of pesticides are less persistent, but are often very to)(ic to many
non-wgct organisms. including the natural enemies ofme peSts arKi. not too surprisingly.
humans, The elimination of natural enemies may allow outbreaks of secondary pests. and
rapid resurgence of the target species, once the pesticide loses its activity. To rnJke things
WOl"$ e. some peStS soo n de velop resistance to each ncw formulation. Ne vertheless. many
chem,cal peslidd~s give quick results and a high level of control, nnd no subs titutt~ aft
yet available for most of them. SO we will incvitably go on using Ihem for many purposes:
but it makes good sense to look for less dangcfOlls altern ~tives, Biological control--often
shoruned to biocontr ol-is one of these alternatives.
How does biocont roi work? We bcgil1 by looking for a l1atural pred:lIor. parasite. or
COmlXtitor of th~ organism to be controlled. then we try to shiftlhc ecological equilibrium in favour of this bioo:;ontrol agent so that it can drastically reduce the population of
the target organism. These are simple principles. bU I their practical application is often
difticult.
;';alU ral enemies of pests and pattlOgens m;\y be few. rare. or inconspicuous. They
may be found only in restricted :treas, or at specific (imes of year. they may have compkx
life hlstones Inl'oll'ing two hosts. and they 01;1)" auack friend as wdl as foc. They may
even hale be",n I,,[t behind when the peSt 'migrated' to a new area or continent. II often
t~kc,; pat ient d~t!C lh'e work to bring them to light. then years to test their host nnge,
dcvelop techniques (0 mass-produce them, and learn the most effective ways und times to
introduce them to the hosl population_
It is encouraging to know that biocontrol h~s alrtudy had several spectac ular successeS-)OU may already be aware of the moth (CacroblaJlis: Lepidopte ra) which was
introduced toAuslralia to controithe pri ~k.ly pear (Opumlc.; Caclaccae) which was taking
o,'er n;t areas of grazing land; and the myxomatosis virus which was introduced to
222
Conidia!>of" .
Trade name
Di~isiOft
Principal target
Coelomomycu
&!lorrwplulrora
Zygomyrota
Aphilb
Conidiobolus
ZygomycOla
Aphid.,
Beallvena
Bowrin
HirSllfrlll1
i\lyclir
MelarhizjUm
l\Jetaquino
Verticil/ium
\ 'ertalte
Vmiciiliwn
"'yeotal
NOlllllraea
AschtnOllia
Dikal'}'omyco!.l
Colorado beetle. codling moth
(Hyphomycctes)
DikaJyomycota Citnl'i rust mite
(Hyphomycttcs)
Spittlebug, mosquito 13f\<lC,
Dikaryomycota
rhinoceros beetle, lepidoptemn
(Hypitomycctes)
[on"
Dikaryomycota
Aphids
(Hyphomycetes)
Dikaryomycota
Whitelh"
(Hypi!omycctes)
Dikaryomycola
Lepidopteran 13J\<le
(Hyphomycetes)
Dikaryomycota
Whitefl}. scale insects
(Coelomycetes)
~GI
r-.. nge of etllomogenous fungi. They can be attacked by members oflhe Chytridiomycetes.
Zygomyceles. unitunicale and bitunicale Ascomycetes. Phragmobasidiomycetes, and
conidial fungi (Hyphoffi)'celes and Coelomycetes). Since scales and whiteflies are diffi_
cult 10 control by chemical means, I think we may evetllually use mycoinsecticides
routinely to keep them in check. Another potential application for biocontrol is in the
suppression of anhropods that infest stored food . where it is impossible. for obvious
reasons, to use regular pesticides. Table 14.1 lists some of the actual and potential uses of
fungi in biocontrol of arthropods.
Nematodes. rotifers. copepods, tardigrades. collembola. soi l amoebae and other
microscopic animals are also parasitized or preyed upon by fungi. I use the l.mer phrase
advisedly. be<:ause a number of microfungi (again from scveral major t.a)(onomic groups)
are actually predators of these animals: they ha"e evolved special trapping devices with
which they catch their prey. thereupon sending in hyphae to exploit the newly acquired
substrate. Other parasitic fungi have small spores ofunusua! shapes, which when eaten by
the unSl.1specting animal. catch in its gullet and colonize its viscera. But these stories, the
pictures that will help you to visualize this strange microcosm, and the possible roles of
such fungi in biocontrol. can be found in chapter IS.
Pucc1n~
Fh,agml<1i_
>\ II~
cCG~~
,
p~cm~
0
ACf~""'n ium
C,,/I.-e /rlol!u,,"
FU~ GI
Ta ble 14.2 Ac1uai (A) a nd potential (P) appUcalioD5 or fungi in weed rontrol
Fungal Biocontrol Agenl
Weed Tatgel
Chondrilia ju/lua
(rush skeletonweed)
R"bu$ sp. (blackberry)
Xanthium spino$UIII
CA) C gloeosporioidu
(Coc:lomycetes) COUl'gO
Atschynomene virginiC/l
MOff1mia (X/orata
(strangler vine)
Pleridium l'quilinJim
Sida spinosa
(pric!;J.y sida)
Cassia /XCiden/ClIiJ
(coffee senna)
(Coe lomyceles)
(P)
(P)
C. demarillm
(bathUfSt burr)
(bracken fern)
COrNo/vu/us afllfnsis
(Coelomvcetes)
(field bindweed)
(P) C c()ffQt:/es
(Codomycctes)
Abu/ilon rheophra.fli
C. gloeosporioides
(vclvetleaO
Jusrimw decurrens
Area
wheat. Australia
pastull:s. Chile
r.rngeland., Australia
pastures. Britain
U.S.A.
sorghum, U.SA
lima beans, U.sA
rice. U.S.A.
(Coelomycelcs)
Cassia $uratll:llsis
(Hyphomycetes)
(kolomana)
Dio$pyros virgillialUl
umlWUI cornara
Eupatorium adelloplwnull
(Hyphomycetc.~)
(crofton weed)
Cauia obtusifolio
(Hyphomycetcs)
(sicklepod)
Anoda crisfara
(spurred anodal
COtton. U.SA
Anoda eris/ala
COlton, U.S.A
AIllJiia
cotton, U.S.A
(persimmon)
(lantana)
eri~'/(j /(J'
Sida spimm,l
(pric kly sida)
pastures, Hawaii
r.Ulgeland. U.S.A.
rangeland. Hawaii
Au stralia
COlton. soybean. U.S.A.
Tabl e 14.2 Actual (A) and potential (P) applications or fungi in weed control, cont.
Fungal Biocontrol Agent
WeedT~et
Cucuroi/a feutJ1l.l
(Texas gourd)
( A) Cerrosporo rodllwnii
Eiclwmio crossipes
(water hyacinth)
..".ater. tropi,s
Eichomin crassipes
(water hyacinth)
water. tropi,s
Eiclwmia crllSsipes
(water hyacinth)
water, tropics
waler. tropics
(Hyphomycetes)
Eiclwmiu crossifles
(water hyacinth)
Cirsillnt arvenu
(Canada thistl c)
CO/lI"O/vu/U$ nn'lmsis
(field bindweed)
(Hyphomycetes)
(P) Acremonium co/w.1ll1n
(Hyp/lomycete~)
(Hyphomycetes)
(P) FlI50rillm Itlseum
Table 14.3
Some n~tual and potential applications of fungi in the control of fungal plant dIseases
Target fungus
(anamorphi~
Rhizoc/(mia so/ani
Aphyllophor.:Jles)
Biocontrol fungus
(Hyphomycel~S)
damping-off. roo!
rot. stem C':lnker:
many ~rops
Trichodemm viridt
silverleaf: plum
H(/erobasidwn willosum
(Aphyll ophorales)
HelerobasiJion anllOSUIIl
(Aphyllophoraks)
Peniophora giglllllea
(AphyJ lophor.ll cs)
Annillnria trU!IIM
(Agari~ales)
Slere"", pllrplmmm
(Aphyllophorules)
(sd~rotial
damping-off:
seedlings
stem blight:
~anulS
anamorph)
Venicilfjum fimgicn/a
(Hyphomycetes)
fl/sarill/!l m.!eum
(Hyphomymcs)
Phyroplillrom cinllamomi
(Oomycete~)
Vatidllium alboa/rlml
(Hyphomycctes )
dry bubbk:
wilt: COllon
Venicillium dalrli<le
(Hyphomyce tes)
wilt: eggplJJ1[
Venicifllllm tUllrliot
(Hyphomywes)
wilt: mim
Aill'mnri(l :in"I'(I(
(Hyphornycetes)
Cln"iceps pUrpUTeli
(Unitunicatae)
ergo!: gr'->,;cs
Sphaavrileca fi(liginl'(I
(Unilunicau.e)
TrichlXkmw h(lJII(1/wn
(Hyphornycctes)
Tric/rft!mm Irar.,iamun
tHyphomycetcs)
Tr.chlJ(lemw sp. (HyP/1Ol1\yCClcs)
mushrooms
seedling blight: com
Chatlomium glahoslIIn
(1: nitunkalal!)
Le:/Copaxil/u,! sp. (Ag:mcnJes)
\ "or-irillium al/H)olUrum
(H: pholTIy~'Ctcs)
Ta!<lfoltl)'ce.r jla<'us (Eurotiales)
\i-nicilfillln nigrescel1s
rH:phomy~etes)
poy,dcry mildew:
cucumlx1'>
I,
Ai:un.aria lenuiJ.r;'n(l
(Hyphomycetes)
F!I.lUT;Um ro.it!wn (Hyphorn}cetes.)
Cicinnobo/u! aSaI;; (Cot!omycctes)
BiOo::ontrol fungus
CrQlII:mium ribicola
(Uredinales)
7id>erculirw maxima
(HypOOm)'L-etes)
Cronartium slrobilinllnl
(Uredinales)
Sphoerrllopsisjilum (Coelomyccte$)
Coniorhyrium minitallS
(Coelomyceles)
"'P'
Gaellmllnnomyces grominis
(Unitunicatac)
take-all: wheat
Phiolophom mdicicola
(Hyphomycetes)
Crinipellis pemiciola
( Agarieales)
witcheS: broom:
CltuiJJbolf)lIIl! lIma::Ollcnse
(Hyphomycctcs)
BOII"pi s cinerea
(Hyphomycelcs)
,=
grey moul d of
strawberry
Gliodadilllll rosewlI
(Hyphomyceles)
cucumb<:rs.
(4) CfadobolrYllm ama.:o nense (Hy phom ycetes) g ivcs control of Crinipdli~
pemiciosa (Hulobasidiomycetes. Agarkales), wh ich causes a seriou, dise~se of cocoa.
called witches' broo m.
Competition be twee n fungi is the area ill whi ch biocont rol of fungal pathugen s has
achieved its gfl:ate~t succes~s. Species of Trichoderma (Hyphomycctes), green moulds
common in some forest soils, arc powerfu l antagonists 10 many palhogens.
(5) Trichoderma \iride both parasitizes lhe hyphac of many othcr fungi and produce,~ an antibiotic. This double-barreled appro3ch allows il to deal effectively with soil
pathogens such as Rltiz()Ctol!ia solani (a sterile basid iomycetous anarnorph that causes a
variety of diseases on many hosts). and Armillaria mel/eo (Holobasidiom >'cetes, Agaricales),
wh ich kills ma ny species of trees.
(6) h iehoi!emm han;ianum, ma,s-produced in \: u) ture and applied to soil. controls
Sclerolium rolfjij (another sterile fu ngus which causes diseases of many hosts) 011 tomatoes and peanuts. A ph:umacemieal company is developing T.ltar:iantmt as 11 commercial
biocontr{)1 for SclerotiulII rolfsii_ Thi~ could be indirectly frustrated by the fact that peanUl~ arc very susceptible to anatk by Ctrcospqra (Hyphomyceles) ..... hith causes a serious leaf-spot disc3<;e. Repealed fungicidal sprays ne<:ded to comrol the Cef{;o.<[JQ'" also
reduce Ihe population of Trichode mw and lend to an increase in stem blight caused by
Sclerotium rol/sii.
(7) Ncyertl1eltss, in France, Trichodemw spray concenlrate is competi tive in pri ce
wi th the we ll-known S)"$lcmic fun gicide. Bcnomyl. and is u~d to control Verticillitlm
fimgico/a (Hyphomycetes). a o;erious p;ilhogcn of the cultivated mushroom, Agaricus
bnlllnesctns (~'garicales).
( I I) Spraying apple leaves with spore suspensions of Chaelomillm g/obosum (Ascomycetes, Sordari ales) reduces infection by the apple scab fUngus. the Spiloc(!ea
llnamorph of Venturia inaequalis.
/
,.,..
~t._'m
RMZOt:I""~
-----
TriCII_
Pon/(lpll.;q
VMicllllum
j .. . , -,,t
'; <;::C'
,. , .
"
~I
,
.
,{~/L:
, C
,
~-
lil,'
,
i\':-,
\"
AU.m",l.
r.g. 14.4
("
Fo>url"m
-,
"') \ '' ;
v'"
rU""culin#
G'J
Fig. 14.5 ....\ore f~ bioconIrd agents and lhei" target patlq,ti IS (see teJd).
Further Reading
Anon. (1980) Proceedings of\\'orkshopon insect peS! manageme nt wilh microbial agcms.
Boyce Thompson I nstirut~ . Ithaca.
Baker, K.F. and RJ. Cook ( 197.l.) Biolo~i cal Con trol of Plant P..llbogens. Fm:man. San
Francisco.
Baker, R. . P. Hanch ey and S.D. Donarar (1978) Protectio n of carnation againsl Fusarium
,
stem rot by fungi . Phytopathology 68: !495-150 1.
Bastos, C.N . H.C. Evans a nd R.A. Sa mson (1 981) A new h}~rparasit ic fun gus.
Cladoboll)"W1l am07.0ntnSf . with pote ntial for control of fungal pathogens of cocoa. Transactions of the British Mycological Soci~ty 77: 273-278.
Burges. H.D. (Ed.) (1981) Microbia l Control of !'ests and I'lant Disuses 1970-1980_
Acudernic Press. New York.
Charudattan. R. and H.L. Walker (1982) Biological Control of Weed s with !'Iant Pa thogens. Wiley_t-.'w York.
Cu!len. D.. EM. Berbce and J.H. Andrews ( 1984) Ch(1elOm iwlI glabo.lllm antagoniles the
apple scab pathogen. Vetlm ria in(1eqlwlis. under field conditions. Ca nadian Jourmil of Uolany62: 181 -1-18 18.
Culkn. J . ~I., PF. Kable and ~\. Can (1973) Epidemic spread of a IIlst imponed for biolog ical control. !'ialure 244: 462464.
Ferron. P. ( 1978) Biological control of in sect pest, by entomogenous fungi. Ann ua l Re\iew of Ent omology 23: -109-442.
Frcem~n. T.E. (1981) Use of con idial fungi in biologic al control. pp_ 143- 165 (in) BiologyofConidill1 Fungi. \ '0). 2. (Eds.) G_T. Cole & B. KendriCk. Academic Press. Kew
York.
Glltterid&e. RJ . and D_B. Slope (1978) [!ffec t of inoculating soils wjth Phinloplrora
mdicjcola var. graminicola on takcall disease of whem. Plant Pathology 27: 131135.
Harman. G.E., I. Chel and R. Baker (1980) Trichodt nna hnmwllm effec lS on seed :md
se~dling di sease induc ed in rudi~h and pea by Pylhiwn spp. or RM:OClon;a .!Clani_
PhytopathQlogy 70: 1167-1 112Hasan, S. (198 1) ,.l,. ncw strain of Ihe ruSt fungus Puccini" Ch(Hldrjlfilla fOf" biological
control of skeleton weed in Australia. Annals of Applied Biolo~' 99: 11912-1..
451.
UFPE.CCB
@BIBUOTECA
Fungi Exploiting
Microscopic Animals
15
Introduction
As a tiny soil nemauxle wriggles along, its head passes through a tiny hoop. Its
body follows, sliding smoothly through . JuSt as it is about to clear the hoop. th is suddenly
innnleS inward and grips the wenn tightly. Thra~h about as it will, the wonn cannot
escape. Soon its tail end triggers another ring- trap. It has been captured by a fungus, and
itisdoomed todic(Fig.IS,\).
'
.' "
I I ,
239
ANl j\ I A I~"
241
(2) Inj ec tl'd spo res: The oomycctous genus Hap/oglossa (Fig. IS.2 C, 15 .3) is
unique among fungi. It produces spores which, though non motile, are sophisticated
'harpoon cells: A harpoon cell adheres to the substrate and sits with Ihe balTel pointing
upward at a low angle (Fig. IS.3). It has a high turgor pressure. and is triggered byeontaet
with prey: a built-in line of weakness ruplUres. and an internal tube with a harpoonlike
tip is rapidly evertcd with sufficient fon:e 10 penetrate the integument o f tbe prey and
injecl sufficient m~terial into the animal to fonn a tiny infection uni!. This is an ex tremely
highly evolved mech~nism: its con sider~blc mecha nical com pkxity can be clearly seen
in Fig. 15.3. TIU! only comparable m~ch allisms I can thi nk of arc: (a) that of the zoo:;pore
in Pla.modiopham, a colonial pmtoctistan. and (b) that of the nematocysts of the antmal
phylum. Cnidaria (corals, sea anemones and jellyfish): there i~. of course. no sugg<ostion
of homology here.
Afler Ihcsc fungi get inside the animal. they grow through ils internal organs. absorbing nourishment from them. This is not healthy for Ihe animal. which SOOIi expires. lis
corpse eventually hOIl~s scveral to ma ny mitosporangia. which liberate large numbers of
thgd late or injective propagu1es to be gin the cyc le again. Sexual reproduct ion can also
occ ur. und M yWC),lilllll. for exampl e. some times fills its hos ts with oogonia. each ulti
matdy containing a thickw alled. resting zygote (oospore).
(3) A d h e.~he s pores: Meriflacrulll is a common nematodeexploiting rygom)"ccte.
From a pa.ra.~itized nemalode arise taU sporangiophores with helically twisted apical
It"j!ions_ Sticky one-spored mitosporangia arc produced on lhese. and are forcibly shot
away- If they dont nUlke contat:1 wilh a nemalode. lhey will germinate and form a small.
adhesivecoated secondary spore at the top of a liUle SI:l.lk. These stick to nemntodes:
some cause infection, while others form secondary spores, and the hos t worm may thos
spread the infection \0 olher nematodes while il can still move about.
HyphQmyceteS are well-represented 11ll1Qng the nematode-e)(plo iling fungi. and
have evolved the widest range of techni ques for gaining access to the interiors of nematodes. Verticillillm and M~ ria (Fig. 15.2 D) use the sticky-spore Ie<:hnique already mentioned. Once pcllCl17l1ed by the germ rube arisi ng from these conidia, the worm is doomed.
After a few day s. its body is riddled wi th assimi lative hyph ae. The n the fungu ~ breakS OUI
of this capsule and produces charneteristie conidiophore!, bearing adhesive tonidia. The
conidia of Nematoct01lIlS Itiosporus (Fig. 15.4 A), after becoming detac hed, deve lop a
vertical extension thaI en(\s in a slic ky, infe<:live swelling. The assimi lative hyph~c inside
the hosl h3vc clam p connections, showing that thi s is a dikaryot ic b.asidiomycc tous
anamo.-ph. Several species of Nemaloc/{;mus h/we been show n to be anamorphs of species
of Hohenlmehd ia (Holobasidiomycetes: Agari caks) (see also method 8. below).
(4) Ingested spores: Some byphomyeelCS have evolved conidia that art designed
10 be eaten by their victims. The conidia of Hmposporirlm angui/lllla~ (Fig. 15.4 B) are
crescent -shaped, with a sharp poin t at one end. These conidia literally Slick in the craw
(acruaUy the oesophagus) of the wonn. and from this initia l bridgehead their hyphae soon
penneatt the host. Evenrually. new conidiophores arise from the defunct nematode. It has
rec ent ly bee n d iscove re d tha t Ih e te leo morp h of Harpospo rjllm angulI/lilac is
Alricordyceps lrarposporifera (Ascomyc etes, Cla\"icipitales), which allacks millipedes.
This is the only case I know of in which the 3nalllOfph exploits One group of animals. tile
telromo rph another. Olher specks of Harpospor;wn al so have 'edible' con idia. Those of
nematoCe
,
Fig. 15.4 A Nem,ltoctonus /eiospc>rU5 (~tic ba~ an,unoq:h) S1icky ccri:la
penetrari1g the IvJSI nematode ardOO<.~assi"rilti...e hyphaewithd.m1JCCIIl"'II:'COOn; 6;
Hilrposparium anguillu/,lC{anall"KXph ci AtricordfCt'ps harpasporiff>rJ. Ascomycetes,
ClavicptJ!esJpror:l.01g ~ and CuveQ, poi1tcd ccriia t:hat are i;lgesll'd by the host ,,-orm
.,
" ..;.
,
H. diceraeum (Fig. 15.5 J) have a striking resemblance to a high-hee led shoe or clog:
th~ o f H. rhynchospqnlffl (Fig. 15.5 K) look like cartoons of small birds minus lcgs. In
e3ch case there is a subtle asymmetry. and OI1e or more sharp poims. which undOUbtedly
combine to help the conidia lodge in the muscle of the worm's buccal cavity or oesophagus. The longer conidia o f H. htlicQidu (Fig. 1S.S L) don't picrce the gut wall me<:hani.
cally, but germinate in the intestine and infect the worm just as effectively from there.
Ha rpospori/,m spirosporwn has sinuatc , twisted conidia wh ich are vcry sh arp at
both ends. These conidia are eaten by rotifers, and lodge in the gullet or mast1l)l. to initiate
an infection. AI least twel ve species of the hyphomycete genus DihtltfOspora parasitize
rotifers after th ey ingest conidia. Altho ugh these conid ia are nOt pointed, they still lodge
in the mouth, gullet o r mast1l)l., and penetrate the body cavity of the animal in the usual
way.
f
......
2
~
~r(
F~,; .
with nematode gluc, and often situated at the e:nds of short side-branches. The y are found
in ne:arly twenty species o f Arlhrobol1)'S, Daery/ella and NellUll(x/()IU~ (all H>-p/"oomyccteS).
Sometimes the: knobs are finnly enough anachcd 10 prevent a nematode from le:avillg the
sce: ne, particularly if the animal has stuck to se veral of them at once:. Oftcn the nemat ode
tears a knob loose from ilS moorings and makes good its t!5capc:. B ... I the ens ... ing freedom
is short-lived. The knob remains fi nnly auachc:d to thc worms cuticle, and soon sends in
an infective hypha. Game ovcr.
Some species o f N enl(lloCIOnU$ which ale anamo rph s of the gille:d f ungi
Hohenb/.,ehe{io and Resupinoms (Holobasidiomycetes. Agaricales). produce unique adhesive knobs shaped li ke: hour-g la.sscs. enveloped in a drop of glue: (Fig. IS.6 C). These
knobs do nOI break off. but hold ne:matodes firmly while infection proceeds. The clamped
hyphae of N enlo/(xto"us also be:arconidia (Fig. 15.5 N). but these Me nO( infectious until
they have germinated and formed a sticky knob at the end of the genn lUbe.
(8) Adh es ive nets (Fig. 15.6 F,G) Me probably the commonest trappin g device. si nce
they have been recorded in nearly 40 species of fungi. They may original ly have evol ved
by anast omosis of adjace:nt adhesive: branche:s (only Eumycotan fungi can do this). and
so me of them are still simple hoops. Others are more comple x. ranging from two-dimensional ladd e r-like arra ngements. to the con torted threedi mensional labyrinths o f
Arthrohol1)S oligosporo. the commoneSt nematode-trapping hyphomycete. These networks can arise only as a result of rep<atcd anastOmoses. The advantage of the more
complex systems is not simply tileir greater extent. but also the fact that l ~rgcr nematodes
are likely 10 bc:L-omc stuck at more than one point. and;\K therefore: less likel y to escape:.
The: adhcsive works equally well on dry and wet nematodes (though not on other soil
an imaL,). The nematodes are not just blind. insens ate victims: they often ~coi l violently
when they tOuch an adhesive net-an ,,ersive reaction that sometimes saves them from
cenain death. When the: fungus is successful in establishing adhesion. an infecti~'e hypha
soon penetrate:s the body of the prey. and the wornl becomes comatose within an hour: so
quickly. in fact. Ihat the fungu s is suspected of producing a loxin. Afte r Ihe prey has hc:e n
riddled by absorptive hyph3e. the convened biomass is exponed~transl()(:aled to the
extcrnal hy phae. which lise Ihe energy. spider-like. to spin new ncts. and also to produce
the distinctivc conidiophor~ s of ArthrobOirys oligQsporo , with their sUL""Ccssive: cl usters
of ty,o-cellcd. co!ourle,s conidia.
(9) Non-constrict ing rin gs (Fig. 15.6 E. 15.7 A). which could also be: called det achable rings. ar~ produ ced by four spel.'ies of ArthrobOlr)s and D"ctyicllo (H)phomycetcs).
A sing!.: byp ha grows around in a perf~ct circ le. tinally anast omos ing with a new bud
waiting at the: tOP of the: stalk-to-be:. The three-celled ring is stouter than the stallc When
:I nematode craw ls through the ring. this fi ts snugly around its body. and easily breaks
~\way from the narrow s talk. The worm g~s on i l~ way we aring its newly a~ quired coll~r.
As you will have deduced. inf~ction and ass imilation soon follow. All species with non
con~tricting rings produce sticl")' knobs as lIell (Fig. 15.7 A). In terms of the spre:ad of the:
pathoge n. it is interesting to note that fungi producing sticky spores. or dctachable knobs
or loops. may be carried somt dist ance by the anim al before it hecome, incapacitated.
(10) Constricting rings (Fig. 15.1. 15.6 H. 15.7 B-D) are the mOSI SOphistlclllcd
nematode traps o f all. They are produced by twelve Hypbomycetes. especially specks of
A rrhrobQ/rp and O(lelyiella. At first sig ht. thcse tra ps seem very si milar to non-constricting nngs: thc ring is composed ofthrce cells. borne on a stal k. But here the stalk is shoner
and stronger: these traps:rrc designed to stay put. Their oue: nature is revealed only when
they are triggered. If ~1 nematode passes through the loop. and louches the inside of one or
more of the cells, all three: cells s imultan~ou s!y innatc inward. in about one-tenth of a
detachabl"
stK:ky knobs
B: de>lelgping
CO/\Strlaing
"".
conidium
Fig. 15.7 Arthr obotrys (Hyf>homtcetes). A: A. f:andida with detachable sticky knobs, and
detachable oon-constrictl'lg rilgs; BD: A. hrof:hopaga- B: ~ constricting ring uap; C:
geminated cori!it.m which has formed a constricting mg trap; D: cooidumywith a constricting mg
trap wl>ich has caught a nem<ltode.
~ UFPE-CCB'
O BIBLI OTECA
Chemical Warfare
(I I) Toxins: mycelia of the widely-ealen and cultivated 'oyster mushroom: Ple!'rvIIIs
oS/Utl/us, and se\<erol other Pleura/us speeies. secrete a substance lh al rap idly inactivates
nematod~s. allowing the fungus to colonize their inert bodies. Since P/t!"v/us species are
often primary ~olonizers of dead wood. a substrate notoriously deficient in nitrogen. the
nematodes may be an important compon ent of the fungal diet. us they uppcared to be for
the other agaric s (HQhenbueIJe/ia and Reslipilllltus) mention~d earlier.
A f~w fungi parasitize nematode eggs. RhopalomJces elegallS . a striking zygomycete
commonl}' encountered on dung. is one of these. N ematod~ eggs appear to release some
Further Reading
Barron, G,L. (1977) T he "'emalode- DeSlroying .' ullgi. Canadian Biological Publica
tions. Guelph.
Barron. G. L. (1981 ) Predators and parasites of microscopic animJls. pp. 167100 (in)
Biology of Conidial F ungi. Vol. 2. (Eds. G.T. Cole and B. Kendrick). Academic
Press. New York..
BalTon. G.L. ( 1985) Fungal para.~ites ofbdclloid rotlfers: Dihl!laospom. Ca nadian J ournal of Botany 63: 21 1-222.
Barron. G.L. (1986) A ne w H",p();poriwll parasitic in bdelloid rotifcrs. Ca nadian Jo urnal of Bntany 64: 2379-2382.
Barron. G.L (1987) The gun cell of HIIP/(}glossil mirabifis , i'> lycologla 79: S77-8S3.
Barron. G.L. (1990) A new predJtory Hyphomycete capturing copepods. Canadia n Jo urn:ll of Botany 68: 691 696.
Duddington. C.L. (1962) Predacious fungi :lOd the control of eelworms. Vje\'.. pohll ~ in
Rio lOg)' I: 15( 200.
Gray. i".F. (1987) Ncmatophagous fungi with particular reference to their ecology. Biological R ~" i ew 62: 245304.
Nordbring-Henz. B. (1988) Ecology and recognition in the n~matode/nemutophagous
fungus syStem. Ad.-anns in Microbial E(olng}' 10: 81 - 114.
Samuels. G.J. ( 1983) Ascomycetes of New Zealand o.AldC(Jrdycep~ IUlrpGspo rijem gcn. et sp.
nov. and its Harposporium anamorph. Ne w Zealand Jou rl131 of Boumy 21: 17 1- 170.
Thorn, R.G. and G .L. Barron (1984) Carnivorous mushrooms. Scicnce 224: 7678.
Thorn. R.G. and G.L Barron (1986) Nenwr(Xr()1II1S and the tribe Resupinat:lc in Ont ~rio.
Can:lda. i't lycota.'\:On 25: 321<453.
I.!!
UFPECCS
DSIBLlOiECfI.,
16
Introduction
At flIst sight. such relationships sculld bizarre. e'>cn unlikely. Wh at service could
fungi render that would make it worthwhile for animals \0 modify their whole lifestyle 10
~ccommoda!e such uEens? And what could be in it for Ihe fungi, which uSUally compete
with animals for food?
th ~
cell ulose and lignin. Some animals. like me detri tivores in streams and ponds. wai t until
amphibious and aero-aquatic hyphomycclcs have exploited the plant remains. trn:n seek
out und eat the hyphae and conidiophores of these fungi. Many other anima ls. including
the herbivorous mammals and some termites, have overcome this deficiency in a more
efficient and reliable way. by harbounn g large popu lations of cellulolytic mic roorganisms in their gul. Then they cun eat the ce llul ose and li!"nin directl>', leav ing their g llt
microbiota to digest the s.e substrates for them. But certain soc ial insects. the mou nd building ter mi tes of Africa and Asia, and the leaf-cu tt ing a n ts of Central and $outh
America. have evolved a rat her differem strategy. They cultivate specific cellulolytic
fungi in underground gardens_ And [usc the words 'cuhi,-:ue' and 'garden' deliberately.
The in5('CI.'i establish pure. axenic cullures or speeial coevolved fungi. keep them consta ntly supplied with food and moisture. and ..... eed Oll! any comamin~nls. The fungu s.
then . receives vcry special treatment. and there is no doubt I h~1 il benefits from the
arrangement. How many Olher fungi have guardia ns th~1 keep out the competition. and
bring endless supplies of food? But then the ant~ and lennites have their turn. As you have
no doubt guessed. they arc exclusively mycophagous. The fungi have transform ed the
.....ood brought by the tenoites. and the leaves suppl ied by the ants. into digestible and
nutritious fungal biomass_
Leaf~cutting
The garden ing ants of the New World milke up the Tribe Altin!. Although you have
prohably never heard of them before. people in South America are only too fumiliar with
the m. Searchin g for leaves to feed to their tnme fungus. these anlS will defoliate trees and
growing erop~. In the sixteenth century. the invading Spani.u-ds may have conq uered the
native peoples of South America. but the O:l\ive ants gO! the beiler of them-their failure
to grow cassava lind citrus fruiu; .....as attributcd to Attine ants. whose nests. at the base of
250
Fig. 16. 1Sectional views of - A: terrnte lTlOU'ld; 8: atlne ant nest. f!X1g31 garden!; Of combs are
shown i1 white.
c _termlte
,
Fig. \ 6.2 Mycophagous nsects and the fl.ngo1lstructures they eat.
254 CHAPTERSIXTEEN
The taxonomy of the tennite fun gi is beller understood than that oflhe ant fungi. for
the simple reason thaI termite fungi fruit in nature (Fig. 16.3). When tennites of the genus
PstudncanlhOlumes desen a comb. Ihe fungus produces basidiomatal primOfdia on its
surface. When the rainy season suns, rainfall of more than 2 em/day stimulates the pri_
mordia 10 develop long stipes. which grow up 10 the soil surface and produce a large
pileus. These mushrooms are identifiable as Termiiomycu siriarus (Holobasidiomycetes,
Agaricales). Interestingly, the combs of fungus-growing termites are often inhabited by an
additional fungus. a species of X)'/aria, which may also produce stromata on the comb.
Although about 30 species of Tl'mli/omyces have been described. only two species of
XY/llria have been found associated with termites.
Macrotemlitinae are regarded as major pests of tropical agriculture, and they are
destructive 10 wooden buildings. They take scaret: organic matter underground. where its
nutrients may remain locked up for years. However, there are a few minor compensations.
Tennites are food for many other animals, and many Tl'Fmiromyces species are among the
most highly prized. and the largcst. edible tropical agarics: so moch so thai a1lempts ha\'c
been made to domesticate them.
u~PECCII
1'- 'n
,.
1
I
- i
\I
2~6
C HAPTER SIXTEEN
Further Reading
B:lIra. LR, (Ed,) (1979) Insect-fungus Symbiosis. AlhmheJd, Osmun. Montclair.
Batra, L.R. and S.W,T. Batra (1967) The fungus gardens of insects. Scil'ntilic America n
217: 112-120.
Bissett, J. and A. Borkent (1988) Ambrosia golls: the signilicnnce of fungal nutrition in
the e"olution or lhe Ceddomyiidae (Diptera) (in) Coe,'ol lliion or Fungi wit h Plants
and Anim:lls (Eds.) K A Pi rozynski & D.L . Hawks\vorth pp. 203-225.
Brundrctt, M.C. and B, Kendrick (1987) T he relationship between Ihe Ash Bolele
(Bolerinellus merulioide5) and an aphid parasitic on ash tree roots. Sy mbi os Is 3:
315-320.
Buchner. P. ( 1965) End osym b iosis or Animals with Pl ant i\Iicroo rganisms, Wiley, New
York.
Couch, J.N. ( 1938) Th\! Gellus Se ptolXlsid iu m. Uni versity of North Carolina Press, Chapc-I
HilL
Currie. C.R.. 1.A, Scott, R.C . Summcrbell and O. l'.lalloch(l999) Fuou~-growing ants usc
antibiOlic-producing b~Cleria to control garden parasites. Natu re 398: 701-7~.
Fishe r. PJ., D.J, Stradling and D.N. Pegler (I m) Leaf cutting ants, their fungus gardens
and the formation ofbasidiofIlma o f ullcoagoric"$ gOflgyloplwrJls. i\Jycologist g:
128- l3l
Pirozynsl::i. K.A. and D.L. Hawksworth (Eds.)( 1988) Coe"olution or Fungi with Phill is
and An imuls . Academic Press, New Yo rk.
Weber, N.A. (1972) Gard en ing An ts: the Au ines. Memoir 92 American Philosophical
Society, Philadelphia.
j
l
17
Mycorrhizas: Mutualistic
Plant-Fungus Symbioses
Introduction
When green plants first colonized the land. more than four hundred million yenrs
ago, the invasion may hnve >ucceeded because they established an intimate alliance--a
mmualislic symbiosis-with fungi. Early lund plams could photosynthesize effecliv~jy,
but hadn't yet developed extens ive root systems and must have been" hard- pre~sed to
a_cquire :"aler and mineral nlltrients. The filamentOliS fungi, which had themsel ves only
recently emerged from the water, were petfec!ly adap!Cd for exploring the soil and fin ding
those vcry things , bllt desperately needed energy-rich carbon compounds of the kind
produced by the plant". Traces of sugars l ind ammo-adds leak out of plants. and Devonian fungi were undoubtcdly attracted by these. The relation,hip5 presumably develoJX:u
in more thun one direction: some fungi remained soprobi": others became destructive
parasites, causing wilts and root rots; y_! mhcrs_eYalCd inlO-lu'!).utually beneficial sym-hiusih Proof of this lies in the fact that fossils of some Devonian plants contain well~
preserved fungal structures just like those we c~n find in the roots of more than 90% of
ealthy modem plant specie!; _
About a century ago, several biologists noticed that some plant roots, thou gh ext~nsi\Cly invadcd by fungi , were not diseased. The name m~Torrhi7,a (fungus root) wa,
coined in 1835. We now know that, especially in poor soils, mycorrhi zal plants gruw
beuer than non-mycorrllizal plants. This is because the hypJ:!ae of tile fungal symbioots
permeate IMge volumes of soil and obtain sCarce e!cments----especiall y phosphorus. whIch
is often limiting for plant growth which they pass on to the plunt in excllange fOf
photosynthates ,
Interest in these symbioses Ilas escalated dramatically in l"\Xem years, bec:)use of
the ir putemial benefits to agriculture. forestry, and the rev.:g.:tation of ecosyst~ms damaged by human activities such as mining. Some plants c:)nnot become e stablished or grow
normally without an appropriate fungal partner (oft~n ca lkd the mycobiont). Even when
plams can survive without mycorrhizas. those with 'fungus roots' ne",d less fertihzer.
withstand heavy metal and acid rain pollution bener. and grow beucr on the infertile soils
of margin:)l lands, un mine spoils and oth.:r areas ' n~eding revegetation , and at high
elevations. They also s,-,r ~ i ve transplant shock better, are more resi,tam to soil-borne
diseases, withstand higher soil temperJlUreS , higher soil salinity, and wider extremes of
257
2~
CHAPTERSEVE~IEEN
~
,.
'-
-, -,' I
~\ ~f
ECTOMYCORRHIZA
VEStCULAR.ARBUSCULAR MYCORRHtZA
endodermis
S1ete
corte.
otd arbuscvle
In tramatrleall'ly~~a
Hartig net
."
lu ngal manil a
i\lYCORRHIZAS 259
The mycorrhizal symbiosis, whethc:r ectotrophic or endotrOphic, must have three
basic functioning components: ( I ) fungal mycelium exploring large volumes of soil and
retrieving mineral nutrients: (2) a fungus-plant interface where the e ~changeof chemicals
can go on; and (3) plant tissues which produce and store carbohydrates. Strangely enough.
within each of the main groups of mycorrltizas, the root-associated fung al components
look rather alike. and we have to refer to otller components, (4) the reproductive Structures, before we can identify the fungus.
8: UClion~1 vit,.
fig. 17.2 EClomycorrl"izas. A: ~tomOUS rnycorrJ-izai short roots d Pinus; B: 5eCOOoal view of
p;lrt of Hartig net, note th.1 cortical cel is cornplelely SlI"I'Olnded by hy~e; C: SU'face view of part
of H<trtig net, showilg c~ ilter\ocking hy~
Systematics of Ectomycorrhizal
Fungi and their Hosts
Most EM (Ectotrophi c Mycorrhizal) fungi are holobasidl omycetes: membeI$ of at
least 73 genera in 9 orders. They are: (I) agari cs (2) former agarics which have become
sequestr:lIe (closcd. nOi shOOling spores at maturity). sometimes fruiting above ground.
sometimes underground (raise trum es); (3) some club fungi , c hantcrelles. tooth fungi.
and resupi na t~ hymenomycclcS (all Aphyllophornlcs). There are also cctomycorrhizal
fungi in 16 unHunic:!te as~omycete genera from 111'0 ord~rs . All but one of the se ascoTahle 17.1
Ta l<onomic Distribution or Ect omycorrhi zal Fungi
Phylum: Dikaryom ycola,
Subphylum: Basidiomycotina,
Order: Ag:u-icales.
Family: Amanitaceae
Hygrophoraceae
Tricholomataceae
Enl olomataceae
COrli nilriaceae
Paxillaceue
Gomph idiaceac
Boletaceae
Suobilomycctaceae
Ru ssu laceac
Order: Gautieriales
Order: Hymenogastral c~
Order: PhaUales
Order: Lycoperdales
Order: Mdanogastraies
O rder: Sderodermatales
Orde r: Aphyllophornles
S ubphylum: Ascolnycotina.
Order: Pezizales.
Family: Pezizaceae
Balsamiaceae
Geneaceae
HclvcIJaceac
Pyroncmntaceae
Tcrfc zi aceae
Tuberaccac
Order: Elophomycctales
Total gen:n:t
Number of
Genera
(2)
(I)
(6)
(I)
(5)
(2)
(5)
(13)
(3)
(5)
(I)
(8)
(I)
(I )
(' )
(3)
(8)
(I)
(3)
(I)
(I)
(3)
(' )
(2)
( I)
90
Table 17.2
Comparison of the PhytQblonts of Eeto- and Endo-Myeorrhizal Fungi
&tomycorrhi7.a1 Fungi
2.000 spp. of pl~t: m:l.inly
t~s
Gymnosptrms:
ALL Pinae~ae & som.::
Cupressac:eae.
Angiospenn~:
Endomycorrhil..al .-ungi
300.000+ spp. of pl~ts:
herb.lccous, y,'OOdy.
380 Families:
(EXCLUDING: ALL
Brakaceae. Commclin:JI."tae.
Cypcl':lCeae, Juoc3CCae,
Proteaceae. SO :'>lE
Amar:ll1!haceac,
Caryophyllaceae,
Chenopodiaceae. PolygoMeeae.
members of 3 other fami Lies.
and I\'IOST ectomyconhiwl
SOD.)
studi('d. The P<'r~entage of my('orrhizal shorl roots can be detennined visually, and the
weights of these ~U\letures determined. Resul~ may bee~pressed as number and weight of
ectomycorrhizal Structures per unit area. Or per unit volume of soil.
(2) Host res ponse. The reaction of a seedling or tree to mycorrhiz:ll colonization
can be measured in \'arious w;'Iys. An ea~y. non-destruCtiw method is to follow seedling
survival. c~pr~ ssed as pI'('1;entages of the initial uninoculated and inoculated popu lations. Such data can be gathered at various ages. before and after outplanting. Other non destructive measures are plant height. thickness of stalk at ground level. number of leaves,
leaf length and I~af area. More definitive measurementS inyolve detennining th e dry
wei ght of the whole plant. or of separate root ~nd shool systems. Measurements of stem
height and Slcm diametcr at $Oil line are evenruaUy replaced by di ameler at breast height
(1.4 m) in older trees. A 'myeorrhiUlI influence value' (~lIV) can be detennined for any
p~ramet er by express ing the mean value for non-inoculated plants as 100, and calculating
the value for mycorrhizal plants as an integer relativc 10 thaI 100. Thus the MIV would be
a percentage of the control value in each case (usually gr~ater than 100%).
(3) l\Iine ral nu trition. Phosphorus up take. and levels achieved in the maml~ and in
the plant. have been ddennined using radiottactr techniques. and are among the most
imparlant reflections of the effccts of 1::1\1 funSi on their hom. Ectomycorrhilal plants
also absorb many other minerals. e.g. calcium, potassium. cop per. molybdenum. maa"'"
Ji~m and zinc. from the soil more efficiently than nonmycorrhizal plants can. The fungal
mantle can stQf'C inorganic nutrients. e.g. chloride, ammoniu m. and especially phosphate.
and release them to the plant durin g periods of deficienc y or activ,;: growth. Pisolillws
linc/orius Ihri"es in $Oils of extremely low fenility, such Bi mine spoils. while Pa.lillu$
U!vn/u1iU does well only on siles with relatively abundant 3"ailabie ni trogen. But since it
is in th e uptake of phosphorus. often n hmiting nu trient in poor soils. th~t EM fungi make
their gTe;'lle,t contribution to the symbiosis, e' aluation of nlte and amount of P (phosphorus) accumulation mu~t be onc of the most impoT1:!nt criteria in selection.
(4) Water rela ti ons. The fungus Cenoc{}/:cum gellpl:ilmn is especially tolcrant of
low water potential. which correlates well with ils propensity for forming cctomycorrhizas
in dry at'l:::!s. In fact. b<,)causc Ctn(H;'QCClllll grows bcs t at a water potential of I5 bar.;. it can
be difficult to establish in irrigated nur.;erics. where it may be replaced by 1'heJtphOfll
ItrreJtris.
(5) Te mpe ratu re_ Pilills cembra dcstinet1 for high-altitude nutplanting is inocul at~d with a cold- ad:!plCd strain of Suillils plorans . Oth~r fungi. especi~lIy Pisolir}llu
(iUcrOTius, havc ~en found to be :!dapted 10 high lemper.lIurcs. Cttt(H;'QCCI/IIl gl!ophilltlll
ap~ars to tolerate both c~ tremes relatively wel1.
(6) pH_ Pine secdlings wit h PiJo/irlws ti!lClo ri,,_~ eCtomycorrhi~ae survive and grow
belief on acid coa! mine spoils Ihan do non-mycorThil~1 seedlings _This fungus can
tolerate a pH range of 2.6-8.4. Ct!l(H;'(XCUIIl geQpllilllm fonn> m)'corrh iz:lS from pH 3.47.5. Olh~r eClomycorrhizal fungi im pro ve the growth of pines in al kaline soi l.
(7) Toxicit)'. E1>'! fungi have been shov.n to destroy h~at- fonncd phytOlOxins In the
soii. In ,iew of the selective absorption of vanous ions by mycorrhizal fungi, and th~ir
capa<:ity for stating ions in the mantle. they may be acti'e in ameliorati ng marginal soil
toxicities. There is stil! lillie published won: in this :Il'e;'l. but studies in progress on the
spoils derived from nidel mining at Sudbury. Ontario. indicate th:!t some Er>.! fungi can
tol erate fairly hi gh levels of heavy metals in th~ 5ubstrate. When soil around pecan tree~
was treated with a variety of flcmalicides and fungicides. an increase in mycorrhiza fOnT!:!lioll by Sc/erodenna bo"ilUl (SderodennatalesJ was obscf\ed. due perh:lps to a combillatiOh of to);i n tolerance and reduced competition.
(9) Disease resi stance. The presence of EM fungi on the TOOlS of trees gives them
some protection against the attad:s of several se rious root-pathogenic fungi. Bolems
bovinus helped to protect Picea abies from IitlerQb.asidion mmosum. Pjsolilh~ linC/orius
inc reased the survi val r:lte of Pinus taeda seedlings exposed 10 RhiZOClonia solani. Myeorrhizas fonned by SuillUJ 8r!ln/llat~ seemed 10 protect seedlings of Pinus exec/sa from
a rool-rolling Rhitocto'lia. SeedJlngs of Pinus ciarull were protected against PhylOplilhoro
cinnan10llli by mycorrhius of Pi$olirllUS lin,IQdrlS. The effects of the pathogen Mycelium
rudieis alrovir"ns on Pic"!l marilma and Pinr,s resil105a were marked ly reduced by the
presence of Sui/ius grallularru. This effect is not fully explained. but may be due (o
competition betwccn fUllg; for nutrients and for access to the root.
( 10) Mycelia l slr.tnd formatio n. These aggregations of parallel hyphae serve as
effective agents for the spread of tile fun gi through the soil. and in the long-di~tanct
transl ocation of phosphate and other nut rienLS to the mycorrhi zas. Different species. and
different isolates of the same species of EM fungus. may have diffe ring strand-fonning
tendenc ies. Other things be ing equal. it would seem reasonable to ehoose a s!rand-fcrming fungus, suc h as Pisalillius /inClari"s, over one thaI did not produce these sU\letures.
(I I ) Ease o f isolation. Pure cultures of ectomycorrhizal fungi are usually derived
from fruit body tissui:. though they can also be obtained from suri:tee-sterilized mycorrhizal rootS, scleroti a, rhizomorphs or mycelial strands. II is difli cult to germinate bl~id
iosporcs, and this is rarely attempted. Isol:llioll from fru it bodies allows prec ise identifi cation of thc fUngus:II the outset. Members of the following genera are oflen fairly easy to
isolate: Amanim. Bolews. Conina,ius. He~/oma. HYSlerongium. l.."ccaria, WCtllrillS,
LeCCinllln. Pa.ril/"$. Piso/ithIIS, Rhitnpogon, Sc1trodermo.. Suill!!s, and Trichofum,j. Happily, these include some of the bener mycorrhizal panncrs with the broadi:st host ranges.
But only a few species of Russula havc yet bee n cultured. r think most E:>-r funyi wiU
eventually bi: gro""n in axenic cu lture when their rather stringent n(nriti onal requirements have been worked out.
( 12) Large sca l~ inoc ul um p rod u ction. Since PisolilJlUs tinelorills has bei:n shown
toeslablish myCQrrhizas with almost 50 differenltree species, thrives over a wide rongl: of
soil pH. tolerati:s high temper:ltures well, and can establish myeorrhizas in the poorest
soils. it has been louted as II p~n<!cea for all our eetomyeorrhizal problems. II was also the
first EM fun!;us to be made available ill the fonn of eommerdaUy produced mycelial
inoculum. Nevenhelcss. it seems unlikely that Pisolitlms can be aU things In all EM trees.
II is probably al its besl coping wilh heat and drought stress. II ha) been collct:tcd only a
f;:w IIrn;:s in Canada. and I suspeCt that il will not tum out to be the perio:l:l part~r for
bori:a! conifers. Some recem work: suggests that when cnnif;:r seedlings with Pisolilhlls
myeorrhizas arc outplanted in nonhcrn QUi:bec. Pisolillius is soon replaced by indigenous sp.::cies. Attempts are being made to scale up production of mycelial inoculum of
CenO<:OCCllm geophilum, Rltiwpogon spp., Sui/lus spp.. Thdephora lerrestris and others.
(13) Edibility. If se\"eral potential panners seem more or Icss equivalent, the ultimate choice may be dictated by secondary, though not negli:ible. factors such as the
edibility or olhe,v.!ise of the fruit bodies of the fungi being considered. For e ~ample. if a
...:
t~hlY
toxic. and
hypothetical choice lay bc!ween a S(Je':ies of Amallira known
another agaric. suc h as BalerU!; tdulis. that was edible and choice, the decision would be
straightforward. U,SS obvious. bUI also important. is the caUli o~ that species known 10
have toxic fruit bodics should nOt be introduced to new areas as mycorrhizal partncrs.
even if they might seem ()(herwise desirable. One of the most toxic of all agarics, Amallira
phalloMes, was in ad vert ently introduced into Sou th America as a mycobiont of
oak seedlings imported from Europe early in this century. The cyc1opep!ide tOxins
(amatox ins) in this fungus have since caused many fatalities. The Australian govemmcll!
prevented a similar problem hy refusing 10 aUow the impottation of cultures or Amanita
plmrilerill(l. a good mycorrhizal partner. but producing basidiomliia containing dangerous levels of ibol:enic acid. At the other end of the scale are Ihe French experiments with
'trufficuhure'- the deli berate use of Tuber meianospornm as a mycorrhizal partner, with
an eye 10 thl: production of truHles. an extremely valuable crop. The flTSt steps loward the
culture of other choi ce edible fungi have been marie. again by the French. Using pure
cultures of the famous 'cep' (BoltlU!; tdulis) and three other boletes. as well as lAclarius
dtUcioSllS and Tricholomaj1avovjrem', ectomyconhizas have been established on Pinus
pinaslu and Pinus radillta in lest tubes and in greenhouse polS. It remains to be seen
whether outpianted seedlings bearing mycorrhizas of these species wiU ult imately produce tY.lsidiomata. thereby providing an interesting and perhaps valuable byproduct of
afforestation.
may be initiated by several different kinds of inoculum. (I) Naturally dis~rsed spores. (2) Col on ized soiL (3) Mycorrhilal seedlings. (4) Ascoma!a.
basidiomuta. spores or sclerotia specifically collected for the purpose. (5) Fungal mycelium prodLl~ed in axenic culture. It is worth comparing the merits of these di fferent kinds
of inoculum:
(\) Natural spore inoculum is, of COUl"5e, one of the prime disper:>al mechani sms for
fungi. but it can't always be relied on to infect nursery or OOlplanted seedl ings because:
(a) It is avail able only during a rel ati ve ly short season, sin ce most agarics fruit in late
summer or early fall. (b) Even when spores are being released. Ihey may not reach the
seedl in gs in adequate numbcl"5. espe ci ally if the seedlings arc a long way from the nearest
stand of eclomycorrhizal trecs_ (e) We have no C()I1trol O"cr the nature of the fungal
partners b<: ing introduced. This is important bec au se EM fungi vary widely in thcir effi
ciency. (d) If seedlings are being started at a low elevation nursery for high elevation
Outplanting, they may acquire local myeobionts unsuited to cond itions at the intended
growth sileo
(2) In Western Australia. pine seeds planted at 14 new nurscri ~s germinated and
grew relatively wcll for a few months. then begun to decl ine and die. The fcw remaining
h<!althy secdlings we~ found to have developed eclOmycorrhlza5. When soil from around
the hcalthy 5cedlings ..... as used to inoculate other seedbeds. the seedlings there rcco\'ercd.
Soil from b.:neath established eClomycorrhizal trees is a fairly reliable sou rce of inoculum
if 10% by "olumc is added to a new nursery bed. The mycobioms are often unknown, and
there is some risk of introducing pests or pathogens. but this has rarely caused difficu lty,
because Ih~ source location can be carefully checked in advance, Colonized soil has been
used to establish e~O{ic pines in muny parts of the soulhern hemisphere, and soil transfer
is a regular procedure in many developing countries.
(3) Introduced mycorrhizal secdlings curry the same risks as (2). but have also
"'orked relatively well. This te<;hnique was first used on a large scale in Indonesia. and is
!\'iYCORRillZAS 267
>tilluscd there. Mycorrhizal seedlings are planted in seedbeds at 1-2 m imervals. At
olltpianting time, some seedlings are left to inoculate the next crop.
(4) The deli~rate collection and introduction of spores, fruit bodies or sclerotia
would seem to be an obvious way of improving upon nature. bUI there arc some problems:
(a) Naturally occurring fruit bodies of most EM fungi are avai lable only during a small
part of the year. (b) In most cases the amount of inoculum available will be limi ted, and
will fluctuate from year to yeur. (e) Fruit bodies usually occur sporadically and scattered
over large areas, so collection in the arnoums needed for large-r.cale forestry applications
would be almost impossible. Only the paniculady concentrated spore-source represented
by gasteromycetes could be obtained in the necessary quantity. (d) Storage of the emi nently perishable basi diomata would be difficult. (e) Initiation of mycorrhizas by basidiospore inoculum takes 3-4 weeks longer than when mycelial inoculum is used. This
gives pathogens longer to anack the roots, and the later-developing mycorrhizas also
provide less growth stimu lation during the LTIlcial early stages of seedling development.
One wide spread mycobiont, Cenococcum geophilum, produces structures called
sclerotia that are much less perishable than either spores or basidiomata. since they
obvious ly evolved a, a long-term survival mechanism. These sclerotia often occur naturally in the soil in huge numbers, and could probably be harvested and used as inocu lum.
Over 450 kg of Pi.mlithus I;nctorius basidiomata were collected on coal mine spoils in
Alabama in 75 person-days . Since less than 1 mg of spores is needed to inoculate a plant,
this collection provi ded enough inoculum for hundreds of millions of pine seeds. The
basidiospores were used in a seed-pelletizing mix , each seed being coated with 500.000
to 5 million spor~s which became dispersed around and below the seed after planting as a
result of rain or irrigation. and colon ized the roots as these developt'd.
(5) If mycelial inoculum derived from pl.lre cultures of known mycobionts is used,
the identity of the fungus will be known. pests and pathogens will b~ absen1-, inoculum
will be compact and e~s ily transported. and should be available year-round . However, it
too has inherent problems, not th~ least of which is that it is by far the most expensive of
the alternatives: (a) Some ectom)'corrh izal fl.lngi are difficult to isolate in pure culture. (b)
Culmres are expensive to maintain, and grow slowly. taking a long time to produce
enough biomass for large-sea\<: applications. (c) We still do not know how well such
inoculum survives in the soil in face of predation and compet ition from indigcnom;
organisms. (d) We have nO! yet defined the best possible fungus -ho>t combinations for
many soilc1imate combinations. ft is hardly worth going to the expense of mass-producing mycelium of many specie, until we are sure that the resl.l lts will be economically
worthwhile. However. some E;"I fl.lngi, often those with relatively small basidiomata (e.g.
The/ephora, w(:caria). are early colonizers. associated with young trees , while others,
often with large fruit bodies (e.g. Eolems) are late colonizers, often associated with larger,
older trees. It would seem appropriate to concentrate on early colonizers.
It is easy to grow enough mycelial inoculum for smallscale research projects, bm
experience has shown that it is much more difficult to generate enough to inoculate the
many millions of seedlings prodl.lced each year. Various methods of producing mycelial
inocl.lll.llll of Piso/ilhlls liru:ror;us. Thelephora lerreslris and CenocoCClim geophilum
have been tried. It was found that peat-moss plus venniculite moistened with modified
Melin -Norkrans nutri ent (M;"L"<) ,olmion gave good results. The l't1.:\oIN solmio!l con tained: 0.05 g Cael,. 0.025 g NaCi. 0.5 g KH,PO" 0.25 g (N HJ,PO.. , 0.15 g MgS04 .7H,0.
1.2 mL I'ii; FeCl3. 100 g thiamine Hel, 3 g malt extract. 10 g glucose, and distilled water
to make lli tre. Using starter mycelium grown in liquid culll.lre and mixed throl.lghoUl tbe
Sl.lbstrate, The/ephoril terresrris and Pisolithus t;nC1orius will thorough ly colonize tbe
substrate in 1-2 months at room temperature. CenococCHmgeophilllm may take 45 months
(
ru
UFPECCB
eSI8L10TECA
to achieve the same result. The inocul um is leached in tapwater for 2-3 minutes. then dri~d
until its Waler tontenl is 20%-65%. Inoculum of Pisolilhus linClOrius ean be slored at :S'C
for nine weeks wilbout mueh loss of activity. but the sooner it is used. the bener. A
tommercial fonnulation of Pisolil/lllS linc/orillS mycelial inoculum has been developed,
grown on a large scale in the vermiculite-peatmoss-MMN medium. Unfortunate ly, quality-control problems (read: contamination and low myeOlThiza-fomting efficiency) caused
this product to be withdrawn from the m:u-ket in 1983. It is now being produced in
'breathable plastic b~gs by another company.
Several methods of application have been tried: (A) RroadcaJit inoculation: a known
quantity of inoculum is spread out over a given area of seedbed. and mi:-;ed into the top
10-20 em of soil before lIle bed is seeded. Inoculum of Pi!OlilhlL~ linctorills. broadeast at
a rale of I litre/square metre. gave the same results as those obtained with higher levels of
inoculum. Inoculum incorporated in container growth media at a rate of 6% by volume
produced effective ntycorrhization in many conifers. Here. inoculation and ,ontainer
filling processes can be combined. Pin us laedu nursery beds have been successfully
inoculated with cultures of Pisoii/hus tinctmius. Laboratory grown inoculum was leached
under ronning tapwater, cool-dried to about 2Q% moisture. and kept cold. but not frozen.
until used. Nun;ery beds previously fumigated with methyl bromide-chlorpicrin weu
inoculated with the dried preparation, wh ich was dug into the top 7- 10 em of soil. before
seeding. (B) Banding of inoculum below Sf!eds: this concentrates inoculum in a lone lIlat
will be penetrated by the growing roots. Seeds and inoculum ean be dispensed at the same
time. This method needs only about a third as much inoculum as the broadcast techniqu~.
(C) Sl urry Inoculum: this has the ad vantage that bare-foot or containerized seedlings can
be r.lpidIy inoculated by dipping before tronsplanting.
The production and field application of myceli~l inoculum of EM fun gi is still in its
e:-;pensive. and at times unreliable. infancy. Yet many foresters believe that the inocula
tion of both bare-root and eontniner-grown seedlings ""itll appropriate EM fungi "ill
eventually become routi",: practice. It is worth noting. however. Ihnt in many pans of the
world it is not afforestation. but refores tation that is important. In th is case. the soil of the
site to be rcplnnted will often contain good mycorrhizal fung i. It may be possible to ghe
Fig. 17.3 Fnety branched arbo.,5CUe of an encIomycOffhizal fllrlb'tlS inside J root eel of the
phy lObiol1!.
l\{YCORRHIZAS 269
th.:se indigenous fungi a competitive adv antage by discouraging othcr compon~nts of
the local myeota with selective fungicides such as Benomy\. which inhibits ascomycetes
and their anamorphs without significantly affecting the basidiomycetes.
The almost omnipresent endotrophic mycorrhiza, often known a~ the vcsiC"idararbuscular mycorrhiza or VAM (though not all fungi of this group produce vesicles), is
"it more subtle phenom~non than the ectotrophic mycorrhiza. The presence of a VAM
fungus in a root is usually undetectable by' the naked eye. There is no obvious morphological change, no mycelial mantle. no sudden flush of large fungal fruit bodies. Yet, as
appropri ate clearing and staining will show, roots arc often extensively colonized (Fig.
17.1 A). Thc life cycle of a vesicular-arbuscular mycorrhizal fungus goes more or less as
follows: spores in the soil genninate, usu ally in conditions appropriate for plant seed
germination and root growth. [f the fungus encounters a receptive root Of root hair, an
appressorium is fonned, and penetration occurs (often through 'short cells' of the exod<:rmis, if these are present, because they are nO! yet suberized), in the elongation zone of the
root. Symbiosis is initiated in juvenile tissues.
Hyph ae grow in or between the cortical cells. bl!! never enter menstematic ceUs or
endodennal cells. Specialized hyphal branches enter individual cortical cells and form
finely branched, tree -like structures called arousculcs (Fig. 17.1 A. 17.3). which are completely en caps ulated by the host plasmalemma. and are the main sites of e xchange between the fungus and the plant. The nucleus of the root cell is enlarged. and th e volume of
cytophsm increases. We assume that phosphorus is being actively transferred 10 the plant
throughout the life of each arbuscule. Polyphosphate granules. involved in P transport in
the fungus. are present in hyphae. but not in the finest br,mches of the arbusculcs, which
contain acid and alkalinc phosphatases. After 4 -1 5 days. the arbuscule gradually breaks
down, and the root cell returns to normal.
Many, though not all. vesiculur-arbuscular mycorrhizal (VAM) fungi also form
"csiclcs in thc rool. Thcse arc thin-wallcd. inflated structures without a basal septum, and
are often full of lipids. r have seen up to 500 vesicles/em in older leek roots, the root cortex
looking like an almost solid mass of vesicles. Despite th is. the root remains functional.
since th e stek is not colonized. and can still translocate substances to and from the active
root lips. Vesicles are not fomled by one actively endomycorrhizal genus. GigasfJom .
While the fungus is developing its intrnmntrical phase within the roOI. it is also
developing an cxtrnrnatrienJ hyphal n~twork in the soil. Extr.tmatncal hyphae extend at
least 8 cm from the root. This means that a mycorrhizal plant can exploit ~ev<! raltime5 the
volume of soil available to a non-mycorrh izal plant. The extramatrical hyphae obtain
phosphorus and translocate it to the plant. which reciprocates by supplying the fungus
with photosynthates. Thes<! enable the latter to extend its hyphal network, and to produce
its large. asexual spores. Spores may form in the soil singly, or in aggregations up to 2 em
in <Jiameter called sporoearps. Individual spores ore large: 50-600 ~ in diam~ter. They
may have walls up to 30).lm thick. are oft~n darkly pigmented, and are filled with storage
lipids. all fealmes that emphasize their role in long-term survival whcn host plants are
ab ,ent or donnant. Vesicles are sometime> reg~rded as 'intram~trical spores: The spores
will evenlll~lly genninate. producing hyphae which will once more grow through the soil
and perhaps encounter ~nother plant. The idcntity of lhe plant may not matter much. since
VAM fung i can usuolly rdate successfully to a very large number of host species (!30
fungal taxa with 300.000 plant taxa).
The spores of Aeaulo$pora species (Fig. 17.4) fonn on the side of thinwalled.
terrninll s,",cllings thaI latcr collapse and vanish. or leave only an inconspicuous rem
Entrophosp"'"
,-
I,
..
~;>p"
~.
V ~ '
.,.
hyphae have been shown to retrieve sol uble and insoluble phosphorus 21 mm from a root-phospttorus that was complelely unavailable 10 non-mycorrhizal
roots at similar distances. The zone of depletion around mycorrhizal roots can be twice
that around non-myeorrliizal rootS. But even the most efficient VAM fungus will have
little or no effect on a plant if available phosphorus is present at lUXUry levels. A relativ<:
myeorrhiza dependency factor can be calculated from the following fonnula:
1(0 )(
to be calculated for any given level of P availabil ity. For exa mp le, at 100 ).1gfg available
p. Ihe relathe mycorrhiza dependency of Can'Ot is 99.2%. and that of wheat is 0%. This
calculatio n also lets us compare the responses of any species of plant to different sources
of P. and to different mycorrliizal fungi.
As yet we don! know much aboullhe contributions to plant growth made by
indigenous VAM fungi in field soils (although we extrapolate from the results of laboratory e.' perimenls). This is partly because any treatment that will kill all spore.~ in the soil.
and aUow comparhons to be made. is sufficie ntly drastic that it wi!! also change the
chemical makeup of the soil, and prooobly alter its nutrient status.
,_ ..-
--
'11"""1
?7f: ,.....
todes, ond 3 viruses, invoh'ing a total of 21 different crop plonts, Most experiments
showed that mycorrhizal plants had less disease, though virus symptoms were more sc
vere, Various explanations have been put forward to explain the reductions in fungal
disease. (1) The mycorrhizal plants were healthier and more able 10 resist the attacks of the
pathogenic fungi. (2) The cells of mycorrhizal plants may panly digest the senescem
arbuscules of the fungus. The same chilinolytie enzymes might be used on other in~'ading
fungi. (3) Possible infection sites on the su rface of the plant roolS may be pref~rcmially
occupied by the mycorrhizal fungus. to which Ihe plam may weB be more susceptible.
Prosp ects
It has been said that 'Most woody plan ts requ ire mycorrhizas to survive. and most
herb~ceous plants need them to thrive: 50 it seems only logical that both VA.\I and EM
fungi must be of \ ital ~on~ern to H()nJO sapiens. a suppo.'\Cdly iluelligent species that
knows it is totall)' dependent on ploms. Tragically. the endolOycorrhizal rainforests are
rapidly being destroyed by logging, agricuhure. mining. road.building. urbanilltion and
other hum an a~ti\'ilics. Smc<: these forests do nOt regenerale e ~sily or qUIckly. they will
oft~n be replaced by plantations of fast-growing e:l:otic e c tomy~ol'Thilll conifers. Coni
f!:rs are also being C'slablished on many treeless nreas. E:o;isling forests need to be rcpl.lnted after har...csting. It lookS to me as though any research and biotechnological
in\c,tments society m~kes in cctomycorrhizal fungi will be wcn repaid by the ease ami
speed with wh ic h t h~ trees become established, Dnd by the acce lerated grov. th of the
maturing forests. Tree nurseries and field crops are often heavily fertilized. This eff~c
li'dy discourages nlany mycorrhizal fungi. which are highly adapted to infenile soils.
Comm~n;illl mycorrhi7.a1 inoculum may evcntually wean forest nurserymen and farmers
away from chemical fet1ili~e rs: increasing energy co.tS may provide the required impetus.
i\lYCORRHIZAS 177
Orchid Mycorrhizas
Orchids produce astronomical numbers of seeds, which are so tiny that they can
carl)' little or no food. For the first two to eleven year':> of their lives - until their first
chlorophyll-bearing leaf develops - these plants depend on being colonized by fungi.
commonly basidiomycetous anamorphs of the genus RhizoC/onia (whose holomorphs ar~
crust fungi belonging to genera such as Thalllllep/wnls, Conicillm and Cerarobtlsidium
[AphyllophoraJesJ). Sin ee these fungi are active saprobes in Ihe soi l. they arc in a position
to provide th e orchid scedlings with nutrients. The fungus enters cells of the root cortex
and, develops coils or peiotons, which eventually swell, degenerate and are absorbed by
the plant cell.
If we observe the gennin Jtion of many orchid seeds, it becomes clear that there are
three common outcome:;: (I) the seed becomes colonized by an appropriate fungus'and
thrhes; (2) the fungal infection takes over, and kills the seedling; (3) the fungal invasion
fails, the fungus is eliminated, and the seedling stops growing, Thi, dues not appear to be
a mutualistic symbiosis, but rather a delicate balancing act on the part uf buth p~rtne rs,
perhaps still in the process of evolving,
GentianaceQus Mycorrhizas
These look rather lik.e orchid mycorrhi1as. producing coils inside cortical root
cells. However, in this case the planl~ do havc chlorophyll and can provide nutriefi!s to
the fungus. If pots containing G~ntianacea~ arc inocu lated with roots of plants
endomycorrhizal wit h Gfomll.l or Gigaspora , the roots become infected and coil,; are
produ ced in cortical cells. So the gentianaceou:; root cdl environmcfi! scems to induce a
morphologicJ I vari ~nt of normal endomycorrhizas.
Ericoid Mycorrhizas
These look intermediate between ecto- and endo-mycorrh izas, and for that reason
o>e r] to be called ectendornycorrhizas.' In Arh"I".\" me,, ~i~:,ii, a beautiful ericaceDus tree
that grows on the \I'est coast of North America, the short roots have a sheathing fungal
mantle Lbe lD\v] and branch in a characteristic way, but instead of prududng a HJrlig Net
bct\l,'~en the hDst cells, the fungus ~ctually penetrates thc cortical cells and fills them wi th
den,cly coiled hyphae (not arbuscules). In roDlS of the ericaceous Arctostaphylos. the
mantle is less obvious, but the fungal coil> cle.u-Iy fill the cortic~l cd!>.
You may have (he impression Iha t ~ll these kinds of mycorrhiza are quite distinct
phenomena, Yet it has been demonstrated that a number offungi: ASIr(ielis hygromerriclls
(an earthstur), Tricholomaj/(ll'ovirells, SlIillllS albidipes , SlIilliiS IOmenIOSIIS . wcwri",~
paradox!!" (all Agaricales) and Colrrici(i pf'rf'""is (Aphyllophorales) can all form norn}ai
ectom),cDrrhizas with PillllS bll"hiana (Pinac~ae), and ericoid mycorrhiz3s with ArcfOswphylos IH'u -IIrsi (Ericaceae). This opens a whDle ncw area of study.
~ UFPECCB
~BIB L!OTECA
18
Introduction
Throughout the English-speaking world , fungi are viewed with suspicion, Toadstools, perhaps because of their slidden appearance. strange shapes, bizarre co lours, and
reputedly poisonolls nature, became associated in folklore with fairies, witehe's, or even
the devil. These superstitions probably saved many lives oyer the centuries. People in
forested areas of Central and Eastern Europe apparently directed their superslitiol.ls awe
elsewhere (see Grimm's fairy Tales .. ,), and did not hesitate to eat mushrooms whenever
they appeared _ Information do:rived from these experiments gradually accumulated and
was passcd on, first in the oral tradition, later in books. A few agarics gained a reputation
for killing those who ate them. These are dealt with in chapter 22. At the other end of the
scale. a relatively small number of fungi eventually e[]tered the culinary hall offame: they
are the chief subj~ts of this chapter.
" ... Ravioli filled with fresh black truflles and celery in melted butter and parmesan
cheese ... sweetbreads with a soya sauce, cloud ears andjulienne of many vegetables ... lamb
with Iddlley stuffing and potato ere~ stuffed with spinach and mushrooms ... warm sweetbread salad with girolles (chanterelles). oysters and leeks in truffle sauce ... tiny veal
kidneys with chanterelle mushrooms ... eloud-like mousse of rattened livcrs of Bresse
chickens with truffles raining over it:' These quotations are taken from a serics of anides
written by th e restaunmt critic ofthc Toron/o Globe and Mail.loanne Kates. after a grund
gourmet tour of Fwnce. The common denominator in this outpouring of haute cuisine:
fungi as ingredjents contributing flavour and texture.
Can we: make any generalizations about the edibility of large fungi? let's try a few.
(I) Of about 10.000 s~eies of fleshy fungi. only a handful are lethal-deadly poisonous.
(2) Unfortunately, some: of that handful are relatively common. (3) Represe:ntutives of
only about 20 genera are regarded as prime edible fungi: check the list below. (4) There
are nosimple ways of distinguishing between the edible and the poisonous: all folkloric
tests such as. 'If the cap peels, it"s edible,' and 'Ifit doesn't blacken a silver spoon. it's OK:
are misleading and d~ngeroos fictions. (5) You should eat a mushroom only if JOu know
its name with considerable precision (and b) that, I mean its scientific name, its La tin
binomial, a unique pair of epithets which specify its genus and species). Don't assume
that all is well if it looks like: a picture in a book. or even if you can identify it to ge:nus:
gencra which contain prized edible: sp<;:cies may also have disagreeable or dangerous
members-this is true of both Amaniw and AgariCHS. (6) In order to discover th~ proper
nome , you will probably have to refer to an expen: every handbook ever pub lished is
279
and fallible. and you wi!! ofte:n nc:c:d to examine microscopic fea,ure.~ (such as
basidiospor~s). (7) Do nOt accept the word of selrstyled 'exp.!'rts' without checking their
credemial>: after all, i!'s your life. oot theirs. (8) The flnt rew times you eat a mushroom
that is new to you. don't eat much of it, because some people develop severe allergic
reactions. ("-en to species generdlly considered safe. (9) Son your collections very care
fully: don't mix species. and never eat old or shrivelled ~pec:imens. ( I O) If you arc st ill
determined to become a rnycophagisl. buy One or more of the wellillustrated manuals
listed atth .... end of this chapter(the lincoff, Phillips and Arora books are the mostcompre
hensivc). and join ),our local natural history or mushroom society. If )'01,1 become fasci
D3tcd hy Ih<' strunge and mysterious world of the fungi. theo you will be ready to join
~AMA-thr North Ameriean Mycological A.ssociation-and perhaps subscribe to Mush
room maguine. Good hunting.
Now for a quick tour of th;: betterknown edible mushrooms. I will begin with those
that h~\'<,. !~ntativc:ly or commercially, ~en brought into cultiyatioll, then move on to
those which are available only in nature. Mushroom cultivation may have an edremc:ly
bright fUtUT? _Consider the following: U we: use a hectare of I~nd to produce beef, the yield
of protein i~ about 80 kglha. If I':e use the: same area for nshfarrning. the yield m~y be as
much as 660 kg/ha . But if we grow mushrooms. the protein yield is commonly 80.000 kg!
ha: ~nd fungi have the added ad\'anl~ge thaI they bioconvert cellulosic debris such as
maw. sa\,-dmt ~nd animal manure. which are prodllced in large quantiti es as essentially
.... onh ie,s byprooucts of other i ndU5tries.
(I ) Agaricus brllllll(S"CI1$ Qr A. bispOfll.f (depend ing 011 whether you foUow IIblloch
or Singe r) fHolobasidiomycetes, Agaricaks. Agaricaceae}. The mushroom of the western
world: to many people. all other agarics are: ',oadstools: to be avoided. Sauteed in bUl{cr.
the s upermarke t m ushroom is an excellent accompaniment to steaks; dipped in bauer
~nd decp fri<'d. it makes a truly gre:a.>y but taSty snack at m~ny country pubs.
Thi < is the one edible mushroom that every Weste rner knows ~houl. [t was domesli
c~:cd in the ;;eventeenth century by the French. and has spawned a considerable industry
in Nonh Amcric~ (sorry about that pLIn. it was quite unint~ntio lla1) _ Annual worl d produc
tion ol'thi, sp~ cies is ~sti mated to b<' about 1,0000.OOO tonnes . and growi llg, As an interest
Ing f')Otnol~ 10 the end of the Cold War, the nuclear missile silos at Csasar in Hung~r)' are
no\\ ocing u,<,d to grow mushrooms. The crop is e);poned toGenn~ny, the ver)' country a!
\\hi~h the missiles were fonnerl), aimed. Can~di~n consumption of A. bnml1t'scens in
erea~d se'-rnfold betWei!:1l 1963 and 1983. Before I move on to the many oth~r edible
fungi . I mu,t insert 11 warning. Mushroo ms should nOl b<' eaten raw. be-couse they cont~ill
sig n ificnnl amounts (0.6 ppm) of th carcinogenic 4(h>'druxymethyl)benzenediazonium
ion. Fonun~\d y. !hi~ un,table iOll is destroyed by cooking.
(2) P!eurorus OSlrtmllJ (Holobas idiomycctcs. Ag~ric~les , TricholOtnmllce~e). the
(l~s ter mushroom . is another good find_ It forms overlapping clusters of large. non$lipi tate oo.,idiomat", on dead or dying trees. In fact. no fewer than seven species of
P/c'IIf!)tli.l b'-e been domestic:l1ed ~nd m~rl:eted. notably Plel/rotlis sajor'wju with P.
OSlr((ltus ;): !!ist~nt second. but some: growers ran intO an unexpected snag: the b~sid
io~porcs arc ~);tremely allergenic. ~Ild cause scl'ere reactions in many of the ,,"orkers _
\\'orld production is more than 20JXJO tonn~s/>c~ r.
winter or velyet stem mushroom, long cultivated in Japan, where it is calkd enokimke.
is now grown on a sawdust-bran mixture in North America. It is too early to say whether it
will catch on hert:. but it suits ourdimate. since it will grow and fruit at low temperatures.
Thc cultivated fonn hus little re~emblance to the natural fruit bodies, since it consists of
long, narrow stipe, with tiny caps at the top. World production is about 40,000 tonOfSl
year.
(6) Pholio/a nameko (Holobasidiomycetes, Agaricaies, Strophariaceae) is anoth~r
1ignicoiOllS mushroom that has been domesticated in Japan, where it is called nameko.
and about 1?,000 tonnes a year are produccd.
(7) Auricularia polytricha (Phragmobasidiomycetes. Auriculariaies), the tree ear
or cloud ear or mu-cr of Chinese cuisine, is ajeUy fungus that grows on d~ad trees (cf. Fig.
5.8 B). Its car-Iike basidiomata are a(]ded to a variety of Chinc,e dishes: mostly, I suspect,
for their slippery, crunchy texture. It has recently been sugge st~d that something in these
fungi re(]uces the clotting wndencics of human blood, and may help 10 explain the low
rat~ of heart disease among the Ch inese. About g,OOO tonnes a year are consumed.
(8) Tuba meianosporum (Ascomycetes, Pezizaies, Tuberaceae). the black, queen.
or Perigord trume (Fig 4.10 G). This is what the French call the (]iamond of the kitchcn.
They also say: 'Ta femme, tes truffes et ton jardin, garde-les bien de ton ,oisin.' (Your wife,
your truffles and your garden: guard them weI! from your neighbour). This old French
saying will give you som~ idea of th~ high esteem in which trome, are held. Moliere. who
wrote much beuer stuff than that, was obvious ly fascinated by truffles. since he ga ve the
old French namc for a truffle, 'Tartuffe,' to the main character in his comedy of the same
name, an(] named his estate 'Perigord: after an urea famous for its bl~ck truffles.
/l.Iy introducrory quotations from Joanne Kates gastronomic tour show how hcavily
the best French cuisine lean, on the subtle aroma em anating from trumes. Iwli,m chefs
place an equal premium on the cxtremely odoriferous white or Piedmont trume (Tuber
magml/urn) that grows in northern Italy-Alb~ hulds a great yearly truffl~ festival in its
honour. which I hope some day to auend. In Decemh..:r of 1984 r visited the tiny mountain
village of Scheggino in Umbria, another centre of truffle collecting. where both black and
whit~ truffles grow. As a gu est of the Urbani fami ly. who appear to have cornered mu ch of
I
FUNG I AS FOO D: l\!YCOPHAGY 285
called lh u-Su ... or 'bamboo sprouts: It is now cuhured on II small scalc on a medium
composed of sawdust, bagasse (sugar-cane debris) and bamboo. The dried product. which
is reponed \0 have II ' pleasant sweetish smell,' sells for USS400-I.OOOIkg in Hong Kong .
Because of its rarity it is served as a delicacy at Slate banquets, but it is widely sought
because" _.. according to Chinese medicals. il not only cur"s high blood pressure, but also
reduces cholesterol content of the blood. and through long lise, it eff~ti\'ely reduces the
belly fat."
( 1 I) Tremella fucifQnnis (Phragmobas idiomycetes, Tremdla[es). a jelly fungus, is
widely cLiltured on wood blocks and in bags of sawdust in China. where it is caUed 'silver
ear' or yl n-er and is used in soups and as a tonic. I saw great mounds ofthc spherical, frilly
colonies for sale in the fascinating market at Guang-zhou (Canton),
(12) Ustilngo t!scu/enla (Tcliomyeetes. Ust ilaginales). a smut fungus, is inoc;ulnled
into wild rice, Zizania caduciflora, in China, It eauses the stem to become very thick and
fleshy. and at maturity produces small poc kets of tdiospores scattered throughout this
tissue. During my visit to China, I enjoyed the fungus-riddled. hypentOphied stem many
limes as a vegetable. For the Chinese it has the added advantage that it is supposed to
have curative powers against feve~. conjunctivitis and kidney and bladder problems.
Although 'mushrooms' of 32 species in 16 genera are currently being cultivated
commercially, only four or five ate grown on a large scale. Many of them satisfy our
demand for recycling and re- use, becausc they can be grown on various kinds of plant
debris, a plentifUl reSOUJce. Agaricus lind V()/variel/" are grown on straw or sim ilar subStrates: by-products of agriculture. Leminuia, Flammu/ina, PlIO/iota, Auricularia and
Gal!(H/tmna (this last is called Reis hl in Japan, and Ling Chi in China, where it is used for
medicinal purposes rather than being eaten) are grown on wood, sawdust or ""cod-chips:
by- products of forestry_ For those of you wbo would like to grow ntushrooms in your
bastnlent or garden. there is now an ellcellent handbook called Thtc Mushroom Cilltil(l/OT.
This gives delailed inslructions on all aspects of home mushroom cultu~, and deals with
many species, incl uding several which are hallucinogenic. Those specifically intc~sted
in cultivating Lenrinu/n tcdodts should consult the Shiirulu! G ro ..trs f/and/xJQk.
Now we move on to species that have never been commercially cultivated. TheS-
includ<.< some of the best of all edibl~ fungi. so there is still room for research and lots of
entr~pre n~llrial spirit in bringing some of them to an eager pu blic.
(13) Bolcl".~ edu/iJ (Ho!obasidi omy~etes, Agaricales. Bo!e laceae) is the cek bruted
cep of Fr~nce , the Steinl)i\): of~nnany, the porcini of Italy. Their IMge, plump basidiomata
bear rleshy tubes rather than gills (Fig. 5.5 0). They are the basis for some European dried
'mushroom' soups, and arc also imponed in see-through plastic packages. Th<.< aroma
emanating from an unopened packet. even after it ha s been sitting in a cupboard for
momhs oreven years. is unbelievably appetizing. Most members of the family Boletaceae
are edible, though species with reddish or orange Port' mouths, and those wh~ flesh
turns blue whcn bruised. should be avoided, Bole/us edulis is mycorrhizal with conifers in
weStern North America, where it fru its from June to November. I collected it in June 1984
ncar the edges of melting snowbanks near Bend, Oregon, and in Nov~mber 1990 along
the southern coos t of Oregon. I have also found it in the east. though it is kss common
then:. Alxlut 25 varieties of this species have been described. The impor1ullce of the
boleles to European mushroom hunters ca n be gauged by the fact lh~t of about 850 ton lIes
o f mushrooms a y<.<ar offered in the r. . lunich market at the tum of the century, over 500
tonnes were accounted for by Bolews crill/is and another bolete. Ltccimllli Jcahrum.
These mushrooms are the tilling for Crepe~ ~ la Bordelais.e: The tubes arc removed, the
ClIpS are cut into slices I ern thick. seasoned with sal t and pepper, and brov.-ned in olive uil
or butter for 5 min utes. Then they arc cooked for 2 minutes in egg yolks beaten with sour
UFPECCB
O SIBLIOTECA
'1/
288 C HAPTER EIGHTEEN
dens by the termitc~. which supply them with chewed_up wood, and ri gorously c.~dudc
()Ilier fungi (5 chapler 16 for the full Story).
(24) Charles Darwin. circumnavigating South America in the ~B eagle." noted Ihat
the go lf-ball-like, compound ascomala of wh:l\ was subsequently n:lllled Cyll(lria darwinii
(Ascomycetes. Cynariales) parasitic on southern beech. NOIlwfagwr, were an imponanl
pan oflhe diet ofthc natives of Tierra del Fuego. The Araucans of Chile take advantage of
the fact thaI Cyllaria contains up to 15% of fermentable sugars. and has on its surface the
yeast Sacc/ulromyus, to prepare an alcoholic beverage from ripe ascomata.
Various amateur rnycophagisls of my acquaintance have told me Ihnt they really
enjoy one or mOTe of the following members of the Aphy!1ophorales (where I have tried
them myself, [ add my own evaluation): (25) 'hen--()fthc-woods,' Grifola jmndQSG
(Polyporaccae): (26) 'umbrella polypore,' Polyporus umbel/orus ( Polypora~eae) : (27)
'~hicken musllroom' or 'sulphur shelf,' Laeliporu.s sulph"reus (Polyporaceat) jexcellent,
Fig, 18.] Man hoIdirlg one of the 'M')rld's largest edllIe flngi, l,angf'fmannid giganlea.
A warning
In eastern Europe, other hazards accompany mycophagy_Since the Chemobyl disaster, wild mushrooms in Poland and Russia contain le"ds of radioactive Cesium many
tim~s higher than those found in other food SOU l"\;es. and radio stations frequ~ntly warn
people not 10 eat 100 many. Bu t it is only fair to point ou t that, wherever they grow, wild
mllshroom~ tend to accumulate Cadmium and other toxic elements. By means of the Ames
test for mutagenicity, it has also ~en established that some 'edib!o::' mushrooms. including AgariCl4$ brullll~scens, shiitrlJ.:e (ullIimda ~dode$) and Boff!1l1s eduJis comain basepair substitution mutagens, and B. edu/is al;;o contains frameshift mutagens, Whik the
mutagen ic activity of L ~dod~j was nO{ reduced by boiling for 20 minutes, that of A.
bnJnnen;ens tlnd B. edllUs dcclin~d. but onl y by 50 %. Since the mutagens have not yet
been isolated and characterized. \I,e dOll't know their implications fQf'human health. They
mayor may not tum out to be siSnificantly cardnogenic _So wh ile eating mushrooms as
an occasional treat may be {inc, they shollld n~"er be rcgarded as a dietary staple.
hyperuricaemia (elevated levels of uric acid in the blood) will result. possibly leading 10
kidney stones and gout. Second. yeast proteins are nutritionally inferior because they are
low in the amino acids, methionine snd tryptophan. For yeast protein to be suitable as
food . it mUSt be separated from the indige stible chitinous wall material, must nOI be
denatured, must have its nucleic acid level reduced, and should be supplemented with
methionine. Apparently, if yeast cells an: disrupted at p H 8.5 in the presence of succinic
anhydride. 90% of the protein can be extracted without denaturation. If the pH is then
lowered to 4.2-4.5, the protein is precipitated, leaving masl of the nuc leic acid {mainly
R.t"<A} in the supernatant fluid. The development of processes like this may bring acceptance of yeast SCP closer. Of course, no one could be ellpected to cal yeast protein as it
comes: it would presumably be used (as the still cheaper soy protein is used) to supplement the protein concentration of otller, tastier foods. Yeastburgers, anyone?
Animal Mycophagy
I am sure none of you imagines that human beings are the only animals to appreciate the dietary value offungL One of the more dangerous myths used to establish edibil ity
of mushrooms assens that if they have ~n nibbled by larvae, slugs, snails or squirrels.
they must be edible. In fact, many animals, both venebrates and invenebrates, seem to be
unaffected by the tOll ins found in agarics poisonous to us (this is especially true of some
DroJOphiw species, as you wilileam in ch apter22). Elapllomyces, the deertruftle or hart'S
truffle, is apparently eagerly sought and relished by the animals for which it is named. In
the forests of California the red -bac ked vole. Clclhrioilomys califortlicu;. lives almost
e:o::clusivcly on truffies (Tuber spp.) and false truffles (e.g. Rhiwpogon): and many other
small rodents feed on, and di sperse, these hypogeous fungi. Wildlife biologists were
surpris~d to lind remains of flying squirrels, which live high in trees, in the faeces of
bobcal~ and coyOtes. Then mycologists spoued truffle ascaspores and false truffle basidiospores in the gutS of the flying squilTels: apparently the squilTels had been fatally lured
onto the ground. away from the safety of the treeS, by the odour of ripe truffles. Bi r<Js
migrating across the deserts of Kuwait. including nine! spec ies of lark, find and eat desert
truffles of the genus Plwcangium.
Flies of the genus Htdamyza are also IUned in to truffl es. since their larvae will eat
nothing else. It is sometimes possible to find truffles by the swanm of egg-laden flies
hovering over Iheir hiding places. Many other insects arc also e;>:;tremcly fon<J of mushrooms. as uny collector of wctarius dtlicio:,u;' or boletes knows. Adult Myeetophilid<lc
(fungus gnats) and members of many other groups (including some species o f Drosophila )
see k out fungal fructifications unerringly. so that their larval instars can fatten on the
proper diet. Aphids, nematodes and amoelfae have been found selecti\'e!y feeding on the
mycorrhilal fungi growing around conifer root.s. Some Amphipods (freshwater crustaceans) graze preferentially on the conidiophores of amphibious hyphomyceles-fungi
which colonize leaves that fall in to stre~ ms (see chapter II ). Collem bola (springtails) and
oribalid mit es (Acarina) have :llso been found to prefer a diet o f fungal spores and mycelium.
Perhaps the masl interesting e;>:;ampks of animal mycophagy are found among
groups of insects thai cann()( themselves digest cellulose or lign in. but still man~ge to
e;>:;ploil Ihese substrates through Ihe medi~tion of spedfie fungi. The insects either carry
the fungi around from tree to tree (Ambrosi a beetles). or actu~lly culti vate them in speci:!1
subterranean gardens (the Attine ants of central and sou th America. and the mound-build_
ing tennites of Africa and Asia), These special relationships are discussed in ch;Jpter 16,
C'
UFi'E.CCil'
Further Reading
Arora. D. (1986) Mushrooms Demystifled. 2nd Edn. Ten Speed Pr~ss. Berkeley (one of
the most comprehensive field guides yet published; everyone should have it, bUI it
does focus on Western tax a].
Chang. S.T. and \VA. Hayes (1978) The RiololtY a nd Culri,'ut io ll orEdibl e Mushrooms.
Academic Press. New York.
Ingraua. F.l. and TJ . 810m (1980) Commerd al i\Iushroom Growing. M inistry of Agriculture and Food. O ntario. Publ. 350 .
Lincoff. G.H . ( 198 1) The Audubon Societ)" Field Guide to North American J\.I ushrooms .
Knopf, New York lrelati\"ely inCApensi\"e; lOts of good colour photographs; 0111' of
the more comprehensive guides for Ihose io east~ m North America].
19
'A loaf of bread, a jug of wine, and thou.' Dmar Khayyam had it right Even if the
right "thou' happens to be away, good bread and wine offer some consolation. Eating
fungi in recogniublc form can be fun (or occasionally fatal). as you may read in chapters
18 and 22. but even those who make a poim of avoi!ling such gastronomic adventures eat
fungi (or fungul byproducts) without even being aware of it. The reason for Ihis is tlHl! a
numbe r of the basi c items in our diet, as well as some of the most interesting tidbits. are
'processed' by fungi . No one seem.~ the slightest bit inl<,reslcd in the presence of the
fungus itself. only in t~ changes it produces in the substrate. And what dramatic changes
they are. Without fungi. French bread would be maUoh. Blue cheeses would be blah.
T he wondcrfulte;.:ture of bn-ad is created by the ycasl. Sacc1rammyces cereviriat,
which fc rm~nts small amountS of su gars and liberates bubbl.:s of carbon dio:o:id~ that
becom e trapped in the dough and leaven it. Bread wi thout yeaSI would be like a day
withom sunshine. or steak without wine, or watching a football match without beer.
Whatever your tipple, its alcoholic wmponenl is ultimately deri"ed from Ih~ act ivities of
yeasts. agoill of the genus S(Jccharom)'c~, which ferment the sugar io grapes or malted
barley. :md liberate alcohol and carbondioxidc . The substrate and end products bal anc~
as follow s:
COH tZ 0 6
--l>
2C 1 H,OH +2CO!
though the process is actuall y ~ery compl ex, involving 22 enzymes, utlea~t 6 coeTlz), mes.
and :\Ig and K ion~. Bottled beer, crackling wincs, and champagne all owe their fi 7,Z as
"d! as thcir kick to yeast. So how come bread doeso't ha~e any alcohol? Perhaps fonunately. it evaporates dunng the baking process, so we aren't all 00 tile ro~d to alcoholism
wi tll Ull( first JX'onut butter s ~ndwich (though we could be on our way to a different kind
of mlfJxk~tion. a, you cun read in chapter 2 1 on mycQ(oxins) ,
The manuf~clure of heer begins with Ihe malting ofbnrle)',during which the barley's
own umylasc COn\'enS the starch in the gr"in 10 sugar, which is then fermented by the
chosen ye:lsl. Lager is produced by Saccharom)'cts c(lr/sbtTgl'nsis, ,lIe by Sacdwromycts
arn;Jirzt. Altho ugh Ihe mukins of beer appears to have been me<:hanized and standardized 10 a high degree , with wilor- made yeasts (see cha pter 10) and precisely controlled
conditions at every step, I have found man y and diffe rent bre ws during sabbatical trips
~round the world, most o f them pleasant e nough. Allhough J was bum in Brit:lin, tny
pref.. rence is for German beer, so I was delighted to find a reasonable f3csimile in Western
Samoa - " 'hieh used to be administered by lheGermans. B ritish becr('besl bitter'), drunk
292
~ UFPE -CCB
~aI8L!OT!;A
Ont-jom is another Indonesian food. this time made from press cake. which is the
residue left after oil has ~n expresscd from peanuts. The press cake is washed, steamed.
put in small containers, and sprinkled with pink conidia of the Chl)'soniUa an amorph of
NeuTOS{X'Ta silOphila (Ascomycetes, Sordariales) from the previoll5 b~tch of Ont-jom.
The containers are incubated untiltllc f~st-growin::l fungus has thoroughly colonized the
substrate. then the resul t is CUI up and cooked.
KlItsuobus hi is made in Japan by fermenting cooked bonito fish with Aspergillus
glaucu$ until it dnes out. Shavings of the resulting hard. dark substance are used 10
n~vour other foods.
It is obvious that we have no more than begun to e:>\.plore the possible uscs of fUllgi
in predigesting and flavouring ill'Lny basically nutritious but indigesti ble or tasteless
food substrate s. A world that welcomes the kind of guStatory trivia presented by most fast
foods .... ill surely embrace whatever comes after beer ~nd wine. bric and roquefon.
Further Reading
Gr:ly. w.o. (1959) The Relation of ~'ungi 10 Human Affairs. Holt. New Yo rk.
Gray. W.O. (19Sl) Food te~hnology an d industrial rny<.:ology. pp. 237-267 (in) Biology of
Conidi:ll Fu ngi. Vol. 2. (Eds.)O.T. Cole ond B. Kendrick. Academic Pn::s.~. New York.
Hc~dtine, C.W. ( 1965) A mil1enium of fungi, food and fermentati on. Mycologi a 57:
P3-1 97.
HesSI!ltine. C.W. and H.L. Wang ( 1967) Traditional fermcnted foods. Bio teC hnology a nd
_ -_ .
SLoengllleenn"
.
'" 9. '75
'8'
Wood. B.1 .B. and F.i'.I. Yong (1975) Oriental food ferrnent'lCions. pp. 265-280 (in) Th e
Filamentous Fungi. Vol. I. (Eds.) lE. Smith and D.R. Berry. Arnold. London.
20
1 have a gtem fondness for damson plum jam with all the lan gy skin of the fruit in it.
You just can't buy swffJi ke that at the supe rmarket. So when I fOllnd some damson plums
at OIJrlocal farmers' market. I carried [hcmhomc in Iriumph. inlendin; 10 makcjam-wry
soon. A week later I remembered my plan, and retrieved the fru it. only to fi nd thAt some of
the plums had a mould sporulating on them. Can you suggest. from the nature
of'~hc
subSLrute (a ston~ fruit), what that mQu ld m ight have been? (Did you remember Monilia?)
J quickly SO!1ed out the mouldy fruit and put it aside for my undergraduate class. I then
pined the sound fru it and cooked it very briefly wilh what seemed like an enormous
amount of sugar. I ladled the jam into steri lized jars, and covered it with a thin layer of
melted paraffin wax be fore sealing the jars tightly, That story exemplifies the problem of
food spoilage, and what we have to do to prevent it.
What 1S food spoi Jage?YOll may think the answer is obvious, But, as oflen hap~ns
when we ~it dO\\'n and try to define a phenomenon, it's not as clear-cut as it might seem.
How about this definition: 'Changes in the appeanmce, texture. smell or taste offoo<!. that
cause it to be discarded.' One imponant flaw in this defin ition is that the criteria for
acceptobility arc strong ly affected by cultura l or eCO rtomic conditio rtirtg . So lhe quantifi.
cation of the variou s criteria may have 10 be reformulated for different counlries or ethnic
groups.
Many kimls of food become visually unappealing ortly "hen fungi are seen 10 be
fruiting on the surfac~. BU! you must be aware by now that the int.. rior of the food wi!l be
riddled by assimilative hyphae. and perm eated by fUngal metabolites. long before visible
sporulation occurs (espedaHy if the surrounding air is dry). Those fungal metabolites
may include m yco to.d ns (see chapler 21). Even the most fastidious consumer can', al ways tell "'hen these are present. l\'lany kinds of food are processed before they reach us.
so the mouldiness that might be evident on raw peanut, will no longe r be appar~nt after
they have been turned into peanUL bUller.
Since ideas of wh:lt constitutes spoilage vary so much, no definition can be completelyobjective and scientific. But science has now added an imponant new criterion.
Food must be rel:!atded as spoiled, no maIler how appealing it may look. smell or taste, if
it contains pot...,ntially harmful levels of myco\uxins, (In bactcri al ternlS, the same would
297
Fruits are often preserved by drying or canning (or by m.1king into jam. as men
tioned under heading 2), and frui t juices now support a whole industry. Apricots and
peaches for drying arc impregnated with sulphur dioxide to preser.'e their colour. and this
also effectively preventS fungal spoilage. Unsulphured dried fruit can go mouldy. Prunes,
especially. afe sold in moist path which have an a.. of 0.SO-O.S5. This makes them
accessible to most xerotoierant moulds, which can be inhibited by sorbic or benzoic acid.
Canned goods are usually heated to a high enough temperature to destroy fungal spores.
but fruits with delicate texllires are pasteurized at lower temperatures. Healing 10 SOQC
will kill al1 zygomycete sporangiospores, and all hyphomycete conidia; but it won't kill
ascospores of BJ$$och{{ImJsfi,hu or B, lIivea. These Ihennotolerant ascomycetes sometimes spoil canned strawberries, soft drinks and fruit juices (prune, grape. pineapple). and
home-bottled fruit. If these fungi are cultu red. their Pal'dlomJces aml.morph s usually
develop. Fruit juices arc naturally contaminated with yeasts.. and the !lonna! course of
events would in\olve an alcoholic fermentation which would ultimately. as in the case of
wine, effec tively preserve the substrate, But if the juice is refrigerated. moulds. rather than
yeasts, will be favoured. Some fruitjuices(blad:curram, grape) are preserved with sulphur
dioxide. In conclusion, it is ....orth pointing out that we can't blame all f("\lit losses on the
fungi-bananas become brown and mushy through the action of their own enzymes.
(S and 6) Meal and Eggs. Although mOSl serious spoilage of foods of animal origin
is caused by bacteria. species of Penicillium* and Aspergillus . are commonly recorded.
aod may produce mycOioxins such as cyc lopiazonic acid. penitrem A, ochratoxin. jXltulin
and anatoxin. Fungi can ~ inhibited by refrigeration. vacuum packing. drying or irradiation.
(7) Fis h , usuall y dried. is most frequently contaminated by Eurol illm'",
Seopulariopsi.r. and Penicillium- species. /I.lyeotoxins produced arc OI.:hratoxin A and
cit reoviridin. Reducing the water activity of the su bstrate is the best way of preventins
fungal spoilage.
(8) Ra w l\lilk is u.' ually spoiled by bacteria ~fore fungi can begin to affec t it.
Pasteurization and airtight. refrigerated storage are the ~st ways to prolonS its shelf life.
Conversion to dried milk or cheese will also extend its life. but cheese is commonly
attacked by fungi. especially P~l!icillilrm comllwne *. but also b>' other penicillia. A.r
persillus ve~icolor. Sc{lp/l/ariopsis spcdes and /lrolium herbariom",. Spoilage is
delayed by reducing water activity, by vacuum packing. and by refrigeration.
Further Reading
Frazier. W.C and D.C Westhoff( 1975) Food Mic robioloJ,;Y. 3ed &In. McGraw-Hili, New
York-
or
Pitt. J.I. (19SI) Food spoi\ag~ and biodct~rioration (in) Biology Conidial Fungi. Vol 2.
( Eds.) G.T. Cole and B. Kendrick. Academ ic Press, New York.
Samson. R.A . and E.S. van Reenen-Hoekstl"il (19S8) Ln troduction 10 Food_ho rn e Fungi.
3rd Edn. Centraalbureau voce Schimmelcultllres, Banrn (with contributions by 12
other authOr<;).
~ UFPECCB
/DBIBLIOTECA
21
Introduction
Foods are usually noll-living bur natural organic substances, wllich are excellent
~ubs[ra[es for sapIc bic fungi. and accordingly Icnd to go mouldy if kepi too long. The
people of western countries. ge neral ly rel:uive ly wealthy and faslidious, will throw Qut
most food that is obv iously mouldy. BUI this is not necessarily true in the poorer nations,
where food is often a precious commod ity. not [0 be rejected because of a littl e Slilface
di scol ouration. This ultitude is re in forced in the Far Easl by the !;ommon use of moulds to
prepare traditionul fermented foods (see ch:lptc r 19). In some areas, indigenous peoples
prefer the spicy na\'our certain foods acquire when they go moul dy (d. the blue cheese
eate n by westerners). Animal,; will ohen accept mouldy feed. To compound tbe problem.
the teon mouldy refers on ly to food on wbich the contaminating fungi are already sporolating . BUI even food whieh looks perfectly edible may be riddled by lhe invisible assimilat ive hyphae of moulds. and contaminated by their metabolites. Do these tbings mailer?
[s mouldy food d3nerous? Thi s chapter will gh'e yOll some answers.
Some fungi. including many common mou lds (mostly hyphomycctes). produce
secondary m e ta bolit es-usuall y st~rojds, c~rol enoids, alkaloid s. cyC IOpcpl idcs and
coumarin, . Many su bstances in the IJstthree categories are tQxil: 10 animals and to other
mil:roorganisms at very low dosages. and are also pe[1;istenl and often lIeat-stable. Sueb
compounds are frequently prod uced in fungus-contaminated foodstuffs. remain there
even afte r processing. steri lization or cooking. and are unsuspectingly eaten. They are
called mycolo.~ ins. Over 100 stleh substanceS. produced by about 150 diffe rent fungi. are
now known, and more are being discovered every year.
':11.-0.55, pigs----O.62, shee~I.O. Th31"5 bad enough, but it was dis,o\'ered that even if the diet didn't contain sufficient loxin to ,ause a,ule poisoning, prolonged exposure 10 IDu,h lower levels will often cause liver cancer. Many experiments
have demonsu;"l1ed this in rats. As little as O.Q1S ppm (parts per million) in the diet over 70
weeks caused neoplasms in all rats tested. At I ppm this takes only 40 weeks. At 5 ppm it
takes 9 weeks. Sh.asta trout are so sensitive thai as little as 0.5 Ilg/kg (0.5 ppb) in their food
over 20 months will produce similar results.
If we examine the incidence of li ver cancer in human populations, we find it is
exceptionally common in some devel oping countries, especially those of Subsaharan
Africa and the Far East. The problem i ~ well documen ted in Uganda. Swaziland, Kenya
and Thailand. All have elevated levels of liver ,aneer, and the diet in ea,h country is
signifi cantly tontaminated with aflatOxins. Although we cannot, of course. prove experime nt:llly th3t aflatoxins cause liver cancer in humans, the suspicion is strong enough to
be almost a ,erlainty (as with the connection between smoking and lung cance r). And we
do know Ihat in some other mammals, aflatoxins are the most potent carcinogens yel
discovered.
G. CWJo'porium
h."O;><~'"
l\ I YCOT OXL~S
What is being done to mo nitor and conlmi the levels of aflatoxins in our diet ? In
Canada the allowable limit of contamination, originally 20 ppb in a finished prodUCt, has
been reduced 10 15 ppb. Germ any allows only 10 ppb. I believe that no detectable aflatoAin should be permilted. Ifproper aue ntion was paid to storage and selection of peanuts
for human consumption, and to appropriate dilution of mildly contaminated nuts, this
standard OOIIld be easily attained.
Aspugillus fla vus competes beSt in wann climates, on substrates that have low
water Contems (low 'water acti vities': see chapter 20). It was originally classified as a
storage mould. but some rontaminarion has now been traced back to the field: the fungus
can be an adventitious parasite. inv adi ng insect-damaged tissue. Serious aflatoxin contaminat ion has been found in peanuts. brazil nuts. pistachio nuts. al mon ds. walnuts.
pecans, filberts, cottonseed, copra. com. grain sorghum. millet. palm kernels, beans. wine,
milk. cheese, dried fish , garlic, spaghetti, noodles, bread, flour, and figs . Aflatoxicosis is
mainly encountered in wanner climates, and it is in teresting to note that peanutS now
grown in Ontario seem to be free of nfl atoxin--one advantage to living so far nonh.
10
b~o.
Each year in South Afri ca about 200 people suffer from an unnamed hacrn orrhagi c
disease with additi onal u:emorgcnic (neuroto:dc) effe cts, plus associated Ii" er and kidney
symptoilli. This complex syndrome is believed to result from drinking home-brewed
natin' sorghum beer. often eomaminated with at least 1\\.0 mrcotO ~ins, tcnuawnic ac id
produced by Ailt'maria allemma and P/W/rW .lOrghilla. and c ylochal~sin produced by
Aspergillus c/mams.
.w
Equine Leucoencephalomalacia:
' Hole in the Head' Disease of Horses
In horses. donkeys ami mules. the first signs of this condition arc apathy, protruding
lOngue. unwillingness to
nl O\'~
./.r'~. ~.-<00,
".
,,
,
,,
co,
. . .
_._.'
.~
. ..:
. .'..:....
..
."J.
.,., I,
."""
....
.-
O C """TOXI~ ~
SPOR ' D IS ~ I N
' ,,
,. J;p4
'"
,'
"
"
PATULIN
TL~ \IAtO"IC
ACID
becomes delirious and may run full ti lt into fences. Finally it falls over. tltrashes ilS legs in
!he air, and dies. Death may oo:;:cur in seven hou rs 0( st,'eral days. A poslmortem reveals
areas of brain necrosis-large. irregular holes whe~ the white matter has disinlegrated.ll
was found th at the disease condition could be reproduced by feeding the animals com
moulded by Fusarium mOlliliforme (the anamorph of Gibberellajuji/.;uroi: Ascomycetes,
Hypocreales) , Fi eld outbreaks of this mycotOll:icosis have occurred in Argentina. Brazil,
China, Egypt. South Africa and the U.S.A. . but de spite Ihe dramatic signs and symptoms
it produces. the naNre of the mycotoxin invoked has nOI yet been detennined.
Syndrome in Pigs
Pig fmncrs sometimes find that their young female pigs (,gilts) develop swelling of
vulvJ , ~nlargemem of mammary glands. cnbrgement of the uterus. and sometimes ev en
rectal and vagi nal prolaps<>-the vagina and associmed structures swell and are often lilerall) ~xlruckd. lntemally. the ovan.:, atwphy.At the same time. the testes of young male pigs
shri\"cl. and their mammary gla~d'i enlarge. Since all ofthesc: symptoms affect primM)" and
secondary sexual ch:lraCteristit:;.. the in,u!\'cment of some kind of
hormone might be
th~
=,
3 12 CHAPTER D VENTYONE
Eventually, in 1963. the e~use of the disease was found to be a to)(in e~lIed
sporid cs min, produced by a saprobie hyphomycete, PithomyceJ dwrtanlm (Fig. 2 1.1 E).
growing on dead pans of forage grasse s. TIle name of the disease is misleading. ~cause
the liver damage. rather than the skin problem, is lifethrealen in g. The photosensitivity
causing the 'facial eclema' isasecondary symplOtncausedby a pofphyrin, phylloeryth rin.
This is a product of chlorophyll digestion that builds up in the peripheral circulation
because the damaged liver cannot e)(crete it. Since il would be very expcnsive to spray
large <lfeas of grassland with fungicide. attempts aTC made to avoid the disease by forecast
ing weather oondueive to sporulation of the fungus, and moving sheep to less susceptible
grazing areas during such periods.
lupinosis of Sheep
Shcep or other animals grazing on lupin stubble in Australia, New Zealand., South
A[ri~a. and Europe. especially a week Of so aflCr heavy raia~, may become anorexic. feverish
and listless, then jaundiced. Up (0 hatf of affected animals may die. 11le liver is cleM!y the
main organ affected. It was fiN suggested as long ago as 1880 that the disease might be
caused by to)(in, derived from fungi growing on the lupins. but final proof of this ..... as not
forthcoming until 1970. Phomops ln A. the hcpatoto.\in responsible. is a cyclic he.xapeptide
produced by the eoelomycete, Phomopsis /eplOslromifomlis (the anamorph of Dioporthe
\>oodii: A~m}'cetes. DialX"'rthales). Thi., fungus produces black pycnidial oonidiorn:.ua on
st~ms and pods of L"pinus. and the teleomorph has also been relX"'rtcd from this suhstF.l te.
TIle fungus is a pathogen that conti nues growing Sliprobical ly after thc death of thc host,
producing toxins in both phases. In Wcstem Australi a. where lupinosis is a ~rious problem,
attempts are being made to breed lupins resistant to the Plromopsis.
Detoxification
It seems thot we wi!! always hove to deal with mycowltin-contaminalcd food and
feed . Arc there wayS of removing or de~troying mytotoxins? Aflatox in has been the
subject of most d~toxification research. Although this toxin is relati ...tly heal-Stable.
heati ng 11 contaminated sub5tr.lte to lOOOC for 2 hours can degrade 80% of the af1ato ~in
pre~nt. Dry roasting nu ts has a similar cffect. But heat treatment won't eliminate aO:1-
Further Reading
Christensen. C.M. (1975) Molds, M ushrooms and i"'lycoloxi ns. Un ivcrsity of MinneSQ{a
Press. Minneapolis.
Egmond. H.P. von (1988) Mycotoxins, sampling and chemical detection. pp. 250-261 (in)
Introduction to Food-borne Fungi. 3rd Edn. (Eds.) R.A. Samson & E.S. vanReenenHoekstra. Centraalhureau voor Schimmelc ultures, Baam.
Howell. M.V. ( 1982) The detection and determination of mycotoxins in food and
feedingsluffs. Journa l of the Science of Food and Agricultur~ 33: 590-59 1.
Krogh, P. (Ed.) ( 1988) i\lycoto;<ins in Food. Academic Press. New York.
Marasas , W.O. and P.E. Nelson (1987) l\ lyco toxi cology. Pennsylvania Statc University
Press. University Park.
Mirocha. C.J., R.A. Pawlos ky. K. Chatterjee, S. Watson and W. Hayes (1983) Analysis for
Fu;arium toxins in various samples implicated in biological warfare in Southeast
Asia _J ourmll of the Association of Official Analytical Chemists 66: 1485-1499.
Pringle. P. (1985) Politicai science. The AII:mlic l\lo nlhly. VoL 256 (4): 6781.
Purchase, I.F. H. (Ed.) (1974) l\I)'cotoxins. Elsc vicr.Amsterdam.
Radicks. J.Y., c.w. Hesseltioc and M.A. Mehlman (1977) M ycotoxins In Human and
Animal Health. Pathotox Pubhshel"l<, Park Forest South, l11inois.
Samson. R.A., E.5. vann Reencn-Hoekstra (and 12 others) (1988) Introduction to Foodborne FungI. 3rd Edn. Centraalborcau voor Schimmeicultures, Baam.
Scott, P.r.l., H.L. Trt;nholm and ~l.D. SllttOn (&IS.) (1 985) l't'l ycotoxins: a Canadian Perspecti,-e. National Research Council of Canada, Ottawa.
Stoloff. L.. S. Nesheim. L. Yin. J.Y. Radricks. M. Slack andA. D. Campbell (1971) A mullimycotoxin detcction method for a nat oxins. OChtato~ins. zearalenonc.
sterigmatotystin and patulin. J ournal or the Association of Official ADalytinl1
Chemists 54: 9 J -97.
Wylie. T.D. and L.G. Morchouse (Eds.) ( 1977-78) Mycotoxic Fungt, l\lycotoxins, i\Iyc_
otoxicoses. Vols. 13. Marcel Dekker, New York.
UFPECCB
@ BIBLIOTECA
22
Introduction
A man is brought to the Emergency Department of a hospital suffering from diarrhea. abdomin al cramps, nausea and vomiting. Hi~ problem is diagnosed as gastro-emerilis. He is given atropine, donnatal, and intravenous fluids to combat dehydration. then
sen! home. The vomiting and diarrhea go on for another 24 hours. By now he is seve rely
dehydrated. and has to be admincd 10 hospital. Over the next IWO days, his li1'cr, kidney
and he:u1 begin \0 fail. Despite treatment of his symptoms wilh a b,attery of :lntibiotks.
CQrtitosteroids. vitamins. stimulants :l!Id intravenous fluid. he dies.
This is a true story. The only thing I didn't tell you was that the man had eaten 11 meal
of wild mushrooms about 12 hours before the onset of his symptoms. By the time you
ha' c read this chaptef, you should be able 10 diagnose his illness correctly, and suggest
treatm~nl.$
People can convenie ntly be. divided inlo two groups: those who love to eat wild
mushrooms. and those who would never dream of doing such a thing. Thcre doesn't se.:m
10 be any mid dle ground on this issue: )'ou are ~ith~f a 'picker' or a 'kicker." This characteri stic seem;; to be culturally determined. Most people of Anglo-Saxon ori gin arc kickers.
II hile those from Cen tral and Eastern Europe are pick.ers. Piclting is a p:lstime that occasionally gct~ thcm into trouble. There are about 10.000 different spedes of fleshy fungi.
The vusl majority arc perfe.;tly innocuous. A rcbtively small number are hunted for theif
dehcious flavour. and a cooperative few have been domesticated (see chapter 18). But
another few 3re de3dly poisonous. and m:tny Olhers can cau.~e more Of less seriou sdiscomion iflhey arc unwittingly eaten. During thc course of human history I would suspeCt \hal
all 10,000 species of agarics ha,"e been ealen. This chapter considers what we hll\'e Icarned
from the trying. tragic or transcendent;!1 experiences ofthosc: who made random Of uncon
\ cntional choices of mushroom fOf theif free meal.
The main problem is one ofidemirication. Thcre is no simple rule or tCSt thnt will
tell wh~ t her a mushroom is edible or deadly poisonous. MOlly people are blis~ full y un~
aware of this. and rely on tes ts which ore irrelevant and fallaci ou.~. Th~y are playing
Rlissian roulelle. You should eat wild mushrooms only if you know, Of can detcnnillc ,
their !.Cicnlific names. If you are sure. from observation (some of it through thc microscope) or cxperience. that all of a particular collection of fungi belongs 10, say. Cantit(lrflhlJ
316
Table
Toxins
I. Amanilins (cycJopeptides)
Fungi
A. ~iroJa.
n. Gyromitrin,
mooomcthylhydrazine
III. Orcllaninc:
IV, Muscarine
V. IbOlenic add.
mu~cimol
VI. Coprine
COllocybe C}'(lIl0f"L~;
Gymllapilus sptClllbilis, (?) GymllOpilus spp.
Panaealus foeniurii. P. slIbballeatus;
Psi/oeybe rllbensis. P. cy,meKtnS, P. semilollceafo, P.
si/,'mica,
PholiOla sqU(lrrosu:
RU$Sf(la emttic(I;
Scltroderma allromimn:
Tricholoma pardi"'''n: etc.
dbariu.l (the chantere]]e: Fig_ 5.5 0), or Morchella escu/elila (the morel: Fig. 22.1 C), and
IhJt the fruit bodies are young a!ld freshly picked, experience tells us that you can eat a!ld
enjoy them. as mycophugists have done fOf thousands of years (though some people are
aliergic to mushrooms). Every year, many people take unnecessary chances by eating
unfamiliar mushrooms, or confuse poisonous species with edible ones, and every year
some unfortunates are fatally poisoned.
Since most North Americans afe kickers, they lend not to become mushroom poisoning statistics _ Europea!ls, however, are pickers, and have suffered as many as 100
fatalities in two weeks. In 1975, a Swiss newspaper reported 54 local deaths during a short
period in late summer. Which fungi killed these people? What are the toxins involved?
We recognize eight different kinds of mushroom poisoning, whi ch are listed in Table
22. 1. A quic k look at this table will show Ihat fatalities arc usually caused only by groups
I, II and III. In fact, 50% of all serious mushroom poisonings, and 95% of all fatalities, are
caused by members of a single genus . Amanita, Which fruits in late summer and falL
B: OaJ.,ina ~ vlum"aJJs
lam." ,,")
Ida rcl>~/J~
UC"IM I~
A:
A _~i l~
vJros:>
I. m.",,)
0 : Gyramflr"
. u"r.M'
IS,,,,"',i"-MMK)
~~ UFPE-CC1/il'
2'<
1\ ::1'' III_l\.'0 -fE Cl~",l
-..
system, irritates the gaslro-intestinal tract, and damages the liver. Methaemoglobin and
free haemoglobin are present in the blood. Levels of bilirubin and livcrenzymcs rise, and
blood sugar falls. Unless the tox ic nature of the mushroom is diagnosed almost immediately arler il has been eaten, there is linle point in evacuating the gut. Pyridoxine hydrochloride should be administered as a spedfic phySiological antagonist of MMH. The
patient's blood sugar, liver and kidney function, and free haemoglobin level should be
monitored. intravenous glucose. foreed diu resis if free haemoglobin rises. haemodialysis
in severe cases, and other supporti ve measures, may be needed.
o """"';1.0
""' ..,.;.,
(;t>oc..,;o "",,,
""""""'1
E: 1'$#0<11'" nrllMoI"
(;l>ilocy~"'. ~I
Further Reading
Azzareni. G .. R. Galli, A. Bernini and F. Polani (1983) Funghi Velc nosi. Edizioni La
Tipoteenica. Milall.
Baslicn. P. (1985) J'al du man ge r desAmaniles mort ell cs. Flamm::uion, Paris.
Bauehc\, 1.M. (1983) Treatment of Amanilll phaIIoides poiso ning - the Bastien method.
Bulletin of the British ~ Iycological Socicty 17 (2): 110-11 1.
Faulstich. H.. B. Kommcrell and T. Wieland (1980) Aman ita To)(ins and Poisoning.
~rhard Witzstrock, Baden-Baden.
Ja~n ikc. 1. (1987J Of toxic mu shrooms, fli es. and worms, Jl,lcIlvainea S (I): 3234.
Lampe. K.F. (1991) Human poisoning by mu shrooms of the genus Cortinor;IIS pp. 497521 (ill) To)(icolo:;yof Pl unt and Fungal Com pounds. (Eds.) R.5. Kccler& A,T. Tu.
~bl"~c! Ddi:er, New York,
Lincoff, G_and D.II. MitChel ( 1977) Toxic and Hallu clnoge nic t\-lu shroom Poisoning.
Van Nostrand Reinhold. New York.
Liuen. W. ( 1975) The most poisonous mushrooms. Scientific America n 231: 9010].
~Ieixner, A_ (1979) Amu toxin -Nachweis in Pilzen. Zeitsc hrift fiir i\lykologic. 45: 137139.
IJ.f, UfPECCB
@ BIBLI01ECA
Medical Mycology
23
Introduction
Three rather different groups of fungi actua lly cause spedfit diseases. A few obligatc!y pardsi!ic fungi (dcnnatophytes) have evolved specifically to onoek the omer sur_
face of human bei ngs. A few other fungi which callse disease ill people are normally soil
organisms, but have also adapted to life in the unusual and rather hostile environment of
the human body. often responding to this environment by developing a different mor_
phology (thermal dimorphic saprobes). A third group of opportunistic saprobcs can auaek
1,15 onl y when OUf defenses arc: down-wiltn OUf immune systems themsel vcs arc: diseased
or deficient. or when \Io'C artificially suppress mem. as we mUSllO prevent the rejection of
transplanted organs.
We can divide fungal auacks on our persons illlo: (I) cu ta neou s in fections, which
involve the outer lay~fs of the skin and cause an allergic or inflammatory response; (2)
su beuhlll~ous infections, usually involving fungi of low inhe relll virulence which have
been introduced to the tissues through a wound of some kind, and which remain locali zed
or spread only by direct mycelial growth; and (3) system ic infections, whic h afe cau;cd,
either by true pathogenic fungi which can establish themselves in normal hosts, Of by
opponunistic saprobic fungi which could nOt infect a healthy host. but can anad: indio
viduals whose immune system is not working. Both kinds of fungi sometimes become
widely disseminated through the body of the host
Cutaneous Infections
Most cutaneous mycoses arc caused by a spccialiled group of kermi noiylic fungi
called the d crmat ophytes, of which you hal'e already learned something. There are about
40 spe<:ies of dcnnatophylic hyphomycelcs. placed in 3 genera. Epidermophyton has 2
spe<:ies. Microsporum (Fig _4 _8 C) has 17, and TrichophYlOn has 2~ species and varieties ,
Eight species of Trichophyton have teleomorphs in ArlhAAiermo, and nine species of
Miaosporum have tcleomorphs in Nnlmiuia . These holomorphic genera are both memo
bers of the family Anhrodermataceae (Ascomycetes, Onygenales).
About half of the IIwnatophytes nrt found only on people. clll.Ising diseases com
monly called tinen or. more colloquially. r ingwo n n . The s.c have no reservoir of infection
in the soil or on animals: they can groll' only on humans, although thcir arthric conidi3
can SUfvive in carpets 3nd upholstery for up to two years. Many of the resl are usually
isolated from other mammals. Microsponlnt canis has its reservoir in tnecal. it rn:ly move
327
328 CHAPTERn\'E1\TI'-THRE E
to dogs o r hl.lmans. bl.l t will die Ol.lt after one or two perso ll -to-person tran sfe rs. If it i~ to
5urviH', il must return to the cat for tejuven:uion. About five sptcies Me recorded from
both man and animals. The irrit:uion caused by the presence of the fungus stimulales the
epithe lial cells of tIle host to divi de more often than usual. This increases the amou nt o f
kerati n availabk to th e fungu s. und also means that more flakes of skin containing infec_
li\e mycelium will be shed. Epid(nnophy/ol'! floa;osum causes transielll infections, and
relies on this nfolialed material for quick spre ad 10 Other hosts. Tric/lOpfrylorl. rubn,m
tends to ca l.lse chronic infection5 of the foot and tOenails. so the host prod uces infect ive
materi ~1 over a period o f years, Almost everyon~ is suscepti ble to short-tenn infection b>'
Epid(nnqphylOl1 floccosum, but a chronic Trichophytol'! nrbrum infection o f one marri.:lge partne r m~y never be transmi tted to the other. TrichophylO'l collcemricllm cau~es a
c hroni c ri ng wonn of the body in Pol ynesians (tinea imbriC2ta. tokel~u). bllt is never
tr;ln~milled to caucasians or blacks living in the same communities. Trichophrton rubmm
can anack any pan of the skin, but Microsp()ntm aldOifini; and Trichophyton tollSfmms
are found mainly on the he ~d (tinea capitis), and Epidennophyton flo cc().lUm usu all y
in fec t. the fC(:{ (tinea ped i~, athle te 's foot) or the groin (ti nea cruris, j ock itch). It must be
emphasized that these fungi are not growing on living tissue. Their cli nical effects are d ue
to the various irritants they produce: enzymes su<:h as proteases. peptidases .:lnd elastases,
li nd other me t~bolite s. The condition is really a form of tox.ic dermatitis.
T he )'ea51. Candida o/bicans ( Fig, 6 .2 C). is a normal compone nt o f the gut
microbiota, but e.~cessive wetness. 01 very ti ght clothing, can trigger rapid ovcrgrowth of
skin by th is fungu s. It <:an cause di~pef raSh, infections around fingernails, in annpits lind
crotch . and under breasts. Mucous membranes Me part icularly susceptible to in fl ammation by the toxins of this fungus : oral candidi.:lsi, (thrush) is common in th e IICwbom.
arising whe n the nomlal fl or.:! of l ae!ob~cjJJi doesn' t develop quickly enoug h. Pre gnant
women produce vaginal secretions with altered levels o f gl ycoge n. Th is encourages the
growth o f Candida. and "~ginal candidiasis is common in pregnant women. Their husbands sometimes contract candida bat ani tis, a nasty infection of the pen is. though this
Ill.:l}' also be a con>equcnce of diabetes. If cutaneous candidia sis becomes chronic, it may
be a sign of various abnormalities of the thymus. of the thyroid, of white blood ce lls
(Jeucocyles). etc.
Systemic Mycoses
As I pointed OUt aoo,c. these
di)~3ses
an:: of two ,"cry diffcrent types: thos.e prod uced by specializcd pathogcns. and thosc caused by opponunistic saprobes_ There are
four true pathogens. all of "hieh an:: dimorph ic-lhis means they havc one kind of
morphology outside the host. anmhcr inside the host Three of these diseases are extremely common in Non h America. and the founh in Sou th America. In the first three
mentioned ~low, the eaUSall\C fungi are rcadil>' isolated from soi l. Although these and
other mycoses occa~ional1y have horrifying effects on the human body, I am not goi ng to
gross you out wilh pictures. If you really must know how bad things can ge l. there are
many pathetic photOgraphs on thc CD-ROM that accompanies this book,
_.-
Dimorphic Pathogens
(1) HistoplasmosIs, commonly abbreviated to 'histo; is caused by the HiSlOp!usma
capslllaw/ll anamorph of Ajellomyces cllpslllaws (A:;comycet~s). This ilililmorph grows
well in high- nit rogen substr~ts like wild bird droppings, chic ken manu re and bat gu ano.
Anyone who distu rbs suc h d~posits, or spends much lime around them, is likely to become infected. Conidia of the fungu ~ are inhaled and cause primary infections in the
lungs. About 95% of 011 cases prodm:e no obvious clinical symptomS. and heal spontaneously, lea"ing tile ~ubjcc t with only a small calcified lesiou in the lung, and resistance to
rein fection . In the other 5~. "mous clinical symptoms del'clop. The inhaled conid ia
aSSUl\1e a yeast_like form, ~nd become parasitic within histiocytcs (phagocyt ic host cells).
At first 'Ilu-like, the di sease may go on to produce a progressive lung disease that mim ics
tubercu losis. If untre~le d, it may eyen d~ve lop into a ge neralized. systemic infection
which can attack aU intcrnal org~ns. ultim ately with fatal result s. Histopla~mosis is endemic in Ih~ !llissi~sippi ar.d Ohio Valleys of the U.s.A ....... hen:: about 40 million ~ople
ha~'e had the disease (most ofth"'m without kno ..... ing it). It allac ks males more commonly
than f"'maks.
(2) Coccidioidom) cos is is a nasty tongue,twister of a name, often eontt"3c1t':d to
'coecy: for the disease caused by Coccidioidts immilis. This fungus thrives in dry, salin~
soils. and is endemic in desen areas of the .outh ..... estcrn U.S .. where th e disease is oftcn
called ' valley ft':ver: and ~k,ic o (though it is strangely absent from the desens of Africa
and Asi~) . The process of infection. progress of the disease. and clinic(tl sy mptoms. ~re
very similar to those of histopl~smosis. though the fungus is not intr;lcellular, and form s
spherical structures containing spoces. In culture. the same fungus produces chains of
alternate th3l1ic-anhric conidia. and h 3~'no known tcleomorph_ Millions of peopl'" in the
Opportunistic Pathogens
Opportuni<;tic infections are cal.lsed by diverse fung i-a few species of Aspergillus,
Candjda_ Cryptococcus, and some members or the Mucorales. All grow well at body
temperature, bUI do not otherwise seem particularly different from closely related nonpilthQgenic spec ies. None of them can usually cause an infection in a normal, healthy
individual. All rely on some b"reakdown in the mechanisms uf reslstanl:e. This kind of
systemic fung al infection is often al:omplic atiun of diabetes, A!DS, adva~ced cancer. or is
a sequel of steroid or ~ntibiolic therapy.
Candidia.>is (aho calkd candidoslS). The causal organism is Candida alhic(m.~. III
children, ural candidiasis that becomes chron ic, and spreads down the oesophagus. is
prob~bly a sign of genetic defects or multipl e endocrine deficiencies. In adults, aliment~ry cand id iasis may be assocIated with diabetes. AIDS. steroid or amibiOl;C therapy,
canc~r. blood disease, endocrine deficiencies, or other debilitating conditions. In \cuke rlli~ p~tients. candidiasi~ may t><;,com~ truly systemic, or may produce a form of ,epticaemiJ. Either way, it cun ultimate ly be fatal. This condition may also be produced by
r~peated entry of the fungus with injections self-administered hy drug addicts, or as a
sequ.e I of long -term antibiotic or steroid ther~py. or indwcllillg catheters. Candida septicaemia may also arise JS a result of parenteral hyperalimentation (feeding by continuous
direc t injection of fll.lids, often undertaken during treJlment uf severe gastrointestinal
disease). If patients remain on hyperJlimemation for more than 20 days, more than half of
them dewlup Cal1dida septi<:aemia. Fortunately, in patients with intact immune responses,
the infection often clears up if the needle is removed.
UFPE.CCB'
MEOICALMYCOLOCY 331
Zyso mycosis is caused by se~eral opportunistic members of the Mucorales
(Zygomycota). Rlrizopus orrlrizu$ and Rlri:oplts of)'UI~ are mo&t commonJ y in~oh'ed, but
s~ies of Muco r, Rhizvnrucor and Absidia have also been reponed. Four kinds of systemic disease occur: rhinot'erebral, thoracic, gastro-intestinal, and cutaneous. Rhinocerebral
zygomycosis attacks acidotic diabetics (who have high blood sugar, high ketone levels.
and usually some leucocyte dysfunction). The infection begins in the sinuses, then grows
with dramatic rapidity outward to the eyes and inward 10 the blain. The eyes bulge and
may become paralysed. the eyelids droop. and there is often some degree of facial para!>'sis. The di sease usuaHy progresses with devastating rapidity, and is oflen fatal within 7
days.
Thoracic zygomycosis strikes people with leukemia or lymphoma. and occasio nally also diabetics, lraIl.>plant patients undergoing steroid therapy, or patietUs on d ialysis.
The symptoms are those of bronchi tis and pneumonia. wilh complications like thrombosis or infarction, caused by direct invasion of blood v~,ssel s by the fUngus. This disease is
also fatal if untreated_
Gasrroimestimlzygomycosis almost always occurs in ThirdWorid coumries, attacking children who art' already suffering from Kwashiorkor (chronic protein deficiency).
The causal agent, Ab$idia cOf)?1Ibifuu (Zygomycetes), invades the wails of the stomach
an d ime~ tine, blocking the arteries. The resulting necrosis and perforations are fatal.
CutaneQUS zygomycosis occurs when zygomycetous fungi colonize bums. In a severely
burned, and the refore extremely debilitated, patient, the infec tion may spread rapidly and
be quickl)' fatal.
Cryptococcosis is ca used by an encapsulated. budding basidiomycetous yea;;t.
Cryptv('OCCUJ ncojonmm,,!, the anamorph of filvoosidiella neojvm,ans (Aphyllophoralesl _
The anamorph commonly grows on pigcon droppings, so everyone is eXpVscd to thc
propagulcs of the fungus. Many people contract sub-clinical or asymptomatic
cryptococcusis which r~sol\'es spontaneousl y. An unfortunate minority, often already
suffering from leukemia or !)'mphoma. or on immunosuppressive therapy following organ transplants, dewlop lung disease which may thcn become systemic, Th is phase
involves bones, or organs such as hean. testicle. prostal<l or eye. and is often fatal. A
second fonn of the disease is cryptococcal meningitis. Patients compla in of inneasingl)'
severe headaches, which eventually escalate into meningitis. Untreatcd cryptococcal
meningitis is always fatal.
As pergillosis_ Although species of As~rgil/lls {HyphomycetCSl cause other health
problem ~, such as acute and chronic at1ato.~in poisoning. we ~ co nce rned here only with
diseases caused by me gt'O\'th of the fungus itself somewhere in the body. (1) Bronchopulmonary aspergillOSiS is usually caused by ihpergillus fumiganu, which colonizes mucus within tile bronchi. evoki ng a severc allergic reaction. (2) In Asptrgilloma. the fungw;
forms a mycelia l ball in a lung cavity produced by an earlier attack oftubereulosis. The waH
of the cavity illay efod~_ causing the potient to spit blood. and necessitating surgical inter
ventian. (3) Invasive aspergillosis is foun d only in patients who are severely debi Jitat ~d. or
are immunosuppressed. as in AIDS. The: fungus grows outward from the lung. invading
blood vessels and spre<lding to other organs through the bloodstream. This insidiolJs diseas<: is usually fatal, and is often diagnosed only when an autOpsy is performed.
Since the rise in the number of immunorompromised patients, those suffering from
cancer and AIDS. as well as those with transplamed organs. new groups of opportunistic
fungi ha\e been ob.erved. Phaeohyphomycosis is the genera! term for suc h diseases
produced by about 40 darkly pigmented conidial fungi. Hyulohyphomycosis is a general
term for opportunistic infections caused by about a dozen non-pigmented conidial fung i.
Fusarium is one of the commonest among these.
332 CRAYTER n YEl";iY-THREE
Treatment of Mycoses
Ahhough pot.:lssium iodide (KI) has been used successfully in the treatment of sporotrichosis s ince 1903. there were no really effective drugs to combat most other fu ngal diseases. Until fairly recently, several of thesc diseases. such as blas tomycosis, mucormycosis.
and di sseminated fonns of histoplasmosis. coccidioidomycosis, cryptococcosis. candidiasis. and aspergillosis. were almost al\1{ays fatal . Antibacterial antibiotics usually had little
or no effect on fungi, and might actually make things worse by knocking Out the competition. Fortunately, a number of effective antifungal antibiotics are now available (though
they are nOl without side effects). Most important until very recently were two polye ne
an tibiotics produced by Srrep/Otn)"ces spp. 1be flfSt, Nystatin, introduced in 1950. is an
e ffective rreatment for superfi ciul and oesophageal candidiasi s, Drs. Brow n and Hazen, the
twO women scientim who di scovered th is antibiotic. philanthropically gave their profits tu
est:lblish a fOllnd.:ltion that finances research in medical mycology.
The second polyene antibio tic. Amphotericin B (Fungi zone). wh ich became avail
ab le 1Il 1957, represented a major breakthrough. It is effective agaim;t most o f the potentially falal deep-seated mycoses when administered. intravenously. But il is a \'Cry to;(ic
substan ce with many side-effect~: patients oftcn need sewmJary treatment to eupe with
the attendam nau sea. phl ebitis (i nflammation of major blood vessel s), hcadaches and
impairment of kidney function. This drug should be given only to patients whose condition is potentially fatal. Although Amphotericin B usually works. some resistant strains of
fungi. especially Aspergillu.1 flul'us. have been encou ntered. and one of my colleagues
has had the truly terrib le e."l:perience of watch ing a 14-year-old slowly die as his brain was
gradually destroyed by this fungus. Miconazole (Monistnt) is a lso used intravenously to
treat several of the major systemic fungal in fections, but il. 100, has unpleasant sideeffects, especially nausea and ph lebitis. Crypto<;occosis is now treated with a combina
tion of 5-nuorocytos ine and AmphOlericin B. Another antibi otic. Griseofulvin. derived
from Penicillium griuofidvwtl ( Hyphomycetes), is useful in oral doses of up to I g per day
for treatin g dermatophyte infections. Newer. topical treatme nts for athlete 's foot an d ring wonn are To lnaftatc (Tin ael;n). Canesten (Clolrimawle). ha\uprogin, miconazole ni Irate. iodochlorbydroltyquin, thiabendazole. or glutaraldehyde. Topical and system ic
ueaunenlS are often used in parallel for stubborn cases. In 1931. a new antifungal anti biotic, Ketueonazole (Nizoral), became available. BUI althou gh it can cure severe cases of
s.ome systemic mycoses, il should be used only in clttreme cases, because il has severe
side-effects: adrenal suppression in both sc;(es. and aspermia and impotence in males.
Perhaps I should conclude this chapter by tclling you not 10 worry too much after
readin g it Although cQccy, histo and blaslomycosis are endemic in many areas of North
Further Reading
Ainswonh. G.c. and P.K.C. AuslWick(1973) fungal D iseases Or Animals_ 2nd Edn. Com~
monwealth Agrkultural Bureau:.:, Slough.
Camp bell, C.K. and
gist 3(1): 7-9.
Delacrctaz, 1.. D. Grigori u and G. Ducel (1976) Color Atlas of Medical Mycology. Hans
Huber, Bern.
Emmons, C. w. , C.H. Binford, J.P. Utz and KJ . Kwo n-Cbung (1977) Medica l Mycology.
Lea and Febiger, Phi ladelphia.
Rippon, 1.W. (1988) Medical Mycology. 3rd Edn. Saunders, Philadelphia.
Speller, D.C.E. (1980) Antiru ngal Chemotherapy. Wiley, New York.
Vanden Bossche, H., D.W.R. Mackenzie and
Aspe rgillosis. Plenum. New York.
The CD-ROM which accompanies this book has many illu strations of dise~s caused by
fungi-just look a1 chapter 23.
: UFPE-CCI!>
I!$ BIl3 U01ECf:,
Commercial Exploitation of
Fungal Metabolites
24
AI the end of the twentieth ce ntury. exploi tation is something of II dirty word. Exploiting people means laking advantage of them in some way - of their gullibility. gIttd.
need or weakness. Exploi ting niltura! resoulU:s has oome, a]lloo often, 10 mean depleting
th~m (thi nk of OUf forests ilnd fisheries). However. I don 'I think we need wOlT)' 100 much
about exploiting most fungi. al least the ones that grow in pure culture. They are in many
COStS il prime e xample of il rencwuble resource, always ready to germinate from an almost
mfm i!c i>Upply of spores or hyphal inoculum, ahle 10 grow on a wide range ofm:uerial-, that
are generally regarded as surplu s to human requirements, such as bagussc (what is left of
sugar cane after the sugar has been c;.;tracted), and :u rnc:d with II broad spectrum of
biodegradative and synth eti<:: enzymes. It isn't that long - only a couple of generationssince !he commercial uploit:l.tion of fungi extended only to !he growing of mushrooms and
the femtentation of various substrotes to produce alcoholic drinks , but since the discovery
of penicHlin. entrepreneurs have bee n busy looking for, and finding. many use ful or inlere~ting fungal products _ And now with the up\osion of molecu lar biology. fungi have
become useful organisms which can carry nnd c:<.press II variety of human and othereukory
otic genes. This chapter i5 not intended to CO\'CT all of those angles. because some of them
have alreildy bo..-en discussed elsewhere in the book - for example. the large scale cu lti valion or collection o f edible fungi is dealt wi!h in chaplC'r 18. their use in the manufacture of
food and drink in chapter 19. thcir use a,<; agents of biological control in chapter 14. their
expression of human genes in chapter 10. But it seemed a good idea 10 compile the various
ways in which we humans use fungi, and especially their metabolilO:s . if only as a benchmark
against which to measure future progress in this area. And some of those ways have not been
explored elsewhere in the book.
The lOp twenty ph armaceuticals $(lId world-wide in 1997 included six drugs dc
rived from fungi. Three are cholesterolreducing drugs (hypolipidaemic5), two are anlibiotics. and one is an immunosuppressant.
Antibiotics
In I'>l an;hof 1942.Anne Shcafe "'tiller was dying from a streptococcal infcction. Her
tcmpcruture npproache d 10TF and she was delirious. O\'~r the course of a month. the
334
. 24.1 A historic phologrJ ph of the fo-st patient cured by peniciRin, with Alexander F1emng,
Fig.24.2 A scanning electron micrograph of Tolypoc/adium niveum, the iU!1gU5 that produces
C)fl"::losporin (from Borel, 1983).
....
338
CIL~PTF:R TWE~TY-FOUR
ated. And treatmenlS for rheumatoid arthritis were an approved goal at Sandoz. Thus was
cyclosporine serenJipilously soncd from the trash-heap of biochemical history.
The structure of cyclosporinc was detennined in 1976. II was a cyclopeptide made
up of 1I amino acids. one of which. alpha amil"lO butyric acid. was new. Tolypodadiwn
";"cum has since ~n shown to produce no fewer than 2S different cyclosporins. all with
II amino acids, and usually differing from each oth~ r in only one amino acid, but none is
as pharmacologically active as Cyclosporin A. known as CyclQsporine.
Most early immunosuppressive drugs acted by bl(X;king mitosis in all ce lls. This
prevented rejection of organs, but interfered with normal replacement of rapidly dividing
bone marrow an d intestinal cells. causing severe diarrhoea and anaemia. Cyclosporine
was foond to be highly selective in its action, interfering little if at all with bone marrow
and gut lining. Cyc1osporinc was found to selectively inhibit divi sion o f lymphocyte,.
mainly T- helpcr cells. by inhibiting: the mitogenic triggers but not mitosis i~lf. It is not
toxic to lymphocytcs. since its effect is reversible, an d it suppresses some kinds of chronic
inflammation. It was effecthe on all mammals tested, and appeared to have no serious
side effects. Thtrc were no further barriers to its use in humans.
Onct: it was in ..... idesp read clinical usc. it was found that cyclosporinc docs in fac t
cause some kidney damage. but this is now minimized or avoided by using lower doses of
cydosporine in conjunction with the stcroid. prednisone. It must also be taken for an
indefinite period, be(;ause the immunosupprcssi ve effect ceases once the drug is discontinued. Nevertheless. because of the selective nature of ilS effect. cyclosporine is un
doubtedly the best immunosuppressant yet discovered, and is the treatment of choice
fol!owing almost all org1m transplants. By 1996,200,000 transplant recipients were usillg
it daily. and the numb.>r is undoubtedly much higher now.
Its potential for the t("eatment of many autoimmune distases, induding juvenile
di~betes. multiple sclerosis, myastheni~ gravis, aplastic anaemia. Addisons disease. systemic lupus erythematosus , rheumatoid arthritis and psoriasis. is stilJ being explored.
In 1996. it was discovered that Tolypoc/(Idium (iliflaw m) nivClIm. the produccr of
Cyclosporine. was the anamorph of Cordyccps SUb.Tcssilis (ClavicipitaJes. Ascomycetes).
Another species of Cordyceps has subsequently also been found to have II Tolypocladwm
anamorph.
The search for other useful m<:t.::lbolites goes on. In Britain, the Xenova Group was
esublished in 1987 to isolate new fungi and bacteria. and SCfeeIl them for useful OOffijXlunds.
This orgQnization has o,"er 30 dise:lSi'-specifk screens, and can carry out over I million test~
per year. The succ<:ss rate is 10'>\. estimattd at one useful compound for every 10.lJ((1 to
lOOJXXl organisms $l;reened. Thus far, we have onty identified , much less isolated. about
IOO,!XX) fungi of un estimated world total of 1.5 million. So I think we may count 011 the fungi
for quite a fcw pleasant surprises Oler the com ing decades. or even ccnturies.
For many yeatS.. type I diabetics have had to inject themselves with inSlllin in order
to control their deficiency disease. Scien tists have long sough t an alternative to this
uoplea;ant ritual. and now they may finally have found an 81lSWer: the first substance that
mimics the effect of in~ulin in reducing blood sugar levels, yet can be taken by mouth
without serious side effects. This substance is produced by a fungus that originally grew
on a kaf in a rain-fures! in Africa. For reasons of industrial secrecy, (he name orme fuogus
has not yet b<:en released. but if this discovery pans out. that name may soon be up there
in lights along with PeniciWum. the producer o f penicillin. and Tolyp(}dadillm. the producer of cyelosporine. Type 2 diabetics. who do produce insulin but arc insensitive to it,
may also be helped by this class of compollnd,. which may dn;unwent their insulin
illsellsitivily. At presem. type 2 d~betics take a variety of oml medications in a somewhat
~ UFPECeg'
~8IBLl OTcCA
Enzymes
Fungi ~crete(that is. produce and telea~) a variety of enzymes into their surround
ings in order to digC5t food or to dJsso!l'e their way through solid substrates. Fungal
enzymes that have been industrially exploiled include amylases. imertaStS. proteases.
pectinases, lipases and ccll ulases.
Aillylase brings about the hydrolysis of starch to dextrin an d sugars, and is used in
the preparation of adhesives and sizings. and to clarify fruit juices. Im'erlase catalyses the
hydroly.~is of sucrose to glucose and fructose. an d is used in candy-making and in the
preparat ion of syrups that will not crystallize. Proleases 3re usually mixtu res of enzymes
th at break down proteins. PrOioelytic enzymes are used in the softening of leather. to
clarify beer. to make liquid glues. and as stain-removers in detergentS. Pecti nase is 11sed to
clarify fruit juices. and 10 accelerate the tetting of !lax (the liberation of the fibres from the
siems) preparatory to the making of linen. Li pase hydrolyzes lipids to glycerol and falty
acids, Lip;lsc from Rhitop"s is used to improve the flavour of some processed foods. and
10 boost Ihe cleaning action of detergents. Glucose o.udase oxidizes gll.lCose to gluconic
aeid: it removes glucose from eggs before they are dried. and oxygen from canned foods.
soft drinks and beer. II is also used in making test papers for use by diabetics. This
enzyme is produced by "arious species of Aspergillus ami Penicillium.
Ccllulases hydrolyze cellulose to cellobiose. and are used in food processing. TIley
aT( usually derived from Trichodenlla.
Alpha-gala ctosidase, derived from Aspergilllls niger. is thc active ingredient of
"Beuno" a product designed 10 prevent flatulence when beans or brassicas are eaten.
~lany people simply can't metabolize th e galactose in the se foods. which is then fermented by bacteria in Ihe gut. "Beano" breaks down the galactose and so prevents the
cmoorrnssing accumulation of gas ... to read more. go 10;
http://w.."w.vibr.mt-health.com/.hJ torecataloglglossarylinfolakpharma.bea no.ht ml
Apparently. the company also sells a T-sh!rt featuring the logo "All Quiet on the
Westcm Front" (presumably witll apologies to Erich Maria Remarque).
Mycologist.
Further Reading
Borel. 1.F. (1983) Cyclosporine: historical perspectives. Pp 3 13 in B.D. Kah an (Ed.)
Cyclosporine: biol ogi cal activity and cl inical applications. TransplDn ta tion Pro
ceedings 15: 1983, Supplement L
Borel , J.F and Z.L. Kis (1991) The di scovery and developmen t of ~ycl 05porine
(Sandimmune). Tra nsplantatio n Proceed ings 23: l867 - 187~.
Langley. D. (1997) Exploiting the fungi: novel leads to new medicines. Mycol ngl st 11:
165 167.
Mounter. lean ( 1997) Dyeing with Fungi. Mycologist 11: ! 75 and back eo\er.
Ric~ . Miriam C. (1980) ~'1us h rooms for Color ( 2nd Edition). Mad River Press.
Tribe. H.T. ( 1998)Thediscovery and deveiopmentofCyclosporin. Mycologist 12: 20-22.
Sources of Illustrations
Fronlispiecc:after C.& D. Hughes. Nalioll3i Geographic. January 198] I Flg.I.lafler
PauerSOn & Sogin 19921 Fig. 1.2 Globe & Mail 12 July 1999 1 Fig. 2.1 after Koevenig in
AJcJlopoulos 1962 1 Fig. 2.2 after Golder in Margulis & Schwanz 1988 f Fig. 2.3 after
Golder in Margulis & Schwartz 19881 FiS 2.4 afler Mes:wly in Margulis & Sch wartz
1988/ Fig. 2.5 L. Tilncy I Fig. 2.6 after Cooney. Baff & Barstow 1985 and Barr 19911 Fig.
2.1A:after Ban pers.comm.: B: aflcrWebster 1980; C: after Karling 1977; Dc after Sparrow
1960 and Whisler 1978/ Fig. 2.8 after Webster 1980 and Fuller 1978/ Fig. 2.9A,8: afttr
Webster 1980: C: after Mueller & Loeffler 1976: 0: after Hughes 1971 and Webster 1980
f Fig. 2.10.8: afler Smith 19381 Fig. 2.11 after Alexopoulos \9621 Fig. 2.1 2 after
Alellopoulos 19621 Fig. 2.13 after Alexopoulos 1962 1 Fig. 3.1: afte r,Ingold 19731 Fig.
3.2: afler Hawksworth, Sutlon & Ainsworth 19831 Fig. 3.3A-D: after O'Donnell 19781
Fig. 3.4B: after Webster 1980/ Fig. 3.5A: after Webster 1980; B: after O'DonnellI979: C:
after Benjamin 1958; 0: after Benjamin 1959 1 Fig. 3.6A: after Jensen 1969; B,C: after
Buller 1934; D. F: after Webster 1970; E: after Rees 1932 {Fig. 3.7 from Benjamin 1979 in
Kendric k 1979/Fig. 4.2: after Comer 19291 Fig. 4.SA-D: after Cole & Samson 19791 Fig.
4.7A-C: aft.!r Cole & Samson 19791 Fig. 4.8A-C: after Cole & Samson 1979. Carmichael
1971 and Matsushima 19711 Fig. 4.9A: after Smith 1938; B: after Webster 19791 Fig.
4.12: after Muell er & Loeffler 19761 Fig. 4.13A: after Scage!, Bandoni et 0.1. 1969; B: after
Ames 1961; 0: after Berlese 190~ 1 Fig. 4.14A-E: after Webster 19801 Fig. 4.15 from
Sam uels & Rossman 1979' Fig. 4.16: after Pirozynski 1Fig. 4.17 1-0: after DiCosmo.!"og
Raj & Kendrick 19841 Fig. 4.18B,C: after Smith 1938; D. F after Tulasne & Tulasne 1865
I Fig. 4.198: afterTulasne 1865; E: after Royle 19781 Fig. 4.20: from Cumlh 19841 Fig.
4.22: after Thaxter 1896 f Fig. 4.23: after Pirozynski 1967 & MueHer & von AJx 19621
Fig. 5. 1 e: after Brocker & Butler 1963; D: after Butler & Bracker 1970 f Fig. 5.2: after
Gaeumann & Dodge 19281 Fig. 5. 3 aftcr 1>10ney 19981 Fig. 5.4B: after Oberwinkler 1982
1 Fig. S.5 A : after Eriksson 1973; C.D: after Pomerleau 1980; G : after Seagel, Bandoni et
a1. 19691 (o'g. 5.6 afte r Hudson 19861 Fig. 5.7B,C: after Pomerleau 1980: E-G: afta
1. . loore-Landeeker 1972 1 Fig. 5.8A-E: after Obcrwinkler 1977 / Fig. 5.9A : after Brodie
195 1: D-F: after Dring 1973' Fig. 5. 10: after Smith 1938' Fig. 5. IIA: after Couch 1931:
B-E: after ot>erwinkler 1981 ' Fig. 5.12: after Seagel, Bandoni et al. 19691 Fig. 6.1: after
von Arx 19801 Fig. 6.2A.D-F: after von Arx 1979: B: after \'on Arx 1970; C: afler Cole &
NOL:lwa 198 11 Fig. 7.I B-D: after Brodo 198 1 / Fig. 8. IA: after Bourke 1969; B: after
Bourke 19641 Fig. 8.2A.C,D: after Cole & Samson 1979: B: :"ICIer Benjamin 19591 Fig.
8.3: after Webster 19801 Fig. 8.4: after Blumer 1933 {Fig. 8.5: after Buller 19241 Fig. 10.1
after 1.R.Aistl Figs. 10.4. 10.5: after Berka & Bamet! 19891 Fig.II.I: after Buller / Fig.
11.2 from Kendrick & Burges 19621 Figs.I I.S. 11.6: after Michaelides & Kendrick 1982
1 Fig. I 1.7: afler De:"lcon 19841 Fig.12.l: afterCruiekshank. Stewart & Waslic 19821 Fig.
12.2A: after Plam Prote>:tion DivisiOIl lei: B: after Coffey 19751 Fig.1 2.3A: after James
1971 ; B: after Large & Doling 19631 Fig.15.l: after Barron 19801 Fig. I5.2: after Barron
1977 1 Fig.1S.3: after Barron 19871 Fig.15.4: afte r Barron 19771 Fig.15.5: after Barron
19771 Fig.15.6: after Barron 198 11 Fig.15.7A.C:after Barron 1977: B: after Barron 1981
1 Fig. 16. 1: after Balra & Batra 1967/Fig.16.2: after Balra & Batra 19671 Fig.16.3: after
Dixon 19831 Fig.17.4: afterTrap~ & Schenck 19821 Fig. 21.1 A: after Samson. Hoekstra
& van Oorschot 198 1; B: afler Booth 1971 ; e: after Raper & Fenne ll 1965: D: after
BametlI960: E: after Ellis 1971: H: after Ellis 19711 Fig.12.1: after Pomerleau 19801
Fig. 22.2B-0 : after Pomerleau 1980; E: after LineoR" & Mitchel 1977 1 Fig. 24.1 Associated Press 19451 Fig. 2~.2 from Borel 1983.
341
/J.i!i,
UFI'i! CC~
Glossary
ABSCISSION:
"p"~l;WI.
as of <onHlia from a
conidiophor~ .
produced by Coelomyce'es,
ofle n subcuticular Or subepiderm.l (i n "0" libue).
ACROPETAL: ~ribu chains of conidi. in which
the young' conidium is l! the tip o f the chaiR;
pattern of apical ,'oWlh.
ACTIVE TRA."SPORT: the pumping of a sub$ .. "".
krOs.. 3 cdlu!..- "",mbr.o. from a point of lowe,
cOtIccnltalion 10 one of h'ghe, co"".n(ralioR;
~quir ""O'iY_
ADAPTIVE E/',' ZYME: s El'OZYME.
ho.l.
AERO-AQUATIC fUNGI: pond -;nllabili", fungi
producing <llboral. floaling pro!""u! ,,-hiob are
"n hand 10 col""i~. aUI~mn-5I'H:J I<a,-~ .... they bll
inlo the waler. lh~n 'eoodilion' them in """ana<rob ic condition. It the bottom of Ihe pond (cf,
AMPIIIB TOUS fungi) .
AEROBIC rcquirin, free oxygen for re.pir.,ion .
AE ROBIOLOGY:
Itudy of fungal (.nd Ol"er)
PCClP>lIul in th" ~tmo>ph"N:.
AF~TOXI,, : virulenl toxin produced by the
Hypbomyttt. A${Hr,Ww flonu and A. poro."ic~
a'O,.in8 "" food.,ull. up, "ulo: bi,bly oattine--
'b"
senko
AGAR: phyco<olloid produ"c~ by the ,ed . 1,0,
Gelidium ; ",ed to .olidify cullur. m<;di. u<ed in
mycology and t>'c'erioloIlY'
AGARIC: gill. Or tubebearin, mu,hroom of the
orde r Allarie.I", (Holeb"idiomyc"te')
AIDS: Acquired Immune Deficiency Syndrome. an
ultimalely fa 1 cOrtdilion produced ..1>00 a virus
demoy. the T
of Ihc body"s ,mmulI< $y5I<m;
AIDS pali~n":ore ,"~cked ."d $Orne,im.. killed by
oppor1u"i"ic fungi.
ALGAE i,ing ... ALGA): unicellular or ,impl<:
multicellular orll""i,m' wilh chlorophyll. lackins Ih.
mullkell"l ...'" organ, typic,,1 of plants. Compri ...
le"eul phyla from Ihreo Kin gdom5--Chrorni<t,.
?I.ntae and Eubacteria
ALIMENTARY TOXIC ALEUKIA (ATA): a
mycOtoxicosi, ~.used by T! !OJ'n (q.v_) which
bllrd many people in Russi. duriog and .ftn World
War IIAL KALOIDS : "i'fO,on.eonIOining o'll,nie
con'poun<i5 producod by planl" phy,iologioally
&Clive in ,ert<brot.. ; m.ny hae a biller t",te .nd
.<orne are poi,onou$.
ALLANTOID: ~au'>G~ih.pe d ,
ALLELE: one of tho two or mare altem.,i,'e "atel
or 0 Ilene th. , occupy \he Ume "",ilion ( locus) on
homolo,ou. chromosomes! alleleo arc separated from
e.c~ othef ., mei.ws.
""U,
oj"".
'+.
343
'",a'
th.,
p[(~luced
CLOSSARY 345
AUXI:-.-S, plan! rrowth bormo""', 10m' In:
by ~clomycO[Thi~ol funsi.
AUXOTROPH, biOChemical mu""l d<fiden, for
0"'" Of mOO! SUbs,o:>ees, it ",m pow otI nUn,mal
medium onl~ if it ho, I>cen supplemented "'\In II><",
pfoduo~d
'UmHI""""
AXENIC: de<crit;.eo col>dition in ",hid! .n
alon . wi,h no other org :tnj.ms
(h<><l )'mbion", 0< pan.itu) pre","! .... in 'uen;e
or~.n i.m f'OW$
cultu,,'_
AZYGOS PQRES: o.>;lram' lricai <PO'u of $Orne
VA~I
b."
..,.,my._
liv;,,~
BIOTROPHIC:
In ill,inu", WOCI.tlon-w'!h ," orlt)pl",m.
BIPOLAR : (I) de",rib< y.",,,, of beleroth. l1i.m
in .. h,eh .. ~u.l comp.!ibililY i5 ronHolled by many
dille ... nt . 1101.. which occur inSI .. locul (d_
TETRAi'OLAR); (2) descnbo!s )'''''' in which
budd;n~ OCCllrs II npposire end< of ,he 'OOl: u" or
the <ell. by per.urrenl prolifera,ion: the)' Ire blaSlic,
ltInellidic.
Of.~nis.m.
,,MI.
."""'g
e.,.
an o"anlsm.
CAROT E.'iOID5 : f4t.""luble p',men" including
e.'ot ..... (l.n"", and o .a"ge ) a nd unthophyll.
()dlow).
CATA80LlC: ok.cnOO m... b<:tlic cl>cmie.1
""octiO<1, "",ulllni in tlte bre.~do ...'n of complex
material, and tl1. ,.I"se of eneriY in Ihe menb<:tlic
p'''''.!' (d, ANABOLIC).
CATIOI.. : pOliti.'.ly eh.tJed tOR.
CELL: unit of prolopl.,m conto;nini a function.1
jI:~n"me and ofle. encl"'e(] by 1'01.11.
CELLULASE; .n .nZ)'mO IhO! con de8 d.
cellulose: a cellulol~tlc en'ym .
CELLU LOSE : pfindp.1 pol)lIcchoridc of pl.nt
"oil ",.11.; a p<,lym., of Illu~ose: ",all . "f Domycetel
.rc p.rtl) composed of , .Imll u~t.nee c.llcd
fung.1 cdlul,,.
.=c'=
lSOoma
t:pichl~:
Y""P''')
CHRO~!ATIO: one of tbe two d>ught<t '''.n<l$ of
duplic:ned chromosom. which .~ joined by Ingle
een"omore.
CH ROMATOGRAPIIY: ..,parat;"" technique
"h;<h u ..... the diff.~ntj.1 r.lles of diftuslO<1 of
different
of molec~"" in gas (OC). hq~,d
(HPLC). 0<1 p.1PCf, and In thin la~..,rs of silic:u<: on
,lass. ah.minnm or plastic pl''''s (l1.C). Now mIlCh
~sed in t'el>cnolo,y.
CHROMOBLASTOMYCOSIS : fWlg.1 din d'''''iIC
of hnmaJl. czw>cd by .peeic. of Phi<lWphcfU
(Hypbomycele.).
.ize.
~ UFPE-CCB
~ BIBL IO TECA
GLOSSARY 3-17
CONIDlOOE.'iESIS , tl>e ptOC:U$ by ,.-hkl>
ir>di"idual conidia rJeo,'dOp: Me aI$o: ACROPETAL,
ANNELUDIC. ARTHRIC. BASIPETAL. BLASTIC.
PH1AliOIC, Rf:."TROORE.SSIVE. SYMPODIAL.
SY;\,CHRONOUS, THALlIC,
CON1DlOOENOUS: l iving rise to conidia.
CON1DIO\ IA (pI. CON!D10:-IATA), .ny
muhihyph.l S1Juctu,~ produoinl conidi . e.g.
iynnem.I.!. sporodoclt.ial. Icel'l~l.,.. 01 p}'cnid;.1
conidioma,a.
CONIDIOPHORE.: a speci. lized hyplLa, simple OJ
Ih~m .
bu""hro,
on ...-bieh conidia are formed.
CLE1STOTHECIAL AscmlA
(CLEISTOTHECruM): l<I ascoml ...hicb i< closed II
CONIDIUM (pI. CONIDIA): a nOR' motile lun,al
malurity; lhe uJlilunk~~e but frequently e ... ne_n,
milOlipotC noc fonned ;nside a sponolium; typical of
asci "'" ofieD 'pl><rical l!Id l I ' not ammged in aft
dibryomycotan anamorphs.
hymenium; characterlslic of Euroual ...
CONJUGATION : tl>< kind of Mxual fusion of
CLONING: produdnll or!.nilm~ .n of " 'ruch
"'malic ceU, ,een in ZYIO"')'Ce l.'; an adapt.tion 10
con .. in copie, of Ihe "'nle gene: the d",ired ~en. is
the .b.. nce of mC>!ilo g.m~I~J .
.. moved from tho dono!. in~nod into a ,'<<lor
CONSTITUTIVE ENZYME : sec ENZYME (ef.
(usually a plasmid). 1M vOCiOl' is rn.ed to transform a ADAPT IVE ENZYME).
I>o!I C\l1t~re. then !bose hosu .. bich ha,'e Lo.I:cn up
COPRIN; a
amino Kid fouoo in 1M aKlri,.
thc ",,,,,,or "'" "'Ir:c'i~ely t uhured.
Coprin .... al""","ntarlwcr, ilS effeclJ mimic "''''''' of
CLUB FUl'GI: "",mbe., of family Cb,-ario~
an!abu .. (q.Y_)
(Aph yllopoonrJcs: Basidiom YC~'~5).
COPROPHILOUS FUNGI: fun,i !ivi", o n du",;
COCCID10IDO~IYCOS IS : deep-... ted m)~i,
indnde mony zy;omycel<=$. ascom)tttc. and
Clu~d by Couidioidu /"''''/1;' (Hyphom~'''o!.s):
bllidlomyc<!es.
common in dry S.W. of U,S .A,
CORAL FUl'GI: Hymcnom)'cete. with highly
CODON: sequence of three adj,cent n"deo1idu (in branch~d, uptight b.sidion1. t . ulu.l!y an,ing (rom
DNA or RNA) that form !he coM for. , ini l. amino ~he l:,ou nd; rome membe r< of Ihe family
,
. dd; a seq uence of ~odQn ""cille' [he amino acids CI"';uiaccac (Aph)'llophoulel. Holoh"id iom),cetu).
[h~1 constitu", a pt<>ltin ,
CORTI NA: (of ag"';cl) I ftl~m.nlou, or weblike
COElOMYCETES: anamorp/lic (mito,l""i<) fungi p.mi:tl Y~il cO"erinK ,he m.lu.e ,ms; 'yp;cal of the
in "hieb!he conidi. or. pro<I'ltl ..,i~hio 0 j)(111"i,. ,uoty.bro...-n.,pured In)'Irrh;ul ,~nu, Coni"", i" .
s[/UCturc, an ac:n>'ulu Or p)'cnidial ~""id;"r:r.a.
CROSSWALLS : SEPTA (q.v.)
COEI'OCYTlC : dcscribe1 IIluhinudc.u h~' pII:u;
CROSSIl'G-OVER (CROSSOVER): c1chan,e of
Iac:king o...... -wons. as In m~n )' .ygom)""''''' .
I~Mlic malerial betw.en ,wo homol"gou< chrom ....
COEN ZYME, an o<,o n1o moleoule. which playl an some, by the \>rCa~.ge lnd joinin, of si"el
ace.nary role io ... ymc-calalYl<d proce".,. of,.n
chTomMid" occurs durins meio,;, .
by .ctin!! a, donor or a~.ptor of $ub'Wlee
CROZIER, in """ogenous hy ph.e, ~ tminol hoo~
in,'oh'td in Ihe ruction; ATP and NAD are "omrnon
1n which conjugal. " uctoa, di.i~;on ~aI:<s pllee j,,'1
coo n.)"me,.
prior ,n nuclear fus;on. mei ... i,. and _u. forma,ion.
COFACTOR: n""-plO!~;n compon<n'h) ""eded by
CRUCIATElY-SEPTATE: describe. ,ho basrdi. of
on Cll)'mt: 10 be functroR>I; $01Ile cofx tor. or. me'al 0Jdc. nemeUalu (Ph ... ,mobasidiomyce'es) ",hich
ions. 0,1><", an:: coeozymu (q.~,) .
:m: divided imo foo, mOl'e or I~~s cq\l:tl ""'" by
COLLARETfE: the oflt,; n"in, "'~n of. phlahdc: .tnka!
",Us.
dl5lal to the conidioaeno." I""" .
CRUSTOSE: rjo""nbe' lichen lh.lIu< thaI adheres
COLONY: a di ,cn:: lt mycelium o( a ("np" ofle"
d ....1), ,,, the <ubmate (often rock ) (d . FOliOSE.
derived from. , inll ie ~p!l<e,
FRUT!COSE, SQUAMUlO SE. LEPRO SE).
COLUMELLA: continu~Iion of the m)k inlQ 'ho
CRYPTIC: ineon'picuO\ls 01 hidden.
hnd of a 'f>Orep,odu~inl otru<!ure; fo"n~ in
CRYPTOCOCCOS1S, a SY$lemk mycosis caused by
'poTangia of Mucoraceae (ZYl:Q m)'Ce1 e, ),
b.. idiomycelO .... )c:u.t. C'ypltXtXr"J "r%rman.
CO~IPATIBLE: oble 10 ~nd~'iO ~xual fu,iOfl. of
(holon"lOlph: Filobasidltlla ntn/''''''G''').
opposite ma.iog .ypu.
CRY PTOGAM: a pl.n,. funs .... Of proIoclistart lhal
CO~IPLETE MEDIUM: .. e MEDlL''''Propal.te! by .pores "'IM( th.ln by .. 1$ (fun,i.
CO~lI'OUND ASCOMA: l ldc<>rnorpbic kJc!irtCa'
bTyoph~'les. fe"tI) .
lion i"""!pOrnin, se"er.110 many distincl .SCOm.1I'
CUP FUNGUS : a 'discom)'ccte', any OS<Xlmycele
on 01 in I .in,1e ..,\letu ... as in the Clniti?i!al<."
"" ith .n open. ,halt"w, (UPUbl' ap<nl><ci.t a,eom.:
CONDITIONING: Ihe p<OCCs> by which fungi mu, l hotc!goneou. ifoupina t-eo'u$' the ..ci may he
unitunic,tc opere"lalo. unilunicale inopercut'le. or in
en<yrnically soften up ,ublU"" like dead te3l'es
t>:fore the detriti.OnlUS an i m~l. oon .a1 Ih<m.
m~ny lieh<n . bi lUniclle,
COt-.1 D1A , ..e CONIDIU~L.
CUTICLE: waxy 01' f~"y I'YeT on o uter w.n of
CONIDIAT10;\': 'h~ Pl"oc:e" of p.-odurin!conidil . eptdenn.1 crlls.
.at.
c..,.,-..
.1,...
.1,.
U'.
p.ur
G LOSSARY' 349
DUAL ORGIu-':!Sl>lS: organi ..... which invll;lbly
C<lS;st of lWO ;nt.rd.pcrxl<DI symbionls ...... Hch ......
In fact. most pllnls _ II"" du:ll or multiple
organisms bocau.. of !heir iDtim.UO' :associalion willi
endO- or ecto-rny<:orrbi ..... fuDJI_ The .... karyolK: cdl
is widely bdic,..,d 10 hove arisen .. a multiple
symbiosis.
DUTCH EL.1.1 DISEASE.: a u.uilly fatll disc1l$C of
lhe American .1m "ee. UIm ... americana. cau$Cd by
Ophi<>SIOIIkI ulmi (Ophio"omaul..: Ascomycetel):
th~ fun,ul il Ipre.d by b,,"-bcede vector.
EA R Fl./NG!: the ~.la tinau . edible wsidiomall of
lit. Auricul~rillcl.
reI.
.bo..
""ttl,
....
GLOSSARr 351
GOL.Ci1 BODY/APPARATUS: .~ i~lI*'dlul",
UOLOCARPIC : with thollu. becoming entirely
conncted iflto ,cprodltCtiv< .Iruel""," (cf.
or,anelle Wt ~on.isa <>f flat. di<e_shape<J vesicles
<>I'ltn fooning tubules al the ed,." sites ol KC\lmul.o. EUCARPIC)_
tiOll and syntt\nis of cdl product ... <_g.. "'111 tmot~ri.l:
HOLO~IORPH:-:tll ..... nif~IU'lons of .ltl>Ol~pe: ifl
ift pllnts. somotim.. called DlcrYOSOMES.
a fungus !hi. frcqUCfttly muns 0"" or I1IOf"e
GRANUlOMA: I oodulo of finn ti .. u. formed u lnamorphs plu, tekomorph.
reKtiOft to ~hronk irrit.,iOft.
HOl>10 l.OGOUS: (1) ,,i ,h IlIe ... me eV01"bOll.')"
os;,i"
'hough oow oflen diff~.ent in form and/or
GRIS EOFU LVIN: I cblorinc--containinll In,ifuD",1
fu".,tiOlt; (2) (of ch,-omoSortlu) bearinl IC~' for tbe
antibiotic from P.n lcilli~m griuDfulvwm. and P.
.arne cll=>ttc ...
nigrlc~nJ: h... bn "5ed "' I sy'temic f\lnllkid~
I,ain't plant pa,hogens and or. ll y .~ain .. derm.to
HO~jOTHALUC: describe. fungi in ..... hicb si ngle
phyte infectio ns in animab .nd human,.
m.in can unde,uh se~ual fCproducI;on: .. If
GYROMITRIN: I he.t-Iabile, c&rcinOlLenio. ec l1ul~1 compalihle (ef. HTEROTHALUC).
to xin prod uced by G)'TI)m;'ra ucul. nla (tht fal"
HOl>IOZYGOUS: h., inK iden t,cal allele... tho
Mor.l): b,.."'" down to mo nomethylhydrlline
Sam. 10<:,,' on homolo,ou. ch,omo",me .
( MM H). "'hicb h II"" extremely toxic.
1l0:-iEY F1.JNG US: the agaric. "'mlli/aria ",t Uta.
HALLUCINOGEN: (>S )'eboa<tive .u~.nco whkh which is prnlSiti.: <>II. trees Inc! c... oes serious "",I
C'''it. disuubaroces or pert:CpUoD. ' .,. I"'ilocybin.
M .
HAMANATTO: In Oriental food obtai""d b)'
HOR~!oKES: usuolly peptide. or steroid<. "bicb
fmncntin. whole soybeans with 1u~'liUMJ "'l';:o:I~:
.... p.-oo""ed in """ pan of In or,an;<m and lrijiCT
IMKIIo (MllaY';I): tac-.i (Philippine.); 'u '"
'pedfic recb""" in lI. cl .... bcn"'.
(China)
HOST: an orzani"" on or in which ~i'k.
HAPLOID: hovinJ: I .i.[lIe .. , of cl\ron>o5orneS
nccrl}(ropbie Of .ymbioric funllus II,...
(oflCn denOl<d by 'n).
HY DROl.YSIS: 'p~uing of a molK"1o in,,, twO
HAIaIO NET' th. int.".1I ul", hyphal network
pans by .:odd ing hyd,ollen and h)'droxyl ion, deri,'cd
f,mned by an eetomyc<NThizal fun;u. in Ihe lu,f.o~ f.um wa ter.
I~)".rs of. fOO l ; lhe effeeti" e in,erface bet.....en lhe
HYM ENIUM (pl. _ HYME1' )A): fenile I.)"u in
,ymboin l'.
fu ngi; bea" asci in a,comOI ba.idia in b~s idi om.'.,
HAUSTOR 1UI>I (pI. _ HAUSTORIA), in parasitio
co niJia in pycni di, or acol'ulL
fun;i . peci.li"~d absO<"[>l ive 'lructUI~ th.t
HYMEI'OMYC ETES: Holobas ldiomy<tt .. "'ith
pcnctwts .nd JlaI'''' food from tho nOSl cell.
hln'~njum ex po",d at m'l~rit). b.sidiospot .. , hot
HEART ROT: decay of the inMr """"" of trees.
off (cf. GAS TERO~I YCETES ).
c,us<'d by ba' ldiomycetes.
HYPERPARASITE:
orsanism .hot "",lI'W."
f1ELlCOSPORE.: a .pore ..'nich cu,,'cs thKIllh
e,lber .noIher par.l.<i,e. or an o'",nhm clouly ",bled
tnI)t"O than ISO". and often through .....ral comple'e
10 itself.
B)m. ooillng in t..-o Of three di"""nsions.
HYPERSENS ITIVITY: Ihc cOt\d";OIl ,n .. rueh Ihe
tlEMTIC: """,,~rnin! the Ii' ... "" in HEPATOMA ho<t ti ... ue dies II the point of anlCk b)' a p"'holl~ D.
(1"'0' cance.).
.., !h:lt the inf""lion doc. noI sp;ad.
HERBICIDE: suMlanc. which kill, pl~nll.
HYPERTROPHY: e. co;'c 01 abnormal Srow,b.
HETEROECIOUS: describe_,
funll' " 'hleh nwl
HYPHA (pI. = HYPHAE): 11>0 lubo,il., ."hJleclu,-,]
IwO bosts t<.> oomplete the ir life cyck (cf. AUTOE
module of ,[mosl all funii. ii, ...11 chili"""s in
eum)"cotan fungi. ce llul",," in oomyc., ...
CIOUS).
HET ERO KARYOTIC : conta ining g<ne tic.ll y
IlYPHOCHYT RIO~!Y COTA : Phylum of
Jissimit .. n"ctei.
Ch,omi, t. n f" n ~ i wi,h anl odo,l)" "nina8.11oIe
z""'pores: hence. h)"phochylrid .
HETEROT HAL LlC : doo,ibe. fungi in whicn t",,
g"o.neall) distincl bul compatibk mycelia muSI l!let t
I!YP HO~IYCETES: con ,di.l morphs ( mo,tly
bef"", it~uIl reproduction can ta~e pIa (d.
...:ornyeet"" . ..,me ba.idiOm)IO"') p<oducinil
1I0,\ IOTHALLlC)_
.
cxposed conidi<>pho,.. . nO! enclosed in any
prOl<cti,c <truelure (cr. COELO~IYCETS).
HETEROTROPHIC: "nable to dcri~e ~nerlY from
p!Io'Oli)nthc,i. or from inOTgMk chemin! ",ac!iOlls.
HYf'(X;EOUS: describe. fun,t whkh fNil
under:,-ound_
AUTOTROPHIC
HIITEROZYOOUS: having 1",0 different allelos II
IBOTENIC ACID: a """1"""Hle of "'m."ma
Ihe ,""'" locus on homolog"''' ch",mo"'mes .
",,,-,CDria; chMlle, to n."scimo!. I h.lluctnOilen.
"hen Ihe b.,Hliomal. a,.. Jried.
HISTOPLAS~ IOSIS: d<cp-.c~,ed mycooiJ of
humans o.".cd by lIiswpli15ma mp..
J.\ I ~1lil"OS UPPRESSM"': I subs"n. such"" the
(lIyphu",)"C.I~'): co mmon in 'he Mi"i .. ippi V~ney
("DJal me,abolite. cydospo<in . (pro<luced by Ih.
hyphom}c cl<. Tolyptx:l~d;"," ";vurn) "hi~h
l!Ol.OIlASIDIO~IYCETES: B .. idiomyect .. in
pacti.lIy or compk'dy $uppresse$ lh.: im",u.e
"'hieh Ih~ ha,idia <m 001 . ubdi,id, d b)" ""pia (d.
sySlem; used to r'O"cnt rejection of Ir:tnspl.nt<d
?HRA(j~10B ASlDIOMYCETES).
a'g. n,.
HOLOBAS 1J)I UM (pI. ~ HOLOBASIDIA) :
II'GEST: 10 ob!,in f<>t>d by ,nllulfing ;t (I<"c
moiosporaniium "'" tli"ide<! by ,cP" ..... bleh USUan)
PHAGOTRO PHIC! (cr. OS~10TROPHIC).
lli.~. rise 10 4 <~ogenou, ba.idiosp"re. (ef.
PHRAGMOBASIOIU M)_
.n
<0"
cr.
,I",,,,,,
orl"ism.
L"OPERCULATE: deocribes .ponngia, esp. some
u"itunic"e
which h.. no sped .h"d op<tcu
lum or ~ap lhat open. 10 permil,pore di>ohargc (ct.
OPERCULATE).
L"TERCALARY: among or bel"'"" ""II.; ref.,.. to
such thini' as non. pi<.1 ehlam)"do,por in m,ny
funKi .
11'..RA.\IATR1CA L SPOkES: .nodIor name f~r tit.
".,ide, produc.d in h~1 fools by most
endu my. olfhi u l fun,i .
IDS : I clwied lIom Of VOUP of nom .
IRItADIAT(ON: .xp<ure to >om< form of rld" nl
en e'sr
ISlD1A: ';mpl. or braIIcbed prowbel2Ilee. of tl-..
eorteX in liohens. which may bre.k o ff and
form of v.8d.,ive Prop'iul .
ISOGAMY: (u.ioa o f morpItolopcally i<knliul
.""i.
u.. ....
LEUCOCYTES : ..-hite (non-humoglobin<o ",ain ;ni) blood cell' o f m ony Iypes. incl ud ing
ph.g)~ic MAC ROPHAGES IJId anllbodyprod""ini LYMPHOCYTES.
LICHEN, a du . 1 O!"g3I1i<m in which. fung .. ,
(u,uall)' an A.. onlYOctt) maintains a glttn
or a
cyanobacterium capl ;"~ "'itbin iu tb.llu. ;n l
symb",u, ~ha, approaehes bal~"ccd pan<iti,m.
LIGNIN: a polytn~r of phenylp rop anoid unill lhat
i, an important cOfl.lilll<nt of .."OOd: very ,..,"stanl 10
biodclraej'lion. bOI dCI....:led by many b,a.idi
~.meln .
omyc.,,, .
JACKINA BOX ASCI : i ee flm]~lCATE.
UPlDS: moJul c<MIl. in;ng a f.lI)" acid ... ith
JELLY FUNG I: ,,ood!nh.bitin, \).nidiom)"e.,,,
10Dl! hydlocarbom (""in. e.! _. tri&i)"ccride. (Clter of ~
w illo I.linO<l. ""idiom.t. : 0nI ....: Tremen.i< .
fOlly odd plus ,Iy.erol). pho<pbohpid! ( lriilyceride
A" ri cu tar; .Iel (Phra ~mob" idi 0 mJ'c. to<);
conl.ining 2 fatty acid chain nd pho,phO\~ as ~
D .crymycetalU (llo lobuidiomyc<t .. ).
polar .'oup).
KARYOGAMY: the f...,on of ICxuatly C()tn""tj~le
LlRELLATE: Ion\: >od thio.
""1'1o,d Rucki.
LOCULI'. : .<por . cont>ining cav ity. ~;p_ on.
KARYOLOGY: the study o f ,he behaviour of n;:,I.i $Ccotld.rily deve lOj><d wjlhin a pscudolbeciai
in .uh,yot~ $.
..eoma. or in !he basi<..~om.au of LyeopoonhlU Ind
KATSUOBt:SHI: a Jall~nc<c fcrm.<n,M food:
Scierodotm.t.I...
cooked bonilO r"h i, f. rm ented by ,,",ptr8U1ru
LOC US (pI. a LOCh: ( I) a 'pecific localion; (1) the
! I" ....~. unt;1 d,y: the product is Ih".d into ribbor..
"",ilion on a chron"'50tne occupied by a panicular
~nd used for thvOllri ns other rood .
.e"..
often u~ .)"nonymoully ...ith I .....
kb: kdob.<cI. an abbre"i>lion (a; 1000 ba>c p';",
LSD: LYSERGIC ACID DIETHYL A!>IlDE. 0
of DNA
powerful hallo>cinogen derived from Clavictps
KfRATll'\ : the prot.in lIo.t i. the ...-'lin eompoc=t
IIderOli .
of ' k'n. bair. r..,he", and horn .
LYOPHILIZATION: f,~t z. dr)'ins, lcchn iq ue
KERAT]Io; OPIULlC: capab le of deoomp<"in;
u..d to pr ...,,'e fun;:.! cultu re, in llale of
k.min. as are ""'ny of Ihc fungi th .. eause supcrij.".pcnckd 'Dim~lioR_
.i,1 my=. in man; ote DERMATOPHYTES.
M ACROC YCLJC: de .critx.. ru>l fung; ,,-hieh
RlIo;GWORM , TINEA.
pmduce III ~ d.:ve lopm.nl~1 . 1'lIu -buidio'port ,.
K.I:."TJA P; an Olie.tal fermented food: h,d"n",i,~
'pc,malia t<iospo,es. uredlni<><pol'e . and
ooy uu"": bl..::t <QYbeans or. ferm.~led for 2J d.:Iys 1eii""porel fd_ l>UCROCYCUC).
b)' i1s~rgillu$ o,,,ac; tho! toOl or K."hup and
M ACROIo;U TRIENTS; ino, ,ni < chemic.1 eltmen ts
Calsup .
r~qu i,ed in Jarlle .mour.,. for pl~nl 01' rU"g .1 ~ ,owlb.
KETOCONAZOLE ( N.. oral): In ,nlifun,.l
t_~_ . nitro!cn. C'rbon. pot."ium. calelum. pho.pm..
,u"ibioti~
..S. rn.,n~'i"m. and '''iphur_
KI C'lE TOS O.\IE: hogal ho<Iy: Jclf'ropli c01ing
MA CROSCOPI C: big enough 10 be ,""on b)' tho
"',anelle al .he ba>c of n~dlum. similar til a
naked ey .
""nino le.
MAG1CMUSHROO~IS: 1)pic. lIy. h.llucino\:enKr",G DOM : Ih. higlle" t"xonomic ""ellory. of
cootain,ns 'p<dts of I"iloc}'b~. but .110 'pp, of
... hkh 7 Of< CUft. ntty ~cog nil<d (A"h .. ~l<ria.
G)""'nllpUus. P~n~~"lw. CORoc),be. and .lmGltiM
EubQcl,ri,. Chrorru>la. PIOIO ..... EumycOla. Plan,":. ltIu.c"ri~ .
Anlmal,a) : run, i con""utc tile Eum) """ a nd 2
~I'\ l'i:-' !TOL polyhyd". alcohol. often fou nd a.
Ph}'I. in K'n ,dom Ch romi"._
'lo,aye compound in col"'ph ic my"otrhizal
II,.
1ICt.,
"",.,:e
m.n(I~ I.
G LOSSARY 353
MAl\'TLE: a compact layer of hypba nclO'ing
short fe.der rool, of eClomvcorrhizol plan,,:
connectM to Ihe Hartig net 'on the in'ide, and to the
e~I"m.tri"al hyphae on Ihe out.ide: adS as ,ink for
nulrion",
MASTIGONEMES: bait llke proces,es on the
,u,bcc of tin",,] f1a~ejJa; flimmer<,
MATSU-TAKE: Trichoicmw. matsulak~; on
important edibl. fungu, in Japan: grows in ""weialion with pine.
MEDIUM, culture : a ,ub"lan~ Or solu!ion for the
cui!ure of microorgani,m" DEFINED MED!U )"I~of
" prescribed compo,ition, u.<d for determinin~ the
biochemical capabilities of me or~Jni'm, e,g ..
~uxo"oph,; CO:'>IPLETE MEDIUM......,ontaining all
nutrient' r"'luired for growth: MINIMAL MEDIUM_thc simples! chemically defined medium On
o.'hich !he wild type (prototroph) of a 'peci.. will
irow and which must be bupplemented by One Or
more 'pecifLC ,ub",nc", fm the grow,h of ,uxotrophic mutants derived from !be wild Wpe;
SELECTIVE MEDI UM : medium containing certain
chemical cumponem, whleh reS!ricl the llrowth of
<omo microorgani,ms but encuur.gc. the gro""lh of
others.
MEIOSIS: roduotion divi,ion, a diploid nudeu,
produced (usually) ~ haploid nucle i by 2 succ~"ive
nudear divisions in which the chromo,ome number
i, hl,eJ front diploid (2n) to haploid (n). and
gonetic ,egrei ation .nd T<combina,ion occur.
l<IEIOSPORAAGlUM (pl _ .. MEIOSPOR.'\..;"G1 ,\): 1
,po"ngium wilhin which meio,i. occur> before
'poro formation (e.g .. ba,idium. asc",): produces
meio,poTC,. (cL MlTOSPORANGlUM).
MEIXNER TEST, for am'loxins: (I) expr<s' nuid
from agaric onW newsprint. (2) dry, (3) add a drop
of co"centmted hydrochloric .cid. (4) blue <olom
developing in 1-20 mins. indicate, pn:<cnte of
am. !oxin. higher In-el< produce colour s(}CIoer.
MELZER'S REAGEt>.'T: u",d!o dic it amyloid or
dextrinoid r"aNion< in 'pores, asci. hymenial ti"uc,.
ctc.; chloral hyd ..1e: 100 .,;. potassium iodide: 5g,
iodine: 1,5 g. di"i llcd water: [00 mi..
!>.IEROSPORAKGIUM (pI. ~ MEROSPORAr-<GIA):
(of Z)"goml'cet~s) a cylindr ic.l outgrowth from tbe
,,,o11en end of. 'porangiophore in which a chainlike series of .porangiospores i, gene,"U)' produced,
MESOPHII.1C: de,cribe, organi,ms which grow at
temperature, between 10-40 0 C (opt, 2(j3S ' C) (cf.
PSYCI!ROPH 1L1C, THERMOPHILIC) ,
,\ l ESOZOIC: the geological era compri,inz the
TriM,i c. Jura.,ic aEtd Crolaceou, period (225.M
million YeJ" befor< p~sont) .
ldETABOI.ISM: the ,urn or all chemical proce ss",
occurring within a Jiving cell or org"ni,m: PRIMARY
~!ETABOI.IS~l _ mct,bolibm as.sociat<d with !ho
normal m. in tenanc nd growth of the organism;
SECOr-<OARY ),.IET,\BOLlSM - proc.,,", which
use p,imory molaoolites a,-ailahle after growth h..
ceased. producini ,ub"a"".. wilh no known role in
primary metaholi'm.
\IETA!<IORPHOSIS: a dr~m~tic reorganil>lion
le ading to a change in appearance. as i" the
developm~ntal ~hangc rrom catcrp ill ar lat', to
huttcrfly.
METIJLAE: ,peci.l cell' at tho al"'X of a conidiophore which ,upport phbJld." "-, in man) ,pecies of
Penicillium. L'ptograpnium .
m\:: <ce MILLIGRAM.
MlCROBOPY: cenul", organelle bounded by a
single mcmb,ane, and contai"ing en2)'m~s; derind
from endoplasmic reticulum,
MICROCYCLlC: dc<cribc, m,1 fungi in which
,orne "a~ .. of the life cycle are b}pO-<sed (cf.
l<IACROCYCLlC).
MICR(J(;RAM: one-millionth of. l!".m: wrine" a<
.]l~' .
MICRON; one thousandth of a mi llimetre or one.
millionth of a metre: wrinen .. ]lm ' .
MICROrORES : ex!remely narrow con nee live<
pcnetraling the sep<a of some myedial yeas!" .g.
Gtotrichuln .
nm.
MULTI POLAR: d es<ri~1 y.~.t. in ,,"'hleh each
... ece .. i~. blasuc """idium artse, from a diff.f.nt
NECROSIS. de.,h of "ells or
point 0<1 "'.. mo!lter cell.
t-.'ECROTROPH: "" organism IIw tillt Ii" .... of
MUSCARDL'lO DISEASES: dbe .., of cerui n
l'ving I>o..s by r<louin. IOX'nJ. then li~u
IOprobical1y on the d.ad li .. uu,
in,",,!>. esp. lil~""onns. caus<d by hypl>omycele,;
GREEN MUSCARDINE-M.ra ,hj,ium anisoplia.;
NEMATOOES: thr dworml or round""om,,;
WHITE ML'SCARDl"E-B,Qu"uia bauldl'la;
member> of Phyl~m N.malod~. p,eudocoelom:ot.
YELLOW !>1t:SCARDlNE-Pauj/"",yces /",inaSfU. ""L1ZOa. 10.000 spp.; common in ooil, decayini
)!.1USCAR1:"E: to . ic qu.tem.f)' ammo nium
orS.nic malle, and as paras'le> af planto and animal .
compoond f<'llnd in ,pedes of C/i'.,.;ylH and
NEPHROPATHY: ~id"ey dam'g. . .used b )'
I"",), be; ~ au . o< P<'''P iut; 0 nl. rivat iOn .Iaery mation
m)'coto ~i" i.
I}'ndlome.
"'EUROTOXIN : a toxin which affcc .. the ne"""",
MUSCI),IOL: hallgcino,enic d~ri .. ative of
,yotem.
ibotenie xid; fo"",-"d in "-manila "",s~lI,ill when
nm: ,ee NASOMETRE.
basidion .. t. are dried.
NO BLE ROT: a cond ilion in wh ic~ tM. mu uld
MUSHROO.\ f: fle,hy b.,idion,a. usunlly , .. 1, 1 B(JI,}'i. 810wl o n o,crripe 11131>"'. A ,i ch. '''Ut,
and wilh ~ap (pilou,) boIroeath ...-hi"" a:iII. or fle,hy
e' p<n.i,'e
i. m:>de in IJNn qu:utulic. from >lIeh
rubol, an: eo,"<od with or lintd with ,be hymc:nium:
i""P<' (Saut~mcs. Tnx:hn&e<renu.lese. 8OU~ti
edible Of poi"'.""'; .... AGARIC, BOLETE.
"'ine).
J.!UTAGES : an .gen' th.1 inc",.>eo! the mutation
NO~ IEN CLATUR E : the ",ming of fungi i,
gO" em ed by the lntemo<ional C<><le of Botanical
.\IUTATJOS : , perm.roent eh'nge in acne.
Nom.nclolul. u adoptcd by e~ch Intern~t ;on~1
.\!uTA:">T mutal"" gent, Of an o,&ani,m c ... ryin, flotanic:>1 Coollre": any proposal. ' 0 change the
gene thOle IllS u<l<k' IOfte a mU(:l.ion; may boI
Code are publ"h"". dcba1<d, and .'otcd on at 'illCh
b<ochemlCal. fe"" <nt.tion. re.i.unce. supp"',sor.
Cong'....'. If moce than Oftc name ~., beeR appli.d
phl"iololl i~. I , in n>lure.
!O fun!u,. tt>< rules h.:lp dedde which il !he pmp<'
one.
The rul.s 01.., ~I!ow ",!",rOl. bioomial. for
~!UTUALlS.\!: kind of Ilmbio<;il in ",hich boIh
.n>morph
and holo",,,,ph .
or all part n ,,,-,n from th. usocialion. ~ . .
NOl'.TARGET ORGANISMS: organisms found
m}co"hiu .
",uh
or ne .... th .... t-eing I.n:atcd ....-j,h a ehe:mieal or
~I YCAKGIA: 'p<ci . l
of .ome "'ood biologicol co"'rol a.,:cnt: il il import.nt 1hal [hese
inh.b it in8 1><<11... nd ...-ood.w",p. in which th.y
ago nt, ha>'c
little .ffcct u possib le on rIOn.target
carry th.i, I)mbioli" "nlblosi. fun!:u, .
organi,ms.
~!YCELl L'~! (pI. _ MYCELIA): ooll""e term for
NUCLEAR CAP: a m_ of Rl'iA and ri~
h~'pb...,. the \.;.tJli~" th.llo. of a fU"lIu, e.eluding
near
the .udeu. in ",me
org.n, of '(XINI ",on Of scleroti .
NUCLEOLUS : or~"n. ll. found in the nud. u, of
~ I YCETO)IES: pouche. al the beainning of lhe
midgut in .n obii d toeI., in " hieh thei, end",ymbi eub.ryo,j" ~,II.; co mposed mainl y of !ibo,omal RNA
in ,he: procell of being tran""ibed from f,om
"'"' ,-<:I$tl ""0 '!Of,d.
multiple ~opi. s of ,RNA i.nes.
)!'IYC081 0~T me fu",.1 p.utne, tn a symbiotic
NUCLEOTlOE: a ,inlll~ Un;' of nucle ic acid.
f<lalian.hip <m},crmiza or lichert).
comjXI""J
of. pho'ph.le . fh'. -carbun .ufj" (.ithe,
~!YCOI! ER SICIDE: a pr<p. rtion of pn )' topa!ho.
ribose or deo~)'ribo<cJ . , nd a purine Or p~'rimidin.,
go.,i, funii ""d 10 kil l ..... d .
NUCLEUS: a lJ><'Ci.li~ed booh wi,hin lbe cuh,y
.\IYCOI"SECTIClDE: pre!",,,,,i,,,, of
"'ie cell bounded b)' a do uble "",mbr:one and
.ntomop.>.tho~n'c funit us<d 10 kill i"S<<:I~
cORtainmll lhe: chromO"'RleS.
~IYCOLOGY: lhe >Iud)' or fungi.
NYSTATIN : an .n' ifu"g31 " ntibiollc dcr;"ed from
~IYCOPARASITE : fvniu! "'h ieh .n><1:1 other
SIU(!tomyas M "TSt'i. "<cd to treat condidi ~!i' .
;ungi (>omem"'" <.lled HYPER PARASITE)
OBLIGATE: in,ori.bly f",,"11 in ~nic~l;lr
~IYCOPH"'GOLS: .~tinl fun,i.
.itll.,,,iOll' u,u~JJy u=;l in rer~,ence 10 <><g,ni."" th,l
mus< li,e tR 'nlim~'~ """",;",ion ,.im a l;" ini bost
(ct. fAC ULTATIVE. OPPORTUN!STIC).
Ii""".
,.i""
,,1<.
0<1'.'
.<
""'''pore'.
~ UFPE-CCB
~ 8 I BLIOTEC'"
many
Pr~iIIi"",
Ibm.,.
Ie".')'
..",'.
PAPILLA: a
au~iliat)"
nippl.-lik~
ulension . on Ihe
-~
.ha,
'0
"'0
358 FWfH
KlNGDO~'1
"""sr.,
,u.
.'OJ.
"""0$.
R",,"'a
.n
,h.
""".i"
Ii"""
at"""
;"<0<15.
TRICHOTHECENES:
mycoto~ins
(Jci'1"'nes) of
,,.It
GLOSSARY 361
UNTVERSAL VEIL: m.mbn~ '",ally tnclosinl
WITCHES' BROO~lS: "'.. ~ outero",th.
KIm. y<>~ng al";' buidiom3la (as in Alll3nill): I n", (proliferali<>ns) of the ,,"lI<:hc. of woody plan ..
ruP'ur. it remains .. th< ,,,In ltO<lnd b.!<: of lhe
.ause<! by mites. viruse . Ole . ond fungi, up. ru>l
stipe. and "fltD 01.0 .. "a1tS O<l the cap (d.
funC i .
PARTIAL VEIL).
WORO)\,"N BODIES: twQ ,mall 'pheri<lI objec ..
L1R..E D!.l>lIOSPORES: tbe d,k.ryotio 'summet
'hOI ,it. one On e",h ,ide , ncar the PO'" of the
.pore,' of Undinal . which Ipad 11>0 fungus from a,comycet. ""p'um_
plan. Itl plant of Ill<' primOS}" hosi during the ~toWinS
XEROTOLERA"'"T: able to grow unde, dry
.. aSOn.
con dilion, .
VAS!: vts;cuilr arbu",ular myconniul
XYLEM: b,nir..d wl.e''''''''ducliog lim'. in
(ndomycorrbi " l).
vlscular plan ...
VASOCONSTRlCT10N. coni!ricti(lfl of blood
XYLOSE: a pcnto... '"II"', C,H 100,. found in Ihe
, tSStl'
cen w.n, nf basidiomyC.tH.
VECTOR : an OlpIIi.m ...-hicll cansciou,ly or
YEASTS : fu ...; ""bi<h in many CUe' Ire \Ulicellu_
UIle<ln>dOOily ~idJ. in the dispersal of .""ther,
1.,-. t hough . om . p,oduce hyphae; mo", yca." arc
dip't"" flin are voclOf> fo, J ,inkh<>ffil,
anm>ot;>h.; thoeir cell.... conidia. and they multiply
VEGETABLE CATERPlLLAR: mummifi~
by viriOUI l<inds of conidlosenesi . Some can
produce .,ei. 00010 can fOlm basidia, and lOme
lcpjdopt<",n Ian... from which ari.e. lilt '!IOmalic
lttonmorph of a ' ped of Cordyctpj (Cla,'idpj.al. " 3ppear 10 be aumorphic holomorphs-----<:nlirc1y
asexual.
Ascomyce,.s).
ZEARAL ENONE: I myeoto,in produced by
VEIL: ,.. """"'lJLUS (pan,"t 'til), VOLVA
(univer,,! veil).
fu'a,;um graminfarum (hoJomorph, Gibb",tlla
:fI"fI); tbe caUSe of oestrogenic syOO'om( (vulVESICLE: (I) .mlll. iOlnlccllul .... membnntIIQvagin;,il and infertility) in pig .
bo\Indcd ~c in ..-hkb S""',"nces are ulnsporte<l or
ZOOSPORANGlA (,in,. '" ZOQSPORANQIUM):
,'"rod; (2) ,"'oUen. lipid -filled <elb produ<od Inside
';><><all,i. within ..-hich lOOSpores (llaxeUale spor.,)
plaot fOOlS by mOSt u<lomyoocrhi""l fUDgi (""".declop,
limu called in<r:Utllluk. 1 sporc.).
VES ICtiLAR -ARJ! tlSCULAR MYCORRHl i;AS,
ZOOSPORES; n~~ejj"c. motile.
JporeJ.
cndomy<ouhi,.ti; pbn' ",,'" colooi.cd by rnutu~li.
ZYGQ!>IYCOTA: Pbylum of """ fungi: fa" -
lie fungi of the Glomal .. (some of "'hkh do not
Z"'''''w" l<!m:llri al. I,.-,ely oapcooic fun,i with 00
produce vU;Cle.)
mo,ile oello: produce >lJIo,po.ao,ia by f~,ion of
",....1Iy simil", ,.,.,<1.10,;,; aloo uc . ual sponln,ia
VIRl.'l E-,"CE: tht dege Of " ".. u,. of J>alhoie (onlain;n~ I to m.o)" ....,..motil. '1"',<,<, and bo,ne
nielIY.
on simpte to comple., Spora niiophore,: gen~ ,all y
VOLVA, " .boa'" '["Qund Ihe b.", of the "ipol in
>Om :;:>rKS, "'I'. Ihe poi>OnOll' A"",niM: "ruin. of called tygomyc.[e,.
tM univOf$01 ~eil.
ZYQOSPORANQIUM: [I>e tclltomorph of the
VO!>!lTOXIN, 4o.oxyni,!lenol, (ri<hothecenc; ,.ycomycete" a U'U3Ily ,h, cl::-wallcd. of.. n
",ented. mUltinucleate rUling .po/angium formed
I m)'c<>(oxin pn><l"".d by f~SIlrium ,rdPlincDrum
(H)pllomytnJ: e,p. in barley and winter ...-!!tal; ""s follo .... iol """'tomo'" of ,ametatt,1I ariJ;"I from
compatible myed;. (in het<fo<h~nic sr<o;el) Or from
In .",etk efrcct OIl Ih."""k,
the sam. mycelium (in IIomoth.llic 'pecies).
WATER ACTJYITY (Iw): e~I""."'" the n ail"ble
ZYGOTE: a diploid cell or protOpl:tSt flXTTlCd as a
",.ltr in Julrnte IS dcc""al fractIon of !be
",.ult
of fu.ion of two h.ploid nucki due;ng ."~uat
amount presc", "'ben the ,ub.tm. il in .~uilibrium
repwduclion; ~y,o'" of.. " become ,eui"1I 'pores.
with' "'I0,,,,.d >tmosphere (In c~uilib<i"m ,etatl>-.
humidity of ~< "'''''00 !he ,uhslrale ""01IS th:at the but ult;m3tcly ,"mliDate 10 prod .... ei!he, l diploid
gcncrottOO (..cry few fun,L mony algae. ,II higher
sub.tr>.1t hilS '... te, 4<"ti~iIY of 0 _70),
pl.nB) or unde'go mei";i, .lId. fulio"-;o, (hi,
WATER ,\IOL=LDS : membc", of 'M Order
genetic recomhi.l!ion. lee,ubliJ.l\ she h.ploid pbue_
S.prokgnill.. (Oomyccte.),
WHIPLASH FLAQELLUM' I flagellum with I
,hlt"t (d_ TI",SEL !Iagdl um)
WHITE ROT: 3 ",000 rot prod=d by b""di ,
omYCe1e hat Can de;rade bo.h cellulO><: .nd Jignin _
WHITE RUST: diJ.tase of crudfe .. ClU.e<l b)'
AlbI!.;nac ... (P:rortO.por>.les: Oomycou)_
WU.T: I ptl"! diIC''', ea"~ b~ s~c;", or
I',,,,dllium and Fu.!arjum (Hyphomyo.'e'J.
chllmcri>ct! by IOil of turgidity Ind toll.pst of
to, .
"'.'"11
"m.,
.m()<)'"
Ic.\~s.
INDEX
~ .8S
,tilt [SO
Xlscissioo l&yer W7
At.sldu. 331
n.
Acan
189. 190
A,'("o1P<"'" III
45. 46
o<ctlldth)'d. 322
""elate 14S
acclyl glucosamin< 144
as,
31:1. 336
139. UJ
adaplatioru 203
Addi$Oll', ~_ 3lS
iIdbesi\o'C Innches 2+1
odhesive hyphk
2~
'"
.:..cia
105. 214
x",,,,ports 105
aerobic JOO
.. r(l-aqU~lk lungi 194 -196
A......f'M"" 116
.n"OXilH'Or.l.min,tt<I food< J.01
a!latoxin. 52. 14j, JOt. 305-307
"'M 149
Agaric""... 89
Ai.nca~1 Ill.. 89. 168
as"""""
m.
c~.uc.. 'lO
"'Jariew! 83. 89. 92. lil9. 233.
1?9. 280. 2SS. 289. 317
'~")~
92
AIDS 3.lO. 331. 332
.lrbomc miIOi!',,"'''''' 21. 127
.i ,bornol 'por", jJ!j.- 14Q
[38
56
AlbII,in;lC'tx 2(;
m.
322
83
alp 4, II. IS. 118. JlII.
IZ~
Aliet!t 219
oJ""".'>!)
21 3.
320
'"
88
c"unlin~
apIIrr~is
apltkls 290
Am.:uri.. 88. SII. 92. 262, 265. 266. aphid>. bto<:oouol 225
279. 287. 317. 318. 319. 323
apbtodisiacs 283
Am.on.itatue 92
Aph)-lIop/101"alt1 83, 114. 114. 116,
amaniUEHoIer,," Oros"""ila n I
Ap<.>sporil\Q 74
amanitinl 92. 93. I~S. 319
lUTU.toxiDi_ amallili
"1'10,,;, ."""mi. 338
amt>;rnobjlc 221
apoplasti" 218
. mbfosia IUngi 2~
Aposlrtljuri<1 601
Ambr<JJio/la 255
.j><>Ihcci .1 as<:<>m .1a 41. 42. 55 .
. m<m<pon:.< 45. 46
Ii-t, 1111. 120
Ame. lUI 289
.ppel\d;l~. 60. 68. 69. 132
..-nino acid! 142. 145
apple juice 312
"""",bac 248, 249, 290
.ppl. . .ob 74. 203. 2 16. 2 19. 234
"""",bojd 10
oppr=-ori. 123.
269
amphibious fIIngi 191
Apron 219
r.mphiplds 290
arbu<Cul .. 36. 268. 269
amphJd:Wlism 16\1
Arbu/W: 277
amphoteric'n B 158. 332. JJ7
Arr<VI8.I~II" 96
amylase 339. 340
A",IIoebactcri. I. 2. 124
amyloid 55. 59. 87. 96
AnlUlltJricJ 88. W. 95. 162. 179.
A",}"/qsur~..m 84. 255
180. 21), 21 4 . 233. 234. 287
..... ,""phic hoIoIl""pN 44. 18. 170 Ann""", 121
on.mo.pllI 31, Jl . JJ. 34. 35. 43. Althoni.I., 122
44.4553. 48. '"'- 55. 57. 59. Anhroascu. 114
60.61, 62.63. 64. 65. 67. 68 . AnhmbotryJ 185. 187. 243. 24-1.
69.70. 71 ,72. 74.75.78. 79.
245. 2-16. 2-1 8
83. &4, 86. 9~. 106, 113. II~. "'nhrodm"" 69. 70. 327
115. 11 6 (Iable). IW. 121,
Anhroderrn.t:oc.ae 6\1
122. 118. 131. 148, 155. 156. arthros><>d. 189, 190
110. 185. 186. 189. 190. 191. al1m', ron~ 86
192. WJ. 207. 208. 209. 110. A>ch<,...",ja n~ . 226
~II. 216. 219. 220. 226
o><:i ~. 41. 4 2, 54. 55. 58. 60. 104.
(tabk:). 232 (~bld. 233. 234.
66. 71. 113. 130. 163.
m.
Icropnal 47. 48
Ae/ln""''''''' 2%
Actinomyc~
271.289, 296.
301. 302.
~. 310. 311. 312. 313. 3:19.
alllllw """'" 84
""nul", 88. SII
:IOObiid b<-<tlu :m
Anub\l:IC 322
.ntasont<m 186
..,tlIcr imUI 107. 21J5
anth.ridi~ 17, l l . 2S
anlheridiol 156
. nth.r.lcno..: 20~
of ~ln! 213
Anlnu.-u.s 100. 101
ilIlbbiooii 33$
""'ibiOli<! 334)37
res;'I",,",.
10 336
("
r' '.'
"
an:hac_ 121
bituni<ale 4), 7). 121
d"..-.:ID(l<I1CnI 80
kinds of 41. 4). IX!
'_'''>OOIill8 131
pr<XOI<lntc..te 43. 55. 71
1hoot,nt: mtC~ "ni,m 13(1
~nilUnica", 42
uiruoli<aleino~'.1UIIote 43. 511. 121
unilunio".GpeI"CulaIC 4 2. 43
Ascobo l""e"" 57
IIscoho/us 41 . 5 5. 57. 157. 168.
135. 186
"'"""ion"", hypb;te 40. ~ I
OS<"OJ:onium 41
AKoUUa 15$
~dra<.... 116
~ 40. 41. 60. 64. 70. 71.
72. 119. 121. 132
e<>nlpound. 57. 59. 60. 6(i
A>comyc.,es 41:1.77
mprop~il<>u,
t 84
Aocomywtina 40-77
<"phore 42.11 4,115
Asc"phyll"", 124
40. 42. 5-1. 55 . 60.
64.70,
121. 130-133. 208
buddinll ~
CQlo\Ir .e .. 163
number 59. 65. 67. 121
p<lfr,ni IX!
.""us!,"'.,
;~
,,
INDEX' 363
Jymmetrically mounted 135.
Am'" IIll
,"oxu.1 rtprOd"cli<>o>---->.<~
'"
4~.
8o.Jilim/>rla 48.
anamorph,
185
"" '" IU
8o.J~ll>Jpqm
Bwi 22~
~3)1
As~
71 .
m.
&lradoh},riWllt
'"""" >9,
Bolbitiaooae
Bl)'cor 219
Ba)'le\Ot1 219
Bayoud fUf\l:uJ 20'2
Beano 339
97
B<>ItUndl... 2S6
Bol..in~' 91
Bol.,,,, 89. 96. 265. 266. 267.
27S. 28~. 289. 3 17
Bombard", 1~7
278
<)2
8oJb;ri... 92
16
AJ,""'....
4')
bii,bl 205
bli>\., ru~ 106. 21"
Bl"" 21')
blue ~ 313
blue mould Q/ td:>acw 25. 201
B""daft,t>o'i~
87
AT ... 308
boles 237
ATBI 7. 198
ATP 1. 1~3
Arrlcqrdyupf 2-12
AM 251
beh>viou:' 252
beetle<
B<>Iry<>lin", 63
B"oe",.,keu.. 194
blnd,n, hypllae 86. 117
blnd"ffd, lri<:tcOIIu-ot 22')
binorniol 4
Latin 5
bi""ides 217
bio<:onU'Ql-IU biological COfl trol
biological (0lI1rol 214, 222-238.
IknJ~(e
lknom~l
A.sr",,,,"'i~ria ')7
'U!O)I;I.vin~
1$0
,,ado ll9
neP~~'QS>3thy
311
discharge 31. 32
balll~""pon:
I~.
Iwbmy
!OJ
'"
,,_~
nI
<)9,
"';ne
223
of
lable
101. 103.
8i'f>(JuliQ 65
Bitenanol 219
bi"<f oo lele <)7
BilUtUCal"" 73
bif\lnic~\e asci H
bl.ck knOl. of cllerry 74
black to! of 5"'~ potato 2lJ
bbck $pOI of lQ3eS 65. 213
blackbrny. biooonuol 227
Blaus/", 32. 33. 118
bl1slK: 46. ~1. 48. SO. In
blUllc:~ 47 . .ut, 6-t. 113.
'"
perelll1ia! 3-1
90. 1331}6
Rl. 135
bcanoh ina
149
12
B"vo 220
8 "",;c~
Brldge<>pOrw
7. 86
budding ! 12
BulIOrio 6j
bunt 108
buntO! 211
B)'s.ochl"",}",
m . .102
cabbase 12
cadmium 289
caloium propiona le 221. JOO
c~du m "",bale 300
CaloplaCOl
120
C~I()J">fM
100
Ca/l."ri" 100
c.lKe,
Ihoer lOj. 306
0C'S0p/I.>,~.1
307. 308
)la.
bl~1io5)'mpodi. , ~8.
'"
ch.....:lcri,lic. 78
B.,idiomy<'ulLo, 78- I 11
b:Is,diosport! .10. 8(). 82. 83. 87.
2t).I
blal\;c"'u-ogn:"iv. "9. 50
..s.
-l.'). 50. 73
bl""ic-pcmtfTCl\' ~9, 50. 113
blll\1e1'hillidic -Ill. " 9. 50, 11 3.
63.
Cane>!Cn 112
canker 205. 21". 2~
Canthan:Uacc.. 8-1.
C",,'ha'el/u/a 9S
Canlhartllu. 8S. 286
<>p-.ICt pi leus
blb6c-anneUidic
>onpour.d 8S
l"'1e'l 100. 287
as~r rrnmIO.l
09'
barley 106. 21 2
b".uxic ~9. 69
notI'iboolin~
'"a,J"an\ago.
Ollhropodl 223-227.
",
237. lOl
fit""
'"""" '"
uen,c ISO
93lk.an
218
55
A.riJ~alpf"",
254. 255
113
blulic-.ynchrotlQus 47. 4.'1. 86
BI:I.SIOCladi.I.~ 17
J;IMfOlnyuI 114, 3}()
Imstomyrosi~ 330
bl.",1 286
as,
100
C.pnoJi""e~t '"
Captaful 218
C.ptan 2lJ. 218
carbohydr.\'es
earbt>n
dio~id.
1"3
292
262
or;HJJt%>
140;.
I~
'"
311
eaulinow~r
fun!ou 85
cew apple ru.l 219
.. null~' 62. 153. 176. 203. 339,
'"
'"
ccp 285
ccph~l ooi.
120
cep .... lo'ipOrin 146. 336
C~pMl"'rid!UJf! 185
C~""<>ey'lis i'l,
72. 211
~9.
on
,,,
ch<m(>Iui, 126. 2~ 1
ohe rr)" 63
che.,nut bliv>t 62. 182. 201, 212
chicken manuIC 329
chinch bug. bioC:4l.nrol 225
dunn 18, 1 ~3
chilll.oid 59. 65
c hi\l);<.:l.n 143
Chlonnil 11 g
CIrI~TQdl>or;" M
ChlQrophylium 317
chluroplom I
chiOl'Qlh>lunil 2ZO
choke of gr.w.eo 1>7. :!OJ
dwk>lCrul .!Cduc"' ~ <iN,s lJ.1
chromalid< 162. 163
Ch~""I'<,,"i"'n
55
Chr<,miq" 2. 19.
chromistOlIl fungi J~
chrumohl>slOmyeo.is
Ch"""OCT'" 169
ns
Cb)uidloPl)"COI.I
Cit,trfdi"", U
14
Cb)'lrids 14
on:l<rot>ic 19
in rumin."u 19
Ckj~mWcl", 231. l3Ii
~;ICadi"" rhylhms 154
1!Ij
C!awzrio 85
dc'-e1opm.m~
'"
eoo;apbo..",,1C 115
COtIlolhyri"", lJ6
conI:.o 85
co'HIlions. anamorph.
leloomorph 44. 53. 314
-,
2~S.
2-IIi
Copnnac . .. 92
coprine 322
m.
CI(t1."I"'''I',i. 85
de;\Huuing. effect< of 19S
~1.;'tOl.hed.1 osromala 42. 43. 71
ClillxylH 95. 286, 317. JZJ
CIi'opfluJ 94
Clotrlmuok 332
doucl e., 281
club root 12, 13
CnidoriJ 241
Coccidiokh. 329
coccidioidomyrosi. 329
CI>IXOIt'},Ctf 219
CochUo/)oluJ 52
coconut 22S
codhnll n>Oth. biocon1.l'Ol 22S
codoas 142
Coc/OtttC'm)'Ct. 21~. 226
Codomycct<.s
~5
Cocmans,,, 32. 35
oocnocy!to 38
coe,o lu.ion 202
coffee ruSt 107. 20'!
ColiCILO 229
Collembollo 1!9. 14S
CclI",,,rlrl<t= 210. 213. 128.
229. 30l
Collybia lIS
colony 28. 88
C"lrricia 86. 278
Nlumella 32. 33
.-s,
CluWlri"dtlph1<.l 85
CltwlctPJ 58. 65. 60. 2().1 . 213.
304
c~s
CI,,";oce.c 8-1. 8S
157. 21 7. 221
ISoI. 18 S
18S. 186
338
72
ZOI
119
CO!1id~ac
83. 8-1
Cenid"," 277
cO'1;n. 88. 93
Con,nm'ccae 93
Con;NlriNJ 88. 93. 262. 265, 317.
~219
COllllluin.11Il 51
coo"" 221
N}<>tCS
190
Crowdl"J 8S . 286
Cr.bm,h.cI"", 114
cr<p.:s :II lJ 8o<<lo:lal~ 285
Crrpjdcrou 93
CTiniptIlIJ 2n. 236
C""",rrl"", 106. 214.
236
cmp kw.es 216
crop lOtOtloa 210. 211. 215
:m .
common ...""" 5
cro"'pro1c'(tion 235
er=-"...IIJ-sce
'"''''''Dg .....''' <WI. 160. 161. 171
double 164
er.Wer 79. SO
CnKib/u", 100. 169
comp3Tibility 169
clu-omo<orr.. mJPS 163. 166
c~ t. 3. IS9. 16 1. 1&2, COII1Pf1t11r;e I is
'"
ohlin! 48 ..12
hifrardlica1 5
CUIJ,obasitf;"", 211
Chalem ofS,
C/rOTn/)1!iT;a
'"
Ci",jMII~
"pi"
"""PrOCOJ 166
IND EX 365
",,,,lose Iicben> 119. 120
Cl)phQn~"ia 62. 168. 182. 201,
[k,Cl)myce< 82. 83
Dacrymycctal", 82
Difolatan 218
Dih"<rofpcra 2~3
DikaryomJcot,
characteri,tic. 39
m.jo< ",-, a 39
dikaryon 40, 41
dikaryori:ealion 168
dimitic 84-. 86
dimorphic pathosen' 327. 329
Diplocarpcm 65, 213
Dipladi", 255
diploidy 3. 19. 1 ~9. 179
D i ~:>eeoe
116
Dipod.:Jscus oW. 114. 115, 116.
Dip'mt 189
di5COlichens 119. 120
di5<"-,"'
animal 52
",,"ssm.ot 20$
aUI<).-imnlUne ~3. 338
control 207. 209212
eradication 210
forecastin; 205, 211
immunization 210
imroduction 209
Ortan-'pecific 204
plant 52. 200, 213
protection 210
quarantine 206
""istAIKc 172 '
=dling 204
,u",optibility In. 216
, y'temic 204
"'ill 202. 20-l
dj'P""al 73. 126-136
dithiocaro.m.te, 157, 2 13, liS
dilypc 165
Divi,jons (Ph)'la) 1
DNA 'n, 142, 1~9, 174
t=files 180. 18 1
sequencing 179, IgO, 182
n-an,crip,jon 175
doddo,. biocontrol 229
Dodin< 220
dolipore 78. 79, 115
domin"Ilt 159
dormancy 146
donrn'"t 'proy, 218
D:,thidcale, 73. 74
Dougl,", fir 21 ~ . 262
d()wny mildew. 2~, 213, 216, 220
Dr<chsltra 52. 137. 201
Drowphila 160, 290, 121
dry.d, ",tld1e 86
drying 299
d1'al cuitur< 272
dual organi'm' 11 8
Dutch elm distose 71. 131. 201
dy< ' 3-10
ear f"ngu, 102
earl)' blight of potatO 2o.t, 213
e,m ball< 98
earthworm, 189
olo~
184199
of """'rofu,,;; 197
e<."J)nomic, 209
""lOndom),con-hiu. 277
eetom}corrhi",,1 funii
edibility 265
host response 264
inoculum 265, 266
inoculation 268
;rolauon 265
m)"ce\io,l s.tr-.nd formation 26~
pc~i"e",:c 260, 26~
.. locuon criten. 263_266
taxa 261 (!.Wle)
ectomycorrhlzas E6, 88 . 92. 93,
96, 98, 219, 258
d,,"elopmen{ 258 , 263
di,"_ lOsi,"""'e 265
fungal tilU 261 (table)
mill<:r.tl nutririon 264
pH effects 264
plrut, taxa 262 (table), 263
temper:trure effects 2M
to.<icilY offeets 264
water .. Iation, 264
<ctotrophic m),corrhizas 258
Ed.Uaul. 29-+
<dible fungi 265. 279-291
rub 279-280, 316
eel gr,,, II
egg (Phallales) 101
egg', ,poilage 302
Iaplwmyc<f 58, 66. 290
[laphomyce",l., 58
t'/",,",om}'C<, %
Eiy"'u< 65
E.\1 fungi 261
E"'~ricella 71
omphym. 137
EnchytraeidJe 189
o"~.~ge",d
on<rgy
Fi.",Una 289
ft.geJl ~
e'iODIOni"" 31
f1.trJ~ncc
C1~etoI
143. 219
t1goI a1k.oloids 145, JO.I
~ot of ry< 6S, 66, 2().t, 21 3
c'lIDloIinc (,6
eCJ"",miM 66. 31
C1Eoilim M. 303-JOj
339
56, 82
Exob.uilli.les 82
ExobtJsldium 82
exocrine ,l.or>ds 312. 32'3
exocn:ymes 147
exogelKHl' DNA 176177
eXOicnous gene produ"," 340
wphiala 319
e~ti".;tion
farmer '
lu" ~
In
rats 143
fl"orocy~
332
325
G'ON 56, ~7
ecr>enti.... bypbae 86, 87
1$9,
1:<_
17~.
177, 178
ISO, lSI
frui1J, spoilage
Geoilosuc=: 64
G<:ot/osJWtl 64
FuMo 173
G<'O"crn 56, ~7
G<mrichum 50, 11 3, 115 , 11 6.
'"
!CfIll lbeo<y 2N
cumy<:ow> 4
phyl.o of 12
fungid<k1 216221
bc""r.1> of 218. 219, 221
choi"" of 220
formulation of no. 221
,n<>rpn", 216
mode or ",,'ion 137158
orpnk 217
rc~SU\IICC '"
sclcc""" 219
"".ay oohoduk 207, 208, 210,
,poil.S. 302
im!.""
g .. n-o-irolwini)
Gauritrl4 97
frct:zefl 300
frogs 16, 196
F.",."imol 219
fi,h 20
GalmK'Ji>t 92
G.....romy= 81
192. 19J
Gamwokws 97
FunaiOO>. 21 9
Fungiton 332
fungus sna" 290
fil=ioI'l
a -.....
~. I~
tlcsh (agarics) 90
IJes.h of the Go.b 324
me. 34. n. 189, 22~
flU,,","'''OI q~tlC"i()fl 181
gall.midgos 255
pI'1l<WlgU. 17, 18. 3 1,
prn<W 3, 10. 13. 136
gill
90
89, 90
.:<In'eficm 89. 94
!WIll
di".~nt
89. 92,
P=llel 89. 94
!!irolle 286
llieba 98, 100
GIi(H;i/;ilium 237 , 300
GI<W!1porium J.O I
Giorn>o:ear; :nO
Glom3lc.< 36. (key) 27{1. 271
G"""""''''''''''>'''J 62,
.!J6
a:alacl<lsid . .. 339
Gai..IM 93. 317, 318, Jj9
Glomt,,11a 169
Glomus 270, li \. 274, 277
tJIICotI 143
~Iuconic
xid 339
glt>OOSC
I~
GnorMllia 1~5
Gornpt\ldi""".., 91. Z62
m
grid~"" inttrs<cl method 174
Grifola 288
gri,eofulvin 145, 332, 336
growth 146 1SO
decline ph.", 148
exponential phose 14S
lag phase 148
localiution of 148
m.,.,umncnl of 146
rat. 148
' tag.' 146
guanine 142
Guepiniop,i, 83
G"ig""rdja 74
Guilli~rmo",ii~lIa
1 14
GymJWm)w> 96
Gy"",opU"J 93, 317, 325
Gymno.porangjum 106, 2 19
Gyrodonw.~.e
97
G}'rodnn 97
G)'romjlm 57, 283, 317, 31 8, 321
iyromi\Iin
321
Gyrvporu< 97
habitat< 197
hJemo<iialy,i, 320
hacm<lper1u' ion 320
haemorrhagk 'p,dromo J08
halfli fc 21~
haloprogin 332
ham.nauo 295
Hanunjasporo 11 4
Hanser.ula 255
hapluidy 3, 160
Haplog/OJ'" 24\l, 141,
harpoon <ell. 24\l, 2.1 1
Hc'p<nponum 242. 143, 249
Hartig net 258 , 259. 26(1
h.u,,,,ri. 67, 69
h:ud nut 58, 282
h.,nrot 2 14
i><:at 'terililOtion 299
i><:avy m""ls 157. 217, 264. 289
Hebda"", 93, 262. 265, 3 17
hrogehog mll,';hroom 85
He/jca/JaJidj"m 211
Htlic(}c<pMI"m 187
Hdjwaf! 195
btlicospore, 45, 46,
.ctivator 340
Humicola 299
humungou, fu ng"' 88
hyaloh)'phomyco,i, 331
Hydnaaae 84. 85
Hydnangi"m 96
H)'dn~lIum 85 , 340
ilJdn~m 340
Hygrocylu ?~
Hygrophoracea. 'N
Hygrophorop.,i. 97
ilygr()piwru< 94
h)'men i. 55, 64. 84, 103 , 0 9.
lJO. 133
H)'m"11}8~'''F 94. 99. 262
H),meoonl),cetae 81
hy!,",>,",,,,i,,, 229, 231. 233. 237
hypc=n<itive reaction 207
hy!,"nrophy 54. 107, 205
hypcruricacmi. 290
Jam 301
jelly 301
jelly fungi 82. 102,281. 285
juniper W6
juvcnik di.bot<, 338
~ UFPECCB
~ BIBLIOTECA
karyoj.my 105
b1>oOOu, hi 2%
ke""in 69
ket-jap 195
k<1OCC"""Qle 332
ke,'s (id.n,iflCationj
gee,.", of E.ry, iphalc' 68
'0 ~e'n.'" of YAM fungi 270
to Orden of A>comycet 74
. '0
...
10 muWooms 98
10 rum v... mulS lOS
Kicbtlk 130
Kickxellal 32 . 35
kidney _ . 290
KingdoDU I. 2
Klouro 11 4
Lm:tOOacillllJ 29'
wlip,m.. S6. 28S
\.tgd' 292
Ims IS
lipase. 339
"""ulae 48
'"
Lophod~rmill'"
meteOo'<lk>iY
t.,." 96
Latin'
t. ...nl 67. 225
""" "
321
leaf.cunlng ..~u 250. 251 . 252
kaf .IP'" 205. 219, 221, 233
UCONlro S8. 120
l= ~no.... l.s 122
Lndnl<m 26.5. 285. l40
u"",~niero 19 2
unr/Jtuu. 180. 285. 289
Wlio M. 6S
Leoo.ixe"" 65
LeoIi.le. 62
L<pidopleta 66
UptOl" 91. H3. 317
upuw
upmrla l!I
uprtx:}'I:><t 93
1<.....- 1"1>1;", 1W
UpIIJgroph,"," 4.'l, 49
up_i<l 94
L~p'IJ,phluritl 329
l..cprospl.u",/;"tl 156
kUlal lollipop 248
h"wri~ 120. 122
leauce. do"'ny "';kkw 213
louci ne , yoI". ,il 146
9'
u"'''''S~ric....
&9. 1'3
Uu<og<J>r., ')9
u"Npui/llU 135
U:K()SIOm/l 2>6
fr.'emul" 2:0
lil>cl1y cap$ 325
lkl'.:n clIcm"U)' n2
110".,h ,,'" 1!3
309
96
macrocyclic "'sl' 10-1
M""ol.piOl(J 92
Mocrop/roma 2 S5
Madur~lI"
226
M"Ibraw:It~
70.
)24. 325
M./ompJ(J", 173
n.
329
lOS
Micoouol< 332
"rreclS JO.4
Ilroh 262
tarks 290
IignilWts 153
Umnopm1iJ1t 98. 195
Jing..,hj 28S
linka~ dil"'fKe 16'
n.
Mehmc(mlt 58
1ox"1.,. 98. W
12mc1l.., 88
La~g.rman"itl
monoculw",. 200
,"oaobryon 41 . lC)..1
montlm<thylhyJrazinc 321
mooomitK &3. 86
MonOlropil 278
monoIropoid myo:<>IThi1~ 278
M""h.lla 57. 283. Is.!. 318
Mor,bclb;ea<: '1
morel. 57, 197. 283. Z8-t. JI8
mosquilO<'S 225. 226
mollie. cell SO, 69
mould inhibilOrS 221
lNDEX 369
mould< 15. 21. 29, 33. 4]53, 62.
63.71. 74. 97. 137. 13S. 1-10.
173. 2().4, 210. 21S. 233. 237.
153. 294. 29~. 297. 299. 300.
301. 302. 303. 305. 307. 308.
310. lil. 313, 31 .;. 33:). 336
nIOCIkly bread 307
MlV:Or !l~. 128. 156. 186. 301.
Mu~or*l
3l. 33-34
muor 281
sclerosi. 338
mul!ipl~ .yn,bion" 2OO
muscll/'\Jinc ru, ..", 224
muscarine 93, 95, 323
multipl~
muscimol 324
N~bam 218
NADH 1.. 3
on,.jorn 296
Ony,o..a!es 69
N"_wkw4 317
""gamy 17. 19
oogonia 17. 11.
.......w
281
N~/zzi4
OOSOftiol U6
fWW1Il .election 3
"""'" ""
"""'WIt
241
ptm.lOde, 189. 2392lS. 239.
,,,
!>WIlla 100
lin.
mycopl>Jv 279_291
rn)wniuu ckpcnd<ncy f.ocIor
'"
151278
ad"I"'~ 257
arl!w:ulat--= vesiculr~!aJ" myco,rhizas
m}'COfThius
ectOU'Il!>hio-=
e.;{om~
endolrophic-see ""i<ulworbu.=Tor
m}~
~~
TI7
,."';,no=u1 277
l'TIOIIOIr<>pOid 278
oo;rud 27;
my<:t>6<'1
321.333
~allnel\l
IIOn,."c1a,,,,,, 4
non"""'''"cti", rin;.
H.
l32
'"
N",/OC
~lNCtura l
,I/)'xad,,'" 93
my~lmOt~
~lpom)~ct.1
M)'~O$I.hoh
My"'p<yri~m
10
10
10
240. 241
2C)j. 213
Ostron",rph" Il4
o.tio!es 42 . 45. 1;6. 99
56
Otid<.~ue
O",I.""""i~lI~
95
161
o.id;sj,,e
phospho!),I.,;""
"'YllU l.\"tls
nllCleoprotcinl
Pan.rna disease of
n..:1eus
142
I. 159
p"""oXddioidont~c""i~
330
243.
m
'"
203
par.... xualily
301
N)"CIllIi. 95
nUL$
=
"" bioIJophy
oblil'~
~nal'''''.
Paru,'uidiuidu 330
Ny~~'in
1M,
O",ponu 7. 86
NOtIto/"11lS 74
nl>C!elt di,'u.ion 161. 219
nl>Cld~ ocids 1.. 2. 289
oc,troaonk J)"IIlltomc R
m)"~ovilU\e'
71
opponunisli<: "",hog...,! 321. 33-0
Or<~id mywntUz&I 2n
onl<-red lCLnd 160
(>I"eUanin. 322
orpn specifIC dis-o;as.e. 65. 66.
'"
do,o,ifi ...
314
201. 2t
119
ion
180
ovary 204
245.
207
01""""
,,,"bn:odin2
187. 237
107. 20-4.
..... laAa
mycoo.:mci<k 225
mycobion' 118, 257
mycoho,bicid.. 229
my~oins.mi,id<:< 22-<
m)~;t." 31. 61. 62. 67. 'M.
25. 241
Ophi""'()m~to.leJ
mulatilm 3. 172
M~riflUl 100. 101
n.
310-
Oidlod<ndron ~. 51.
Ojd/~m 49, 67. 69. 21). 219
oil. 143
Olpidi"m 14, Ili.
Omploa/ina 121
OmphaW/us 317
onIon di\eil$eJ 107. 210
onions 272
2~;.
2j3.
2~S.
2~1.
2H. 288.
321. ]29
pa ....1hesome 78. 79
P"nndw 120. 122
~ oporei 66. 67
partial 'ei! 88. 93
pani'" dl<pem.l IlS. 136
I';t"~"r 293
I>'<hoi~ni~il)' 202
palulin l12. 113
Pa<illoc~oe 97
P=ill", 97. 264. 265 , 28~. 340
feui"" 317
PeR 179. 180
reach leaf ,"(I $4. 20$. 219
pe""~ scab 219
Phy:on 218
l'IIyl. l. 4. 12
Phyll""linia 68. 69. IJ2
Pt' tnnip<>ria 87
219. 220
Pilob"lus 3 1. 3).:>4. 33, 128. 154. poslzygotic bani... 170
peridiole, 100. t OI
peridium H. 99, 100
perithecw ascomaut 42. 60, 61
perim..:w >qIUSb 16)
P"r",,,spora 20. 25. 20 1. 210
PtrotlOSpornl.. 20. 21. 2.J
Pur",ana 121
PtWl"'" ~9
pc.cici<les 222
1"0(11. 55, 56
Pcztzaceu 5S
Peliules 55
pIIy.iolOC 1421SS
pb)1OaIe,;ins 207
phytOOioM' 258
PhYlophliwl"tt 21. 24 , 126, 127.
128. In 101. 203. 228. 229.
235, 265
ph)'toplani;ton 15
pickles 300
pi,. 310. 311
pikipeUi< 90
pile.. liS, lI', 90
pilm>ge. 305
ru"
pi .... blister
of 106. 214
pi~" mu, hroom 286
, p ine needle. 188
Pipr<>c. phalis Il~. 185. 187
""-- .
Pilhomyces 312
plant breedi., 172. 206, 31 2
plait< di .."", ron,costini 20S
pian, gI1l",tb It&U].at(lr'; 203. 259
plan. patIIoIoJl 200-215
Pwid,-"", 63. 64
290
phUQ/t)'p/tomycosi.
n I
Plt'""'-'" ~
P""if'" 115
Phalla les 100. 10 1
p/toI Loidin. 319
p/taILotoxin. 319
PluJlba 'J'jI, 100, 101
I'h;\I WI 2 I8
p!lam,:< utical. 7. ))2. 334339
Ph.Ili,,", 21 4
p/tenO)U 21 7
pheromone. 11. 131. 156. 169.
Pl3nue 2
pla'mid,I 75. li6. In, 179
pl modi> 10, 13
P/wmodioplwro 12. IJ. H I
Plasmodiop/lorid> 12
P/oBntJpturl. N. ZO, 25, 201, 216
plastics 27
Pluln<S 9.t
P~
228. )(J8
phornopsin 312
ph~"""pore,
46.
liS
poly~etid.'
pl.S!i<h 1
Plto<pom 73, 74
I'Ieo>poroo::t 74
PlelOrotw 247, 280
Plu~ 94
Podaxi, 93
pod.etia II', 120. 121
PDdohydMn g;um %
PtJdrupM"a 68. 219
P<>IIMpora 59. 60. 185. 187
poisoning. rnusluoom 304. 305,
306. }J6-l2(i
effccts 319. 322. 323. 324.
325, 326
rult. rot noidins 279-280.
'"
145
polyo,in.
15 8
poJypheool o.id:l-<e 153
poIyphiilides 49
PoiYp<lI..,eg 85
"'"'
"
poaXe namps 97
P<>ril! 86
pol cul~
'"
Pina= 263
PftfferUng< 286
Pl\a<:i.dioc"e 63
PM~~i"",
ph)'lJoery\hrin 3 12
PIt]U01licla 74
272
PR 1O.lin 313
~ory fun,i ~3, 239249
pnoiooculatlon 2lS
pn:>~,gotic bMrie,.. 170
primers lSI
primary !>OS, 106
prim:uy iDOC"lum 203, 207
....-,
"",bryotts I
"",_rs In, 176. 180
proph"'" 1~ 1
propicon 'lol 220
propionic odd 300
pOI:IotS l39
pro<cctan .. 217
~n diles,ion 153
proIein; 142
Pm'o8aUl i~ria
97
2. 189
329
Pwda/I~J(:qrla
Pwd<>C)ph.llorio
PwtJoit)'<in,,,,,
120
1 0~
~udopar.iphy~
4J
PUNltOfMIYI'Wlporn
220
~.tides
)23, 314, lH
..... lmtO( 320. 321. 321. 324,
pscudoplawodia II
psaldo<bc:<:i>l a5C<1<na,a 42 . 73.
32. 3S
PJjl<x)'~ 9~.
polhnion. altJlOspberic In
poly'"" ..yl ..., 145
pol)'cemric 14
psilocin 325
psori:ui. 338
INDEX 371
poych<>acti,.., fungi 31).1. J2A. 321
poychrophilic 153
poychmlclennce 298. 300
PrycllogQJt~r
pycnidial ronidiornl\1
120. 121
"""nidium 45. -4
~ 5,
46. 64.
l)renochoelD 210
p)unula 121
p)~nul.:Les 112
Pythi""'a< 21
p)lhium 21 . 23. 126. 2<l4. 111.
12 I
Ro~11a
roo!
2S6
. pItids
lOS
root n>U
fO'l""ron;nc 31l
Q"atemaria 50
qui """", I~g, 218
Quom 289
roridin
2~S
,,'iculum 89
",tina 33. 3~
RFLP 180
rheumatoid :trtkriti. 337
m.~olytic <ttelsi(M! 47. 129
min<><:eros beetk. bioxoolroi 225
RI,Uwcl:Mj,lla 48
Rhi;pc/Ollia 211. 233. 2.34. 2M.
m. 312
m;.md. 14
dtiwrnorpl!. 95
Rhm)",ucor 331
, ttitomyc.lium 14
Rhj;:opogon 97. 135. 178. 256.
262, 265. 290
R~j;:Op04 32 , n. 3-1. }S. 128. 148.
168.220.296. )01. HI, 339.
RJoodosporiJl"", 116, In
RJrodom<lo. 113, LIS. 116, 157
RO"/UNi~
11!9
R..upinarus
of conifm 2 13. 21 4
'"
rad~vity
Rigi1;Wpon.. 86
!S
__ G/cmUJ
ScI.rc<I.""" 98, 99. 261. 264.
Sc/~mcyJriJ
265. ll7
Sckroderrn.,lle. 98
ScI,,<>srilbum 95
sclerotia 9', 256. 266
Schrrninitl 63. 168. 169. 211.
236. 301
ScIeroUDi_ae (iJ
Schrori"", 63. 210. 233. 2J.l
OOIocospo! 4(;
Sccpul<>rlopnJ 48. 49. 23'. 302
SCP 289
Scult ilinla 55. 56
Sc~lfllospora 270, 271. 272
SOS,PAGE 178
Ka$Ofl.ilily 260
''''
brv\\,. 86,
81
$CCot>d
96, 262
funp
103. 203
"'" physio!oa:i~1l rac .. 106
ruSl wb:!pecia 106
rye. <1&01 of 6S
rust
292.
:m, 295
Sacch>rO<llycellcne 116
Saa:twom}"tes 114, 116
SacrIu1"""ycodts 11 3
Saallarom)"COp1h 114. li S. 116
Sacco./>ohu 57. 18~
soddlc fun:i 57
saffron
milk
c~p
286
""I. 29')
<aniw1io n 210. 2 15
"probel IS. t3. 19.21. n. 29.
30. 31. 39. n. 59. 64. 83 . 86.
88. 9Z. 94, 95. 100. 148. 190.
191. 203. 21L. 21 4. 217. 223.
234. 237,
271. 298, 300.
303. 312. 321. 3:28. 329
SaproL 219
u.o.
5aprol~ln",
ZOo ll. Z2
SiJrco'ph.JtrU 317
satr>loxiol )()9
""",rlr:tlj\
)(()
scab lOS
ale i,,~s
H~
"""" "
septa"011 87
&pcobuidiaL.. 102. US
Mpl.:>lHuitiiJlm 102. 1().j
Mploria I lume bIo1ch 2011
<equence
180
scquostr:lI< 57. S8. ro. n 93. ~.
9S. 96. 97 . 98, 101. 109. Il ~.
135. 179. 261
MrICt<>C}'/1I: 93
IerOIOnin 325
MFJ'I'lo. IS
><n'icc:berry 106
.,.,...."'.Iion
~~
156-1~7
sco hormones
1~ 157
dimc:o-phism 167
.."ual rep,oouclion---->.<.
Ideomo'ph.
, baggy m:l/le 9"2. 0.1. 287
s.hakes 3 12
~xu:t\
Ihoyu 29S
.i""oi<l lPO=
191
lilkwonns 224
Iii"., .... 2SS
,;L.icullur:>J pr3<,ices 214
li... nin 1S6
Si""'rtlfUl !J.I
sl<.kI.l! h)'p/= 86. 87
Jl>fr.Im!ne 312
Sli""",omyc~J illS. 1.!9
372
yiF'l' H K I NGDOM
1Iime IIlO\lJds 9
.kIIlbtr fa.tOT 312
Smillium 36, 37
10lIl1 fun" 104. 107. 113. 1/iS.
'"
>r>aiI 196
bl.igltt 63
oodi um benrooto 300
oodillm Itwe 300
ron rot of peach ~. 208
.,.,w
"
Spof(,.hrl.. 329
$pOI~' 329
. porul.tion 146. ISS
~ad ai di.u.es In. 133
.ptiniwh 2~g. 290
-"
squamujo~ tich~"$
conidiomata 45. # .
'"
S",,~)lin<l
36
stager< 31 2
be<clI 74
119. 120
143
roybeans 2 19
S1lJpII),/oco(C14
135, 136
...reh 143
l taurosporu 45. 46
SE<'inp,1L 2&5
289
SpaoJud<.ria 6J
'pe.;iel 4
COtDparuool
,~ir.c IfO"th
SttlfWftiri,
1go
me 1.l.3
'PC"" 13. 17
$pe"""iOll.i3 104. 105
, pc:rmati. 104
$p/l<Julla 65
'"
spind]~.
"
l~l.
H!.
1~3
"""pl;"J 138
tetr>r.tdi,," 191
s.porid.smin 311. 31 2
lI6
Sporol><Aomy<:tl 113. 11 4. 1\5,
116. 139
.porotladia 32. 15
Sf>')rid/oIK>tl<S
1&
3]4
Strtp,omyc,s 25 3
Slrtptoti>UD 6J
StrolJ</omys 97
StrObilomycrt.x .... 91. 262
SIfOIlWJO (6. 66.
Slropha,.ul 95
St.ropllJri_k !M
Stylopag, IS7. l4.ISubdue 119
~!lial '~ICle H. 3ii
",bll,..' .. 190
1OC<~ ]91
on dun. I~
GIl 1.0 tiEter 188
mywnmul 162
, uf" Z96
"'$ar
.k:ohoI~ 143
lUg .. W<1tont 299
' "ian 143. 292
.
s,ul/J<s 'n. ]78. 262. 263. 2~.
265. 278
IU]ph ..... 217
"'lp/ll.:f dio.ie!. Ill. 300. 302
,ulphur <htlf 86
IUmmtl spores lOS
, uptmta,ke. mu.hroom 280
,na tOO<h
8~
. oll
1e<n1.n~ c atl
32 4
2S~.
281
145
192
thymi". 142
nll~ri<l 1001 , 108, 137
Nboe. 89
2i2
Tilktiac<:..., 108
}oel .c tio~
..."
Tulasnel!ale. 102
Twiostoma 9'}
T'uJOIitomataleS 100
Nninz full:; basidi:I 8l
Nl'go< Pre$su", 247
turkey
87
1I.ti'kt)- X dj...... 3O!i
till no
Tin>elin 332
lint.. 321. 328
toad<tools 88
tob3CCO, bl"t mould or 25, 201.
'"
IOInaftat. ~n
wi
T)'lapi!us 97
1)'""",UJ 86
301. 311
8S
Torvlopsis 116
toxicity 217
Umbilicafii, 122
UIICj"..Ja 68, ~9. 133
utUc<:Uubr 112
Unitunk.t ... ,~n:ul.tae $9
Unitu" i"a .. e cpercul .,~ ,~
un"-~,,>1 vcil 38
ulxil 142
UrMin.ales 103
ure<linia 105
urcdiniosp;:>r!:' 105
UrocpRs 100, 210
UPtM 120
uitilagi....cue 101
UlliiaginaJ .. 107. 114, 11 6. 168
UJriiago I ~ , 107, 168. 2a.., 2M.
285. 289
tOQ!h fun,i
tnII5f<>nn1lion In, In
tnft.locatloa 26(1, 26S, 278
transport 1'2
.cti". 152
pa:l.>ive IS 2
Trt"-tia 119
rrn:irifPtJFIl 84
trel1.lose 143. 260
T,..m~lla 102, 1113. 157. 2S5
Trenlellala 102, 103, 11~
T,..m~{/odolt 10Z
Triadimcf.". 219
tricarboxyUc acid ""Ie 145
rridrotknntl 62. 1~3. 176. 233,
234. 2]7, 300. 339 , 340
rrlc~o{oma 95, 262. 26.5, 266,
27S. 286. ll7
Tricholom.'l3C 95
Trichom)'C'1:lC$ )6. 37
Tric~oph}'l<><I 52, M , 70. 153,
317. 328. 332
Trlelooi""",," 11 5
Iric~ 145. lOS. 309. 310
Trlclr"'h:I,,'~ 49
Trk ho:.ygo.fX'''' 37
rn'churu,f 18S
lrid<morph 213
vee
IS2
,'octors
arthropod 100, 1()4 , 131. 136,
186. 237
buman 128
mammalian .58. 131. 135, 1S6
<nnSmI..wn
>lem 28!
173, 203
V.nturi"" ... 74
1~2
".1'
W"a""" 95
,,'h t bunl lOS
20~
.. iJr, -W , WS
.. in. 112.
293.29~
86, 214
217
..'OQd ....~ps lSS
Wo,orun bud)' 78, 79
... cod
WQt.l.nd
<1<0')'
pre>C1"'.n,.
po""i'.
236
X'rMfphaiir.a 9'
MroIol<nn<e 29, 298. 301.
X,,,,la 9S
X~l\lhcc>< %
xi.lll;-", 280
X)!.oria S9. 60, ln, 2S4
, )'to..e
'"
-eh'
''''''''. 182
..-ovd
"'FOrr~t"
27~
31 ~
II~
),..,t, 54,
Tnd~nlari" 2~9
\'e"kldudi~lIa
Vcrticic4uliw", 190
V"ricilli"", 49, 171. 202. 204,
22.1. 225. 216. 233, ~. 235.
236. 242
'e$klts 36, 269
v icul .... t>llSc uTor m)'corrl>iz"-,
258. 269276
..,bu""ules 16/1
<:\cYclgpmenl 2M
di",,~ rUist:lllCe 276
fungal la.\. 270 (~ey)
ino,:ulal;O<I 276
ullmjmyc~J 96
ZH'lCb 218, 2:!O
Zlx>PM8u-, 2J1i. ].19
zocopor.!",i. 16. 20. UO
lOOspoo"" 13. 14. IS. 17. 19. 22.
l.l, 203
olln""'o,",. J ~
l4lfuc 11
Z)J""'}CCICS JO.31. 38. 12R
zYJ""')-cOOs 331, 3)2
rripo>p<>ri7Ul 249
vUporic acid U6
r"",hi/a
,rout 19J
6'
,rum.
tlies 2110
uuffh:< 5S. 279, 2SI 2SJ, 290
Trw=N>l..-II" <n. 262
~9
Z)"i'omycotl 30
zygo<porani,ia :;0, 31. 34. 35, 128
<),I"t., 3. 10, 17