Arbuscular Mycorrhiza: A Review of Its Biological, Chemical, and Molecular Aspects

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Style file version June 28th, 2002
C 2003)
Journal of Chemical Ecology, Vol. 29, No. 9, September 2003 (
REVIEW PAPER
ARBUSCULAR MYCORRHIZA: BIOLOGICAL, CHEMICAL,

AND MOLECULAR ASPECTS
DIETER STRACK,1, THOMAS FESTER,1 BETTINA HAUSE,1

WILLIBALD SCHLIEMANN,1 and MICHAEL H. WALTER1
1 Leibniz-Institut
fur Pflanzenbiochemie
Abteilung Sekundarstoffwechsel
Weinberg 3, D-06120 Halle (Saale), Germany
(Received April 16, 2003; accepted May 18, 2003)
AbstractMycorrhizas are the most important mutualistic symbioses on earth.

The most prevalent type are the arbuscular mycorrhizas (AMs) that develop between roots of most terrestrial plants and fungal species of the Zygomycota. The
AM fungi are able to grow into the root cortex forming intercellular hyphae from
which highly branched structures, arbuscules, originate within cortex cells. The
arbuscules are responsible for nutrient exchange between the host and the symbiont, transporting carbohydrates from the plant to the fungus and mineral nutrients, especially phosphate, and water from the fungus to the plant. Plants adapt
their phosphate uptake to the interaction with the AM fungus by synthesis of specific phosphate transporters. Colonization of root cells induces dramatic changes
in the cytoplasmic organization: vacuole fragmentation, transformation of the
plasma membrane to a periarbuscular membrane covering the arbuscule, increase
of the cytoplasm volume and numbers of cell organelles, as well as movement of
the nucleus into a central position. The plastids form a dense network covering
the symbiotic interface. In some of these changes, microtubules are most likely
involved. With regard to the molecular crosstalk between the two organisms, a
number of phytohormones (cytokinins, abscisic acid, jasmonate) as well as various secondary metabolites have been examined: (i) Jasmonates occur at elevated
level, which is accompanied by cell-specific expression of genes involved in jasmonate biosynthesis that might be linked to strong carbohydrate sink function of
AM roots and induced defense reactions; (ii) apocarotenoids (derivatives of mycorradicin and glycosylated cyclohexenones) accumulate in most mycorrhizal
To whom correspondence should be addressed. E-mail: dstrack@ipb-halle.de
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STRACK, FESTER, HAUSE, SCHLIEMANN, AND WALTER

roots examined so far. Their biosynthesis via the nonmevalonate methylerythritol
phosphate (MEP) pathway has been studied resulting in new insights into AMspecific gene expression and biosynthesis of secondary isoprenoids.
Key WordsArbuscular mycorrhiza, (apo)carotenoids, chemical interaction,
ecology, MEP pathway, mutualism, phosphate transporters, secondary metabolism, symbiosis.
INTRODUCTION
More than 90% of terrestrial plants are associated with root-colonizing fungi, establishing a permanent and intimate mutualistic symbiosis, called mycorrhiza. Several
types of mycorrhizas exist, defined by plant/fungus combination and the symbiotic
structure. The endotrophic arbuscular mycorrhiza (AM) is the most common type,
occurring in about 80% of plant species. The AM fungi are represented by more
than 150 species of the Zygomycota included in the Glomales (Morton and Benny,
1990). Recent work on the phylogeny of AM fungi provided a basis for a new
systematics (Schuler et al., 2001; Schuler, 2002), removing these fungi from the
polyphyletic Zygomycota and placing them into a new monophyletic phylum, the
Glomeromycota.
There is a disagreement about usage of the term symbiosis, originally defined in 1869 by Heinrich Anton de Bary as an intimate, outcome-independent
interaction between different species, ranging from parasitism to mutualism. Later,
especially in Europe, the term symbiosis was used to mean only mutually beneficial association of organisms (=mutualism). In this review, the term symbiosis
is used in its original meaning.
The term mycorrhiza was coined in 1885 by Bernhardt Frank by recognizing special structures in tree roots. The term means fungus root, later characterized as ectomycorrhiza. Frank not only described its morphology but also
inferred its physiological role (Frank, 1888). Arbuscular mycorrhiza (AM) replaced the earlier term vesiculararbuscular mycorrhiza (VAM) because not all
endomycorrhizas of this type develop vesicles, but all form arbuscules.
There are two major types of mycorrhizas, AMs and ectomycorrhizas. The
latter evolved as a more recent symbiosis of woody trees and shrubs with ectomycorrhizal fungi. The plant hosts of AM fungi are mostly angiosperms, some
gymnosperms, pteridophytes, lycopods, and mosses (Smith and Read, 1997). The
physiological interactions of lower plant mycorrhizas, however, are poorly understood. With regard to the systematic distribution of AMs in higher plants, it is still
an open question how some nonhost plants, e.g., members of the Brassicaceae,
Caryophyllaceae, Chenopodiaceae, or Urticaceae, resist mycorrhizal colonization
(Vierheilig et al., 1994, 1996). The nonmycorrhizal state of nonhost plants might
be a derived trait. It might be the outcome of specialization regarding, e.g., the
plant habitat (Fitter and Moyersoen, 1996).
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ARBUSCULAR MYCORRHIZA
According to the fossil record and molecular data, the origin of the AM symbiosis goes back at least to the Ordovician, 450500 million years ago (Remy
et al., 1994; Redecker et al., 2000). It is assumed that this symbiosis aided plants
during their land colonization in the acquisition of water and minerals, especially
phosphate (Simon et al., 1993). At the time of land colonization, the first bryophytelike plants appeared in terrestrial environments. Today, a number of bryophytes
and pteridophytes are still capable of forming AMs (Read et al., 2000; Schuler,
2000).
In contrast to AMs, ectomycorrhizas (Tagu et al., 2002) and the more specialized ericoid mycorrhizas (Perotto et al., 2002) evolved later in evolution and are of
polyphyletic origin (Fitter and Moyersoen, 1996). These symbioses are especially
adapted to habitats rich in organic material that did not exist on earth when the
AM symbiosis developed.
Interesting questions to be addressed are on the selective forces that led to the
mutualistic coexistence of the two partners. Whereas the macrobiont (phytobiont)
can live without AM fungi, although suffering in nutrient- and water-deficient
soils, the microbiont (mycobiont) became dependent on plant roots and developed
towards an obligatory biotrophic life cycle. Another challenging problem is the
complexity of field situations, where many plant and fungal species coexist with
many different soil organisms in different ecosystems.
ECOLOGY
In accordance with the evolutionary history, AM symbioses can be found in

almost all ecosystems. They have been described from deserts (Corkidi and Rincon,
1997; Dalpe et al., 2000; Titus et al., 2002), tropical rainforests (Brundrett et al.,
1999; Guadarrama and Alvarez-S

anchez, 1999; Siqueira and Saggin-Junior, 2001;
Zhao et al., 2001; Gaur and Adholeya, 2002), aquatic environments (Khan, 1993),
as well as from ecosystems with strong saline (Carvalho et al., 2001; Sengupta and
Chaudhuri, 2002), sodic or gypsum soils (Landwehr et al., 2002). The relatively
low number of plants colonized by AM fungi in some arctic and antarctic habitats
seems to be due to a lack of suitable vectors for fungal spores rather than to other
causes (Allen, 1996).
In addition to the global distribution of AM symbioses, there is large functional diversity as well. Whereas most AM symbioses are mutualistic, a growing
number of nonphotosynthetic plants are described, which are receiving a large portion of their nutrients from AM fungi (Imhof, 1999; Yamato, 2001), resembling
the functioning of orchid mycorrhizas (Rasmussen, 2002). In some cases, these
mycotrophic plants are living epiparasitically on other plants using the hyphae of
their fungal partner for the transfer of nutrients (Bidartondo et al., 2002). On the
other hand, AM fungi may become parasitic themselves in relation to their host
plant under special circumstances (Allen, 1996).
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Regarding plant communities, there is a large number of possible consequences of AM colonization (Francis and Read, 1994). Interactions between plant
and fungal communities rely primarily on the fact that a given plant or fungus
prefers some symbiotic partners and neglects others. In addition, the benefits obtained from the symbiotic partner are dependent on the actual partner and on various
other conditions. Even the direct transfer of nutrients from one plant to another
via fungal hyphae has been discussed (Francis et al., 1986). Within ecosystems,
a network of feedback dynamics based on these interactions between fungal and
plant populations has to be taken into account (Bever, 2002). These dynamics
may be important to maintain diversity within plant communities. Sanders et al.
(1996) have stressed the importance of fungal diversity for the ecological impact
of the AM symbiosis, and van der Heijden et al. (1998) have shown in a case
study that fungal and plant population diversity are directly correlated to each
other. In general, the results from single ecological studies regarding ecology of
AM symbiosis are highly dependent on the local situation (Hartnett and Wilson,
2002). As the main possible consequences, Koide and Dickie (2002) have singled out (i) increased plant reproduction, (ii) stable plant populations because
positive mycorrhizal effects might inversely correlate with population density,
(iii) favoring of the most robust individuals by AM fungi, and (iv) patchy distribution of mycorrhizal areas due to the spread of colonization starting from
mycorrhizal plants.
Apart from supplying plants with phosphate and other nutrients, further beneficial effects have been described for AM fungi. The symbiosis has a positive effect
regarding plant water potential especially for plants under drought stress (Auge,
2001). AM colonized plants show a significant degree of bioprotection against
various pathogens (Cordier et al., 1996; Dugassa et al., 1996; Bdker et al., 1998;
Vaast et al., 1998; Slezack et al., 2000; Elsen et al., 2001). In addition, positive
effects of AM fungi on soil structure have been described. As a consequence, the
AM symbiosis is regarded as a key component of sustainable agriculture (Bethlenfalvay and Lindermann, 1992; Jeffries and Barea, 2001), whereas under conventional agricultural conditions, AM fungi seem to be only of minor importance
(Ryan and Graham, 2002). Mader et al. (2000) have compared conventional and
organicbiological agricultural systems directly. They found stronger mycorrhizal
colonization for the organicbiological system and preliminary evidence for a partial compensation for the disadvantages of the organicbiological system by the
AM fungi. Apart from agricultural systems (Kiers et al., 2002), the application of
AM fungi is tested for the revegetation of desertified areas (Saito and Marumoto,
2002) and in cultivation of micropropagated plantlets (Yano-Melo et al., 1999). In
this context, major technological problems are the form of application of the AM
inoculum (Saito and Marumoto, 2002) and the combinations of AM inoculum with
other microorganisms that are beneficial for plant growth (Vazquez et al., 2000,
2001; Vassilev et al., 2001).
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FIG. 1. Morphology of the life cycle stages of an AM fungus, Glomus intraradices in a

maize root: A, germinating spore; B, appressorium; C, intercellular hyphae; D, arbuscule;
E, intercellular vesicle; F, extraradical spores. The fungal structures are visible after staining
with trypan blue (Phillips and Hayman, 1970).
COLONIZATION AND MORPHOLOGICAL CHANGES
Steps in root colonization by AM fungi are shown in Figure 1. The process starts with germination (hyphal growth) of fungal spores, followed by poorly
understood events. Subsequently, appressoria are formed from which the fungus
penetrates the root surface and colonizes the intercellular space of the root cortex. On the fungal side, nonaggressive cell wall-lytic enzymes become active,
and both the plant root cells and the fungus change their gene expression pattern and morphology. The hyphae penetrate the cell walls and develop within
the cortex cells tree-like structures, called arbuscules, by repeated dichotomous
branching. In some cases, intercellular storage organs, lipid-rich vesicles, and
finally extraradical spores are formed, which may enter another colonization process. Fungal root colonization is under control of the plant aiming at a morphological and functional compatibility of the two partners (Bonfante and Perotto,
1995).
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The key feature of AMs is the arbuscule, a highly branched haustorium-like

structure within root cortex cells, responsible for nutrient exchange. However, the
arbuscules represent a dead-end in the growth of AM fungi (Bonfante and Perotto,
1995) and they finally senesce and collapse after 410 days of symbiosis (Sanders
et al., 1977), possibly caused by the continuously stressful environment of the host
cortex cell (Harley and Smith, 1983).
Colonization of root cortex cells by AM fungi has been shown to induce
dramatic changes in the cytoplasmic organization and morphology of root cells.
The fungal arbuscule occupies a major portion of the plant cell volume but is still
separated from the cell protoplast by the host plasma membrane. This membrane
completely surrounds the arbuscule and forms a periarbuscular membrane, leading
to a two- to fourfold increase in the plasma membranes surface. The resulting
space between the plant protoplast and the fungus develops into an apoplastic
compartment that represents the symbiotic interface (Bonfante and Perotto, 1995).
Figure 2 shows some arbuscule branches surrounded by the plama membrane and
the interfacial matrix in a colonized maize root cortex cell.
Formation of arbuscules is accompanied by alterations in morphology of
the host cell: the central vacuole is fragmented, the volume of cytoplasm and
number of cell organelles increase significantly, and the nucleus moves into a central position and undergoes hypertrophy (Balestrini et al., 1994). The nucleus of
arbusculated cells (arbuscule-harboring cells) is characterized by enhanced fluorochrome accessibility, increased nuclease sensitivity, and chromatin dispersion,
all together reflecting a greater transcriptional activity of the plant genome in
the colonized cells (Gianinazzi-Pearson, 1996). The host cytoplasm and cell organelles proliferate around the branching hyphae. The number of plastids in colonized cortex cells increases (Bonfante and Perotto, 1995) and networks are formed
covering the arbuscules (Fester et al., 2001; Hans, 2003). The plastids in these networks are connected to each other by so-called stromules (stroma-filled tubules)
(Kohler and Hanson, 2000). In addition, the nucleus is surrounded by plastids
forming octopus-, millipede-like or ring-shaped structures. In cells that do
not contain fungal structures, the plastids are distributed anisotropically throughout the cytoplasm, similar to cortex cells of nonmycorrhizal roots. The formation
of those dense plastid network-covering arbuscules indicates a dramatically intensified metabolism in these host cells. Figure 3 shows confocal laser scanning
micrographs of plastid networks in AM roots, labelled by green fluorescent protein
(GFP) in transgenic tobacco roots (Fester et al., 2001) and by immunodetection of
the plastid-located 1-deoxy-D-xylulose 5-phosphate reductoisomerase (DXR) in
maize roots (Hans, 2003). This enzyme catalyzes the first committed step of the
plastid-located methylerythritol phosphate (MEP) pathway (see below), stimulated
in AM roots.
According to their role in a variety of cellular functions in plants, it has been
shown that microtubules are involved in changes of host cell morphology and
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FIG. 2. Electron micrograph of an arbusculated cortex cell of a mycorrhizal maize root (bar,
0.5 m). The graph shows sections of several arbuscule branches (arb) surrounded by the
periarbuscular membrane (pam) and the interface (if). Note also some of the proliferated
organelles (m, mitochondrion; pt, plastid) and the fragmented vacuole (v). The root was
fixed by high-pressure freeze fixation and embedded in methacrylate. Ultrathin-sections
(90 nm) were stained with uranyl acetate/lead citrate and observed with an EM 900 transmission electron microscope (Zeiss, Oberkochen, Germany). Micrograph courtesy of Diana
Schmidt.
cytoplasmic architecture. Plant cytoskeletal components respond to the penetration

of a symbiotic fungus with the reorganization of microtubules and microfilaments.
However, an understanding of the role played by the cytoskeleton in formation
and function of mycorrhizas has been hampered by technical difficulties in handling mycorrhizal tissues. Recently, application of improved labelling techniques,
suitable for both the plant and the fungal symbiont, combined with either epifluorescence microscopy or laser scanning confocal microscopy, gave interesting
results (Timonen and Peterson, 2002). They show extensive remodelling of the microtubular cytoskeleton from the early stages of arbuscule development until the
arbuscule senesces and collapses (Genre and Bonfante, 1997, 1998). Four types
of microtubule patterns were observed in arbusculated cells: (i) long bundles of
microtubules crossing the cytoplasm among the arbuscule branches and passing
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FIG. 3. Confocal laser scanning micrographs of plastid networks in AM roots, colonized by Glomus intraradices: A, fluorescence of the
green-fluorescent protein targeted to the plastid compartment in transgenic tobacco roots; B, immunolocalization of DXR in arbusculated
root cortex cells of maize. The plastid-located DXR protein is mainly detected by the green fluorescence around the nucleus (ring-shaped
structure) and in the network around an active arbuscule. The presence of the arbuscule is indicated by autofluorescent signals (red) around
and within the network structure. The lower cell in A and the upper right cell in B show disintegrating arbuscules (increased autofluorescence)
with only few plastids left exhibiting green-fluorescent protein (A) or labelled DXR (B).
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through the arbuscule; (ii) short microtubules connecting fine arbuscule branches
or connecting arbuscule branches either to the cortical region of the cell or to the cell
nucleus; (iii) bundles of microtubules in the periphery (cortical region) of the host
cell and along the hyphal trunk; and (iv) perinuclear bundles of microtubules. In
addition, it was found recently that cortex cells adjacent to the arbusculated cells or
to the intercellular hyphae reorganize their microtubules as well (Blancaflor et al.,
2001). This indicates a molecular dialogue between the symbionts prior to fungal
penetration of the plant cell wall and an active role of the plant cytoskeleton in
mycorrhization rather than passive reaction to the physical pressure created by the
fungus invaginating the cell plasma membrane. The alterations of the microtubular
network are consistent with the identification of a mycorrhiza-inducible fi-tubulin
gene in maize. Expression studies of corresponding promoter::GUS fusions in tobacco indicated that this gene is induced specifically in cells in which arbuscules
are developing (Bonfante et al., 1996).
Besides the possible function of the cytoskeleton in reorganizing the cell for
the accommodation of the arbuscule, the cytoskeleton might also be involved in
developing the periarbuscular membrane. This membrane, although originating
from the plant plasma membrane, shows differences in some of its properties relative to the membrane around the periphery of the cell. In particular, high activities
of H+ -ATPases and phosphate transporters were shown to be located specifically
in that membrane (Gianinazzi-Pearson et al., 1991; Rausch et al., 2001; Harrison
et al., 2002; Paszkowski et al., 2002). Recently, a plasma membrane H+ -ATPase
gene from Medicago truncatula has been described for the first time that shows
arbuscule-specific induced expression in mycorrhizal tissue (Krajinski et al., 2002).
The interface compartment that develops between the plant and the fungus is
continuous with the peripheral plant cell wall (Bonfante and Perotto, 1995). Although the fibrillar interface differs from the peripheral plant cell wall in structure,
its components reflect the composition of the wall of the host cell that is being
invaded. By immunocytological approaches, the presence of pectins, xyloglucans,
nonesterified polygalacturonans, arabinogalactans, and hydroxyproline-rich glycoproteins within the symbiotic interface was documented (Balestrini et al., 1994;
Perotto et al., 1994; Bonfante and Perotto, 1995). This mixture of primary plant
cell wall components indicates that the arbusculated plant cells have maintained
their abilities to synthesize and secrete cell wall material. That this material does
not assemble further to build up a secondary wall might be the result of lytic activities of the fungus (Peretto et al., 1995). When the arbuscule begins to senesce,
the fibrillar material encapsulates the collapsed fungal structures that are then degraded completely by the plant cell. Subsequently, the cells regain their original
morphology (Jacquelinet-Jeanmougin et al., 1987) and are able to allow another
arbuscule formation.
Some processes of AM establishment are known to be mediated by phytohormones on the plant side, as suggested by application experiments (Barker and
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Tagu, 2000). The levels of cytokinins are higher in shoots and roots of mycorrhizal
plants compared to nonmycorrhizal ones (Allen et al., 1980). A possible role of
abscisic acid was suggested from the fact that its level increases in AM roots
(Danneberg et al., 1992; Bothe et al., 1994). Jasmonic acid applied exogenously
promotes colonization and development of mycorrhizal structures (Regvar et al.,
1996). The observed endogenous rise of jasmonates in barley roots correlating
with myorrhization, however, is more indicative for a role in AM (Hause et al.,
2002). The rise in jasmonates is accompanied by the expression of genes encoding
for an enzyme involved in jasmonate biosynthesis, allene oxide synthase (AOS),
and of a jasmonate-induced protein, JIP23. In situ hybridization and immunocytochemical analyses revealed that expression of the corresponding genes occurred
cell-specifically within arbusculated root cells. Since jasmonate levels increased
after the initial step of the plantfungus interaction, the development of AM may
cause expression of jasmonate biosynthetic genes and finally elevate jasmonate
levels. The induction of jasmonate biosynthesis could be linked to the stronger carbohydrate sink function of mycorrhizal roots compared to nonmycorrhizal ones.
Taking into account that jasmonate-induced genes are involved in various defense
responses (Wasternack and Hause, 2002), higher endogenous jasmonate levels
could help mycorrhizal roots to become more resistant to secondary infection
and/or other stresses. It might also indicate plant control of the invading AM fungus.
CHEMISTRY
Despite increasing efforts in research on metabolic changes, virtually nothing

is known about signalling compounds or about the role of secondary metabolites
in the establishment and maintenance of a functioning AM. It is known that compounds from secondary metabolism play a significant role in the interaction between plants and their biotic and abiotic environment (Harborne, 1993), and it may
be assumed that secondary metabolites play an important role in mycorrhizal symbioses as well. It has been shown that flavonoids occurring in plant roots promote
spore germination of AM fungi (Gianinazzi-Pearson et al., 1989; Tsai and Phillips,
1991). Root exudates of phosphate-deficient white clover plants were more active
in enhancing hyphal elongation of Glomus fasciculatus spores than exudates from
phosphate-fertilized plants (Elias and Safir, 1987). The level of the phytoalexin
medicarpin is reduced in mycorrhizal Medicago truncatula roots (Harrison and
Dixon, 1993). Roots and root exudates from phosphate-deficient parsley contain
additional compounds that are absent in phosphate-fertilized controls and mycorrhizal plants (Franken and Gnadinger, 1994), but the nature and function of these
compounds is unknown. Mycorrhization of Citrus jambhiri led to an induced accumulation of leaf sesquiterpenoid volatiles (Nemec and Lund, 1990).
It was shown in 1924 by F. R. Jones that mycorrhizal roots of many plants develop a yellow coloration based on accumulation of the so-called yellow pigment.
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This phenomenon has been taken as an indicator to estimate the degree of mycorrhization by the naked eye (Daft and Nicholson, 1969; Fyson and Oaks, 1992)
or by colorimetric measurement of root extracts (Becker and Gerdemann, 1977;
Schmitz et al., 1991). The component containing the chromophore of the yellow pigment was isolated from mycorrhizal maize roots and identified (as its
dimethyl derivative) by NMR spectroscopy and MS as all-E-4,9-dimethyldodeca2,4,6,8,10-pentanedioic acid, named mycorradicin (Klingner et al., 1995a). Besides maize, other gramineous plants (wheat, barley, millet) show the same pattern
of pigment formation (Klingner et al., 1995b). It was later shown in a screening
of 58 species from 36 different plant families that mycorradicin as part of the
yellow pigment is present in mycorrhizal roots of all Liliopsida analyzed and of
a considerable number of Rosopsida (Fester et al., 2002a). In addition, chemical
analysis of the yellow pigment indicated that mycorradicin is the core structure of a mixture of various oligo- or polyesters with glycosylated cyclohexenone
derivatives. In mycorrhizal maize plants, these esters were localized in vacuolar
hydrophobic droplets (Fester et al., 2002a).
Because of structural similarities of mycorradicin with crocetin (C20 -polyene)
and azafrin (C27 -apocarotenoid), it was speculated that it derives from a C40 carotenoid precursor by splitting off two C13 -units (Klingner et al., 1995a,b). At the
same time, studies on changes in secondary metabolites in roots of cereals (wheat,
barley, rye, oat) colonized by the AM fungus Glomus intraradices resulted in the
structure elucidation of a mycorrhiza-induced glycosylated cyclohexenone derivative [blumenol C 9-O-(20 -O-fl-glucuronosyl)-fl-glucoside], called blumenin (1)
(Maier et al., 1995). The level of blumenin was found to be directly correlated with
the degree of root mycorrhization. Table 1 depicts the structure of blumenin and
lists all other cyclohexenone derivatives identified so far from mycorrhizal roots
(see below).
It was assumed (Walter et al., 2000) that the aglycone of blumenin, blumenol
C, may be another carotenoid degradation product along with mycorradicin. Thus,
cleavage at the 9,10(90 ,100 )-positions of a C40 -carotenoid should lead to mycorradicin and the cyclohexenone derivative. Further detailed investigation of mycorrhizal barley roots revealed in addition to blumenin the presence of closely related
cyclohexenone derivatives [7,8-dehydroblumenin (2) and 13-hydroxyblumenol
9-O-fl-glucoside (3)], which showed an AM fungus-induced continuous accumulation, whereas putrescine and agmatine amides of 4-coumaric and ferulic acids
increased only transiently in early stages of the root-fungus interaction (Peipp
et al., 1997).
The occurrence of compounds 13 in cereal mycorrhizas initiated a study
on their distribution within the Poaceae. After inoculation of various members of
the Poaceae with Glomus intraradices, HPLC analyses of root extracts revealed
marked changes in the patterns of UV-detectable metabolites along with accumulation of these cyclohexenone derivatives. The latter occur most often in the
CH2 OH
COOH
Glc(100 60 )GlcGlc(100 60 )GlcGlcGlc(100 60 )GlcGlc(100 60 )(Glc1000 20 )GlcGlcGlc(100 40 )Glc-
4d
6
7
8
9
10e
Ta = Triticum aestivum; Zm = Zea mays.

c 7,8-Dehydroblumenin; 17,8 present, absent in all other compounds listed.
d Nicoblumin.
e Hydrolysis product of the yellow pigment.
Structure scheme
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= Nicotiana rustica; Nt = Nicotiana tabacum; Sc = Secale cereale;
Nt, Nr
Hv, Ta, Zm
Nt, Nr
Nt, Nr
Nt, Nr
Le
Zm
Maier et al., 1995

Vierheilig et al., 2000
Peipp et al., 1997
Peipp et al., 1997
Maier et al., 1997
Maier et al., 2000
Maier et al., 1999, 2000
Walter et al., 2000
Maier et al., 2000
Maier et al., 2000
Maier et al., 2000
Maier et al., 2000
Maier et al., 2000
Fester et al., 2002a
Reference
August 20, 2003
a Blumenin (in all compounds listed: Glc = fl-glucose; GlcUA = fl-glucuronate).

b As = Avena sativa; Hv = Hordeum vulgare; Le = Lycopersicon esculentum; Nr
CH3
CH3
CH3
COOH
CH3
CH3
Ta, Sc, As
Zm
Hv
Hv
Hv, Ta, Sc, As
Nt, Nr, Le
Nt, Nr
Hv, Ta, Zm
Hvb ,
Occurrence
1966
CH3
CH3
CH3
CH3
R3
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COOH
CH3
CH3
CH3
CH3
CH3
CH2 OH
GlcUA(100 20 )GlcGlc-
CH3
2c
3
20 )Glc-
R2
GlcUA(100
R1
1a
Compound
TABLE 1. STRUCTURES OF GLYCOSYLATED CYCLOHEXENONE DERIVATIVES ISOLATED FROM MYCORRHIZAL ROOTS OF VARIOUS PLANTS
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tribes Poeae, Triticeae, and Aveneae (Maier et al., 1997). To evaluate the AMspecific formation of cyclohexenone derivatives, some inoculations of barley roots
with pathogens (Gaeumannomyces graminis and Drechslera sp.) or an endophyte
(Fusarium sp.) were performed. These, as well as treatments with abiotic stressors
(heat, cold, high intensities of light, heavy metals, and drought), did not induce
the formation of cyclohexenone derivatives (Maier et al., 1997). Because of the
occurrence of both C13 and C14 apocarotenoids (cyclohexenone derivatives and
mycorradicin) in mycorrhizal roots, their formation might be similar to that of abscisic acid, involving a dioxygenase-catalyzed cleavage of a carotenoid precursor
(Maier et al., 1998; Walter et al., 2000).
One of the first arguments for a carotenoid origin of cyclohexenone derivatives derived from NMR spectroscopic analysis of blumenin (1) after [13 C]glucosetracing experiments, indicating a mevalonate-independent biosynthesis of the cylohexenone derivative (Maier et al., 1998). Figure 4 shows the 13 C-labelling pattern
of blumenol C, after feeding [1-13 C]glucose to barley roots. For comparison, potential labelling of mycorradicin via the MEP pathway and isopentenyldiphosphate
(IPP) synthesized via the mevalonate pathway are shown.
The assumption that the AM-specific isoprenoids are apocarotenoids was
recently supported by a study showing that carotenoid biosynthesis is strongly
stimulated in AM roots, at least partially at the transcriptional level (Fester et al.,
2002b). Tobacco plants transformed with a phytoene desaturase promoter::GUS
construct showed a cell-specific induction of the phytoene desaturase promoter
activity in arbusculated root cells.
The role of the cyclohexenone derivatives in mycorrhizal symbiosis is unknown, although there is some indication that they might be involved in control
of mycorrhization. Exogenously applied blumenin strongly inhibits colonization
and formation of arbuscules in the early stages of mycorrhiza formation in barley
(Fester et al., 1999). Inoculation of barley, wheat, and maize with different AM
fungi (Glomus mosseae, G. intraradices, and Gigaspora rosea) led to the accumulation of 1, 4, 5, and another, yet unidentified, cyclohexenone derivative in all
plant/fungi associations. The relation of all compounds to each other was quantitatively different, but qualitatively identical, indicating no fungus-specific induction
of selected compounds (Vierheilig et al., 2000).
In addition to the well-characterized AM fungus-induced accumulation of
cyclohexenone derivatives in gramineous plants, a set of similar compounds was
found in roots of tobacco and tomato (Solanaceae) after colonization with Glomus
intraradices (Maier et al., 1999, 2000). In the major compound, named nicoblumin
(4), the aglycone of 3 (13-hydroxyblumenol C) is connected at the C-9 hydroxyl
group with a 1,6-linked diglucose (gentiobiose). Both in mycorrhizal roots of
two tobacco species (Nicotiana tabacum, N. rustica) and in tomato (Lycopersicon
esculentum), 3 was found to accumulate. The aglycone of two further tobacco
cyclohexenone derivatives is formed when the hydroxymethyl group at C-5 in 3 is
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oxidized to a carboxyl group. This structure accumulates as 9-O-gentiobioside (5)

and 9-O-glucoside (6). Additional strongly induced major compounds in tobacco
are the gentiobiosides of blumenol C occurring as S- andR-isomers at C-9 (7),
whereas a minor component is a triglucosyl derivative of blumenol C (8). In tomato
roots, an additional 9-O-glucoside (9) bearing a carboxyl group at C-1 occurs, but
the relative configurations of the asymmetric sites (C-1, C-6, and C-9) could not
be etablished from NMR spectroscopic data. Further comparative studies of cyclohexenone derivatives in mycorrhizal maize and wheat roots revealed the presence
of six compounds from which only the 9-R,S-isomers of blumenin (1), nicoblumin
(4), and 5 were tentatively identified by comparison of HPLC retention times with
those of reference compounds (Walter et al., 2000). By alkaline hydrolysis of the
yellow pigment purified from mycorrhizal maize roots, besides mycorradicin, an
isomer pair of a cyclohexenone derivative was liberated, which was identified by
NMR spectroscopy as blumenol C 9-O-fl-cellobioside (10) (Fester et al., 2002a),
assumed to form esterification products (oligo- or polyesters) with mycorradicin,
establishing part of the yellow pigment.
MOLECULAR BIOLOGY
Traditionally, levels of metabolites, proteins, or transcripts of known identity

have been tested for being affected by a certain stimulus. In the case of the interaction of plant roots with a symbiotic partner, mineral nutrient transport proteins are
obvious choices. Recently, nontargeted approaches, particularly at the transcript
FIG. 4. Biosynthesis of isopentenyl diphosphate (IPP) via the MEP and mevalonate pathways leading to various terpenoids (Rohmer, 1999; Rodriguez-Concepcion and Boronat,
2002). The DXS- and DXR-catalyzed reactions are pointed out in this review. The pathways show the 13 C-labelling patterns of IPP and blumenol C, the aglycone of blumenin, that
accumulated in AM fungus inoculated barley roots after feeding of [1-13 C]glucose (Maier
et al., 1998). For a comparison, potential 13 C-labelling of mycorradicin via the MEP pathway and of IPP via the mevalonate pathway are shown (parts of the chart have been adapted
from Lichtenthaler et al., 1997; Rohmer, 1999). The 13 C enrichment in blumenol C determined by 13 C NMR spectroscopy is indicated by dots. The precursor carotenoid (shaded
in grey) is still elusive. Mycorradicin (R = H) is the core structure of the yellow pigment (R = glycosylated cyclohexenone derivatives) (Fester et al., 2002a). Abbreviations:
Ac-CoA, acetyl coenzyme A; AcAc-CoA, acetoacetyl-CoA; DHAP, dihydroxyacetone
phosphate; DXP, 1-deoxy-D-xylulose 5-phosphate; DXR, 1-deoxy-D-xylulose 5-phosphate
reductoisomerase; DXS, 1-deoxy-D-xylulose 5-phosphate synthase; GAP, glyceraldehyde
3-phosphate; HMG-CoA, fl-hydroxy-fl-methylglutaryl-CoA; IPP, isopentenyl diphosphate;
MEP, 2-C-methyl-D-erythritol 4-phosphate; MVA-5PP, mevalonate 5-diphosphate; TPP,
thiamine diphosphate.
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level, have become popular and have now also been applied to mycorrhizal systems (Lapopin and Franken, 2000; Franken and Requena, 2001; Stougaard, 2001).
Whole AM root transcriptomes (total mRNA transcripts at a specific stage of mycorrhization) can be captured in cDNA libraries. Partial sequencing of all or of
a fraction of clones in the library then results in so-called expressed sequence
tags (ESTs) (Journet et al., 2002). A biochemical function can often be attributed
to specific ESTs or to the proteins they encode by finding sequences with high
sequence similarity and a known function in DNA databases. If done on a sufficiently large scale, this approach can provide an, albeit still fragmentary, overview
of metabolic activities during the mycorrhizal symbiosis. Analysis of changes
in the levels of specific transcripts by RNA blot, real time PCR, or DNA array
methods can identify transcripts and genes and, thus, areas of metabolic activity
up- or downregulated during mycorrhization. Subtractive methods (subtraction
of nonmycorrhizal transcripts from the population of mycorrhiza-regulated and
mycorrhiza-unaffected transcripts) can reveal mycorrhiza-affected transcripts already at the cDNA cloning stage (Voiblet et al., 2001).
Diploid and autogamous plants with a small genome are particularly suitable
for such approaches. Unfortunately, the prime model plant Arabidopsis thaliana,
a member of the Brassicaceae, is not a host for AM fungi. However, extensive
efforts of groups in the United States, France, and Germany on the model legume
plant Medicago truncatula, which easily accommodates various symbiotic partners, have now led to the availability of more than 100,000 ESTs in databases from
various Medicago truncatula tissues (Journet et al., 2002). These include control
roots or roots colonized by AM fungi or other mutualistic and pathogenic microbes.
This resource now even allows various in-silico (computer-based) analyses, e.g.,
to carry out electronic Northern experiments by comparing the frequency of specific ESTs (representing transcript levels) from defined tissues and environmental
circumstances in the database. Unfortunately, fungal sequences with known identity are poorly or not at all represented in databases.
Another valuable resource are specific mutants of host plants, which are
blocked at certain stages of the AM fungal colonization. In Medicago truncatula,
many of these mutants are also disturbed in the accommodation of Rhizobium
bacteria forming nodules for nitrogen fixation. A recent example is the identification of SYMRK, a receptor-like kinase required for both fungal and bacterial
recognition (Stracke et al., 2002). Whereas this shows the existence of at least
one common signalling component for the recognition of two very different symbionts, characterization of other mutants argues for additional SYM-independent
signalling pathways (Kistner and Parniske, 2002).
One of the plants main benefits from the AM symbiosis is improvement of
phosphate uptake. Recent molecular studies of various phosphate transporters have
demonstrated how plants can adapt their phosphate uptake to the interaction with
the AM fungus. Specific phosphate transporters with different properties compared
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to those known so far are expressed in the arbusculated root cells. It is assumed
that they are located at the periarbuscular membrane where they are involved in the
acquisition of phosphate supplied by the fungus (Gianinazzi-Pearson et al., 1991;
Rausch et al., 2001; Harrison et al., 2002; Paszkowski et al., 2002). Phosphate
transporters active in nonmycorrhizal roots are downregulated. Interestingly, the
AM-specific transporter OsPT11 from rice is not an ortholog of the potato transporter StPT3. Thus, this feature may have evolved several times independently
(Paszkowski et al., 2002). The molecular mechanisms of phosphate transport in
plants are described in a recent review (Rausch and Bucher, 2002).
Isotopic labelling and NMR spectroscopy contributed significantly to our
understanding of the physiology of AM symbiosis (Douds et al., 2000; Pfeffer
et al., 2001). It was shown that glucose and fructose are effectively taken up by
the fungus within the root and are metabolized to yield mainly trehalose and
lipids (Wright et al., 1998; Pfeffer et al., 1999). The lipids are then translocated
to the extraradical mycelium, translocated within AM fungal colonies, and are
recirculated throughout the fungus (Bago et al., 2002). Carbon flux and gene
expression studies indicate that the glyoxylate cycle is central to the flow of carbon
in the AM symbiosis (Lammers et al., 2001).
The first molecular studies on plant secondary metabolites in AM roots were
carried out on phenylpropanoid metabolism in alfalfa and soybean. In alfalfa, increases in transcription levels of phenylalanine ammonia-lyase and chalcone isomerase were observed (Volpin et al., 1994). In soybean roots, however, the level
of chalcone isomerase decreased (Lambais and Mehdy, 1993). In Medicago truncatula and Phaseolus vulgaris, transcript levels of phenylalanine ammonia-lyase
and chalcone synthase increased (Harrison and Dixon, 1993; Blee and Anderson,
1996), whereas isoflavone reductase transcript formation was suppressed in Medicago truncatula (Harrison and Dixon, 1993). The latter correlated with a reduced
accumulation of the phytoalexin medicarpin.
As discussed above, the biosynthesis of apocarotenoids is known to proceed via the plastid-located nonmevalonate route, which is now commonly called
MEP pathway (Rodriguez-Concepcion and Boronat, 2002). Two key steps of the
MEP pathway, catalyzed by 1-deoxy-D-xylulose 5-phosphate synthase (DXS) and
1-deoxy-D-xylulose 5-phosphate reductoisomerase (DXR) (Figure 4), were investigated for changes in transcript levels upon AM formation. Levels of both DXS
and DXR transcripts were considerably higher in AM fungus-colonized roots of
various cereals compared to nonmycorrhizal roots (Walter et al., 2000). In a subsequent work with Medicago truncatula, two distantly related DXS transcripts were
identified, which both specified functional DXS proteins (Walter et al., 2002). Only
DXS2 exhibited elevated transcript levels in mycorrhizal roots, whereas DXS1 remained unaffected at a very low level during this interaction. Conversely, DXS1
was highly expressed in aerial photosynthetic tissues, where DXS2 transcripts
were low. Additional experiments with nonmycorrhizal and mycorrhizal maize
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and tomato plants corroborated these results. They indicate that there might be
a division of labor between DXS1, expressed for primary functions, such as supply of chloroplast components, and DXS2 whose expression profiles correlate with
formation of secondary compounds, such as (apo)carotenoids in mycorrhizal roots
(Walter et al., 2002).
The diversification of DXS enzymes and genes from the isopentenyl diphosphate-generating MEP pathway and their specific involvement in primary and
secondary products came as a surprise. Previously, assignment of enzymes to
primary and secondary isoprenoid formation was known only for a later step in
this pathway, namely the one catalyzed by various terpene synthases (Trapp and
Croteau, 2001). DXS2 genes and their promoters are currently being isolated in
our laboratory to identify regulatory sequences responsible for the differential,
and particularly the mycorrhiza-dependent, expression. The subsequent step in the
MEP pathway, catalyzed by DXR (Figure 4), does not appear to be diversified,
since a single DXR transcript species accumulates in leaves and mycorrhizal roots
(Hans, 2003).
Finally, production of the AM-specific apocarotenoids is catalyzed by dioxygenases. The first of these enzymes, characterized from the pathway leading to the
C15 apocarotenoid abscisic acid, was the vp14 of maize (Tan et al., 1997). A related
carotenoid-cleaving dioxygenase (CCD), generating C14 and C13 apocarotenoids,
was identified later (Schwartz et al., 2001). This enzyme could be involved in the
generation of AM-specific mycorradicin and cyclohexenone derivatives. Unpublished results from our work with maize and Medicago truncatula indicate that a
CCD transcript is mycorrhiza-regulated in roots (Hans, 2003). Taken together, the
AM-specific isoprenoid metabolism and apocarotenoid formation raise attractive
questions to study both the evolution of plant secondary metabolism and its role
in ecological interactions.
SUMMARY
Mutualistic symbioses of mycorrhizas are crucial in the ecology and physiology of terrestrial plants and are most effective in supporting plants to cope
with various environmental stressors, such as nutrient- and water-deficient soils
or pathogenic infection. With some recent success in mycorrhiza research on the
metabolic and genetic levels, we are beginning to understand the complexity of
the chemical dialogue of the two partners. We expect that the growing interest in
mycorrhiza research and availability of new analytical techniques and molecular
genetic approaches will lead in the near future to new insights into the strategies
of plants and fungi to develop mutualistic symbiotic associations. In addition,
understanding the mechanisms that prevent mycorrhizal colonization in nonhost
species will help to elucidate the molecular interactions responsible for a successful
establishment of mycorrhizal symbioses.
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AcknowledgmentsThe investigations at Halle have been supported by the Deutsche Forschungsgemeinschaft in Bonn (Research Focus Programme 1084: Molecular Basics of Mycorrhizal Symbioses) and Fonds der Chemischen Industrie in Frankfurt. We thank John T. Romeo (Tampa) for
encouraging us to write this review and T. Hartmann (Braunschweig) for comments on the manuscript.
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Journal of Chemical Ecology [joec]

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ARBUSCULAR MYCORRHIZA: BIOLOGICAL, CHEMICAL,

DIETER STRACK,1, THOMAS FESTER,1 BETTINA HAUSE,1

AbstractMycorrhizas are the most important mutualistic symbioses on earth.

To whom correspondence should be addressed. E-mail: dstrack@ipb-halle.de

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STRACK, FESTER, HAUSE, SCHLIEMANN, AND WALTER

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In accordance with the evolutionary history, AM symbioses can be found in

1999; Guadarrama and Alvarez-S

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FIG. 1. Morphology of the life cycle stages of an AM fungus, Glomus intraradices in a

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STRACK, FESTER, HAUSE, SCHLIEMANN, AND WALTER

The key feature of AMs is the arbuscule, a highly branched haustorium-like

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cytoplasmic architecture. Plant cytoskeletal components respond to the penetration

Journal of Chemical Ecology [joec]

STRACK, FESTER, HAUSE, SCHLIEMANN, AND WALTER

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STRACK, FESTER, HAUSE, SCHLIEMANN, AND WALTER

Despite increasing efforts in research on metabolic changes, virtually nothing

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Glc(100 60 )GlcGlc(100 60 )GlcGlcGlc(100 60 )GlcGlc(100 60 )(Glc1000 20 )GlcGlcGlc(100 40 )Glc-

Ta = Triticum aestivum; Zm = Zea mays.

= Nicotiana rustica; Nt = Nicotiana tabacum; Sc = Secale cereale;

Maier et al., 1995

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a Blumenin (in all compounds listed: Glc = fl-glucose; GlcUA = fl-glucuronate).

Journal of Chemical Ecology [joec]

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oxidized to a carboxyl group. This structure accumulates as 9-O-gentiobioside (5)

Traditionally, levels of metabolites, proteins, or transcripts of known identity

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