Physiological and Molecular Plant Pathology (1999) 55, 77–84

Article No. pmpp.1999.0215, available online at http :\www.idealibrary.com.on

COMMENTARY

Induced disease resistance : how do induced plants stop pathogens ?

R. H A M M E R S C H M I DT*
Department of Botany and Plant Pathology, Michigan State UniŠersity, U.S.A.

(Accepted for publication May 1999)

The phenomenon of induced or acquired resistance to disease in plants has been studied intensively in
recent years. This has led to a better understanding of the signaling pathways involved in the expression
of systemic resistance as well as the genetic regulation of induced or acquired resistance. Although the
induction of resistance to disease results in the expression of less disease in the plant after challenge with
pathogens, how the plant is able to restrict the development of the pathogen is not clearly defined. In this
paper, some of the defenses expressed in plants with induced resistance will be discussed in relation to how
the induced plants may restrict disease development. # 1999 Academic Press

Keywords : systemic acquired resistance ; induced systemic resistance ; SAR ; ISR ; salicylic acid ; defense ;
PR proteins ; phytoalexins ; lignification ; papillae.

process. SAR can also be induced by exogenous ap-

INTRODUCTION
Localized treatment of plants with virulent or avirulent
pathogens that cause necrotic lesions, with certain non-
pathogens, or with certain biotic or abiotic chemicals can
result in the local or systemic induction of disease resistance
in the treated plant to subsequent pathogen attack
[24, 26–28, 38, 40, 65, 72 ]. Resistance induced by these
pretreatments is generally characterized by a reduction
in the size and\or number of lesions that develop after
inoculation of the induced plant with virulent and
sometimes, hypersensitive response inducing avirulent
forms of pathogens. This induced form of resistance can
occur in the absence of major parasite specific genes for
resistance in the plant but likely uses the same defenses
that are used in other forms of resistance [31 ].
Induced resistance to pathogens can be subdivided into
two broad categories. The first of these is systemic
acquired resistance, or SAR [27, 28, 65, 72 ]. This type of
resistance develops either locally or systemically in
response to a pathogen that causes a necrotic lesion. The
necrotic lesion can either be the result of a successful
infection or a hypersensitive response (HR). The resistance
expressed is generally effective against a broad range of
pathogens, is associated with the production of PR
proteins, and is mediated via a salicylic acid dependent
* All correspondence should be addressed to : R. Hammer-
schmidt, email : hammers1!pilot.msu.edu ; Fax : 1517 353 1926 ;
Department of Botany and Plant Pathology, Michigan State
University, East Lansing, MI 48824-1312, U.S.A.
0885–5765\99\080077j08 $30.00\0
plication of salicylic acid or synthetic compounds such as
CGA-245704 (a benzothiadiazole derivative referred to as
‘‘ BTH ’’) and CGA-41396 (2,6-dichloroisonicotinic acid
or ‘‘ INA ’’) that appear to act similarly to salicylic acid
[38, 41 ]. The second type of induced resistance develops
systemically in response to colonization of plant roots by
certain rhizosphere bacteria, known as plant growth
promoting rhizobacteria or PGPR [72 ]. This type of
resistance, known as induced systemic resistance or ISR
[72 ], is mediated by a jasmonate\ethylene sensitive
pathway and does not involve expression of PR proteins
[52, 72 ].
Genetic analysis of SAR has resulted in the identification
and cloning of several genes that appear to be key to the
regulation of this type of resistance. A series of mutants
that express constitutive resistance in a susceptible host
background have been described in Arabidopsis. These
include both mutants that express spontaneous lesions
(e.g. lsd mutants) [16, 76 ] as well as one class that
expresses resistance without spontaneous lesions (e.g. cpr
mutants) [2 ]. Another class of mutants isolated from
Arabidopsis was found by screening for lack of resistance
expression in response to salicylic acid or synthetic
resistance activators. This screen resulted in the isolation
of the npr1 or sai1 mutant [5, 6, 15, 56, 58 ]. This is an
important finding as this gene is key in the expression of
salicylic acid-mediated resistance. Use of transgenic
technology has further allowed evaluation of salicylic acid
[14, 25 ] and catalases [18 ] in the signaling pathway that
leads to resistance. In addition, mutants that are
# 1999 Academic Press
78 R. Hammerschmidt
insensitive to jasmonic acid or cannot synthesize this
signal molecule have been valuable in understanding the
regulation of jasmonate-dependent ISR type of induced
resistance [52, 73 ].
Understanding the genetic regulation of SAR and ISR
is important in determining how plants are capable of
transducing the signals generated during infection that
lead to the expression of putative defense genes and the
ability of the plant to mount effective resistance against a
wide range of pathogens. However, a major question that
needs to be addressed is how the induced resistance
phenotype is expressed and why pathogens do not cause
symptoms or spread in induced tissues. In other words,
what stops pathogen development in tissue expressing
SAR and ISR ? In this paper, I will examine some
examples of how plants expressing some form of induced
resistance respond to challenge by pathogens. I will
generically refer to all plants expressing greater levels of
resistance after induction as being ‘‘ induced ’’ or having
‘‘ induced disease resistance ’’.
PRECHALLENGE CHANGES IN PLANTS
EXPRESSING INDUCED RESISTANCE
As described above, one of the results of inducing the SAR
type of induced resistance in plants is the systemic
expression of PR proteins [71 ]. Roles for PR proteins can
easily be imagined by their activity as glucanases or
chitinases or by their association with other antimicrobial
properties [71 ]. The location of many of the PR proteins
in the apoplast also suggests that these proteins are
positioned to come into contact with the pathogen during
the infection process [71 ]. Transformation of plants with
PR genes has also been shown to enhance the resistance of
plants to selected pathogens, thus supporting a role for PR
gene expression with the acquired resistance state [1, 45 ].
Similarly, analysis of mutants that constitutively express
PR genes also support the observations that PR proteins
are correlated with acquired resistance [2, 78 ]. However,
transgenic plants expressing PR genes do not necessarily
become more resistant to all pathogens e.g., [44 ],
suggesting that PR proteins are only part of the induced
disease resistance phenotype. What is not evident from
these studies is how PR proteins directly contribute to
resistance and, if they do, to what degree they contribute
to resistance.
There are two obvious mechanistic roles that the PR
proteins can play in SAR. The first is to directly block the
development of fungal, oomycete and bacterial pathogens
via hydrolytic action on pathogen cell walls or by other
antimicrobial activity [71 ]. The enzymatic activity of the
glucanases and chitinases may also aid indirectly in
resistance through the release of non-specific elicitors [77 ].
Although there is in Šitro evidence to support these roles,
demonstration that the PR proteins exert direct anti-
pathogenic activity in the plant and\or release elicitors is
lacking. The real challenge is to determine how the PR
proteins act in the plant, and approaches to demonstrate
the direct antimicrobial activity, pathogen lysis, and\or
elicitor release in plants with acquired resistance are
needed.
POST-CHALLENGE RESPONSES OF PLANTS
EXPRESSING INDUCED RESISTANCE
Unlike the biochemical changes that occur in plants as a
result of a resistance inducing treatment, there have been
fewer studies on the response of the induced host plant to
subsequent infection. In this section, examples of host-
responses expressed after challenge of induced tissues with
fungi (including oomycetes), bacteria and viruses will be
discussed and evaluated as potential defenses.
Fungi and Oomycetes
Induced disease resistance of green bean (Phaseolus
Šulgaris L.) to Colletotrichum lindemuthianum has been
reported to be a localized phenomenon in several plant
parts [21, 61 ], induced at a short distance from the site
of resistance induction in etiolated hypocotyls [19, 20 ], as
well as a systemic phenomenon in larger, green plants [9 ].
In hypocotyl tissues, the early stages development of a
compatible race of C. lindemuthianum into the tissue
expressing induced resistance was similar to that seen in
control tissues [19 ]. The fungus produced appressoria,
penetrated into the tissue, and established primary
infection hyphae in both control and induced plants. This
is clearly different from the hypersensitive reaction
expressed by host tissues after inoculation with an
incompatible race of the fungus. Only after the es-
tablishment of the primary hyphae were differences
observed between the control and induced plants. In the
control plants, rapidly spreading secondary hyphae
developed from the primary hyphae. However, in the
induced plants, the hyphae stopped development at the
primary hyphae stage. The cessation of hyphal de-
velopment was followed by browning of the host cells
(possibly a delayed hypersensitive response ?) and ac-
cumulation of phytoalexins [22 ]. The development of C.
lindemuthianum in induced tissues was similar to that
observed for age-related resistance of bean to compatible
races of C. lindemuthianum. Because the age-related re-
sistance of soybean hypocotyls to Phytophthora megasperma
var. sojae is associated with phytoalexin production [42 ],
it would be interesting to determine if age related
resistance in bean exhibited the same pattern of phyto-
alexin production seen in the induced tissues.
 Induced disease resistance : how do induced plants stop pathogens ?
Based on the timing of cytological events described
above, it is difficult to determine if the induced disease
resistance was operating via more ‘‘ traditional ’’ defenses
(e.g. hypersensitivity, phytoalexins) and\or by influencing
the ability of the pathogen to make the developmental
shift from its biotrophic mode of infection its necrotrophic
phase. The latter mechanism was briefly discussed by
Elliston et al. [19 ] in relation to other research that
suggested a correlation between secretion of poly-
galacturonases and the conversion from the biotrophic
phase to necrotrophic phase. Elliston et al. [19 ] suggested
that perhaps changes in cell wall chemistry caused by the
induction resulted in the inability of the pathogen to shift
from primary to secondary hyphae because of inactivity of
the polygalacturonase on cells walls in induced tissue.
Showalter et al. [59 ] demonstrated that bean hypocotyl
tissues adjacent to sites inoculated with an incompatible
race of C. lindemuthianum had strongly elevated transcripts
for hydroxyproline rich glycoproteins. Because cell walls
enriched in these proteins are less susceptible to pectin-
ases than are non-modified walls [64 ], the role of
structural changes in bean cell walls in relation to induced
disease resistance described for bean hypocotyls merits
further investigation.
In contrast to the hypocotyl studies by Elliston et al.
[19–22 ] induced disease, the resistance response of bean
leaves to C. lindemuthianum induced by a prior inoculation
of lower leaves with the same fungus was associated with
reduced numbers of infections from appressoria [9 ]. The
decreased penetration was associated with rapid formation
of papillae under appressoria. Thus, the lack of disease in
induced tissues could be attributed to a lack of penetration
into the leaf tissue by the pathogen.
A similar lack of penetration by fungi occurs in
cucumber plants in which the expression of induced
disease resistance to leaf infecting fungi has been associated
with the rapid modification of the outer epidermal cell
wall of the host at the point of attempted infection
[10, 30, 39, 66 ]. The cytology of the induced resistance
response to Colletotrichum orbiculare has been studied in the
most detail, and it has been shown that there is a rough
inverse relationship between the number of successful
penetrations in control plants with the number of
unsuccessful penetrations in induced plants [30, 54 ].
Histochemistry has been used to detect both lignin and
callose deposits under the appressoria that have not
successfully penetrated [30, 39 ]. Ultrastructural analysis
has also demonstrated that outer epidermal cell walls are
modified under appressoria and that these modifications
include phenolic compounds and silicon [63 ].
Modification of the epidermal cell wall directly beneath
an appressorium is a possible explanation for the failure of
fungal pathogens to successfully penetrate cucumber
leaves expressing induced disease resistance. The failure to
penetrate into tissues also provides a logical explanation
79
for the reduced size and numbers of lesions that develop
in cucumber with induced disease resistance. However, it
is not clear which (if any) of the cell wall modifications are
key in blocking pathogen entry into the tissue and if these
changes are the cause of the resistance or occur only after
the infection has been aborted.
Not all appressoria that form on cucumber epidermal
cells are blocked from penetrating into the tissue [30 ]. In
some cases, primary infection hyphae form but appear to
be encased in a lignin-like polymer which could effectively
block further development of the hyphae [63 ], or the
entire epidermal cell lignifies [39 ]. On the other hand, a
small percentage of the appressoria produce penetration
pegs that result in successful infection into the tissue and
no obvious host response [30, 54 ]. This is an important
observation because it helps to explain why induced
disease resistance to C. orbiculare is expressed as fewer and
smaller compatible appearing lesions and not always the
complete inhibition of disease.
The successful penetration by some (but not all)
appressoria into induced tissues, however, raises two
questions. The first relates to why host cells in induced
plants respond quickly to infection. This is a subject I will
return to later. The second concerns the role of PR
proteins and other systemically induced enzymes. Induced
disease resistance in cucumber is accompanied by the
accumulation of chitinase [49 ] and peroxidase [30, 62 ] in
the extracellular spaces of the host tissues after and
inducing treatment. Although a possible role in enhanced
lignification ability can be hypothesized for the peroxidase
[29 ], direct evidence to support this role is lacking.
Hyphae of C. orbiculare that have successfully penetrated
into induced leaves should come into contact with
chitinases, yet there is no evidence that indicates that
hyphal growth is restricted after it becomes established or
that these enzymes directly interact with the pathogen.
The observation that both chitinase and peroxidase
activity remain high in cucumber leaves from plants in
which the induced resistance state is no longer present
suggests that the presence of these enzymes is not sufficient
to explain the induced resistance state [11 ].
Post-inoculation studies of induced tissues have also
been carried out with Oomycetes. For example, Arabidopsis
leaves with acquired resistance are penetrated by Peronos-
pora parastica, but the pathogen does not develop [41, 47 ].
A ‘‘ trailing necrosis ’’ of host cells along the hyphae has
been observed in induced leaf tissue [70 ]. Lignification
has been reported to contribute to parasite-specific
resistance in this system [48 ], and the cytological pattern
of lignification appears similar to the pattern of host
necrosis observed in the response of induced disease plants
to Peronospora. Thus, it would seem likely that lignification
is also part of the induced disease resistance defenses in
Arabidopsis. However, since multiple defenses are likely to
be expressed [31 ], lignification in induced resistance will
80 R. Hammerschmidt
likely play a partial role in defense as it does in parasite-
specific resistance.
Bacteria
Induced resistance to bacterial pathogens has also been
examined. Early studies by Lozano and Sequeira dem-
onstrated that infiltration of tobacco leaves with heat-
killed cells of Ralstonia solanacearum would induce local
resistance against the same pathogen [46 ]. Interestingly,
the heat killed cells also protected the tissue against the
hypersensitive response elicited by an avirulent R.
solanacearum isolate [46 ]. The induced resistance was
associated with less growth of challenge bacteria in
induced tissue [46 ] and the production of inhibitory
substances [53 ].
Systemic induced or acquired resistance to virulent and
avirulent bacterial pathogens has also been reported as a
decrease in necrotic symptoms [3, 4, 7, 17, 41, 67, 70 ]. The
lack of necrotic symptoms that develop in induced disease-
expressing plants after inoculation with bacteria has been
hypothesized to be the result of a suppression of disease or
confluent HR symptoms [16 ]. Based on the observation
that bacterial populations in control plants were no
different to those observed in plants expressing induced
disease resistance [17 ]. An increase in antioxidants has
been reported to occur systemically in tobacco in response
to resistance inductions and in response to salicylic acid
treatment, and this change in antioxidant status has been
proposed to be the basis for necrotic lesion suppression
[23 ].
In most studies of the effect of resistance induction on
bacteria, there is suppression of bacterial growth in
induced plants of one to three orders of magnitude as
compared to control plants [3, 4, 7, 41, 70 ]. This suggests
that inhibitors of bacterial growth are produced as a result
of resistance induction or that the plant responds quickly
to inoculation by production of bacterial growth in-
hibitors. To my knowledge, there have been no studies
demonstrating systemic changes in compounds known to
be antibacterial in plants expressing induced disease
resistance either before or after challenge. However,
induced Arabidopsis plants respond to Pseudomonas chal-
lenge inoculation with enhanced salicylic acid accumu-
lation and induction of PR-1 gene transcription [4 ]. The
apoplastic class III acidic chitinase from cucumber has
homology to lysozyme and is produced as a cucumber PR
protein [49 ], but neither the activity of this enzyme
against bacteria nor the further accumulation of this
enzyme after bacterial challenge have been reported.
Because there is a certain threshold of bacterial cells
required to cause a visible, confluent HR or rapid
development of disease associated necrosis [69 ], it is
possible that inhibitors (either produced as a result of
induction or challenge) may keep the population of
bacterial cells below the threshold needed for macroscopic
symptom development. This reduction in bacterial popu-
lation in leaf tissue could account for the induced resistance
phenotype observed after challenge with bacteria.
Recently, resistance in the absence of hypersensitive
necrosis has been partially characterized in dnd1 mutants
of Arabidopsis [78 ]. Plants with this mutation constitutively
express PR-1 and glucanase genes, contain higher levels of
salicylic acid, and appear to express constitutive acquired
resistance to P. syringae. Populations of P. syringae in dnd1
plants are decreased by about one order of magnitude
below that seen in wild type. dnd1 plants respond to
challenge inoculation with virulent P. syringae by further
induction of PR-1 and glucanase. This suggests that part
of the observed resistance may be the result of post-
inoculation defense expression and not just a masking of
symptoms. Inoculation of dnd1 plants with avirulent
isolates of P. syringae results in a lack of HR expression, but
bacterial populations are even lower than seen with the
virulent isolates in dnd1 plants. This parasite-specific
resistance, which follows a gene-for-gene relationship, is
accompanied by even greater PR-1 and glucanase
expression after challenge than is seen after inoculation
with a compatible P. syringae. Thus, even the expression of
resistance in the dnd1 plants, which behave very similarly
to plants with acquired resistance, is accompanied by
further induction of defense after challenge suggesting
that the suppression of symptoms may be due to the rapid
inhibition of bacterial growth.
The lack of necrotic lesions caused by virulent and
avirulent bacteria in induced plants is similar to what is
seen in plants infiltrated with hrp mutants [43 ]. Compared
to wild type virulent and avirulent strains, hrp mutants
multiply in plant tissues to levels one or more orders of
magnitude lower than wild type strains [43 ]. Since the hrp
mutants grow normally in vitro, it is possible that host
factors restrict their growth. Jakobek and Lindgren [32 ]
found that hrp mutants of P. syringae induce transcription
of genes associated with active defense and the ac-
cumulation of phytoalexins. New gene transcripts were
observed within one hour of inoculation. Thus one possible
scenario that may account for the suppression of disease is
a rapid induction of defenses that may slow or stop the
growth of the bacteria in planta. These induced defenses
may prevent the bacteria from reaching the critical
populations needed to cause necrosis or may in some way
inhibit the production of factors required by the bacteria
to initiate cell death.
Viruses
The classic studies of Ross [55 ] demonstrated that local
inoculation of N gene tobacco with TMV results in a
 Induced disease resistance : how do induced plants stop pathogens ?
systemic increase in resistance that is characterized by a
decrease in both necrotic lesion size and number. This
suggests that the induced resistance state decreases the
replication and\or spread of the virus. Although it has
been proposed that the observed induced resistance to
viruses, like bacteria, is due to a suppression of necrotic
symptoms [68 ], recent evidence supports enhanced defense
that acts by suppressing the infection and not the
symptoms.
Induced disease resistance in tobacco to TMV also
appears to be the result of an effect on the virus. Mur et
al. [50 ] demonstrated that transgenic tobacco expressing
salicylate hydroxylase to suppress salicylic acid accumu-
lation resulted in greater spread of TMV in N gene
tobacco even though the necrotic phenotype was still
expressed. This result can be explained in part by the
observation that salicylic acid induces mechanisms that
interfere with TMV replication in both N gene (hyper-
sensitively resistant) and nn (susceptible) genotypes of
tobacco [8 ]. The fact that the salicylic acid affected TMV
replication was observed in the susceptible tobacco,
strongly supports the role of salicylate-mediated resistance
operating via an effect on replication and not symptom
development. In a subsequent study, salicylic acid
mediated resistance of tobacco to PVY and CMV was
found to be related to inhibition of viral replication and
movement, respectively [51 ].
Treatment of Arabidopsis with the synthetic plant
activator CGA-245704 results in resistance to turnip
crinkle virus (TCV) [41 ]. This resistance is characterized
by a decrease in necrotic symptoms. The decrease in
symptoms is apparently due to inhibition of viral
replication as no viral RNA could be detected in the
plant.
Thus, at least for salicylate-dependent induced re-
sistance (SAR), the observed resistance phenotype may
be explained by either an effect on viral replication or
viral movement. Either mode of action would result in
decreased disease expression. However, the biochemical
mechanism involved in suppressing viral replication or
movement has yet to be elucidated.
WHY DOES AN INDUCED PLANT RESPOND
MORE QUICKLY TO AN ATTEMPTED
INFECTION ?
The research reviewed in this paper shows that plants
with induced resistance respond to infection by some type
of host response that restricts the development of
pathogens. With fungi, the deposition of structural barriers
occurs commonly in response to infection and decreases in
bacterial and viral reproduction are observed in plants
expressing induced disease resistance. What is not known
is how the plant is capable of rapidly responding to
infection.
81
In parasite specific resistance, R gene products are
hypothesized to recognize pathogen avirulence gene
products, and this recognition leads to the expression of
defense [31 ]. This model seems unlikely in the case of
acquired or induced resistance, yet many of the same
types of defense responses or patterns of pathogen
suppression are observed in both. One possible expla-
nation is that the PR proteins act to release non-specific
elicitors from the cell walls of fungi or bacteria, and these
elicitors quickly trigger defenses [77 ]. Similarly, PR
proteins may inhibit bacterial or fungal development
much like certain fungicides, and the inhibited pathogens
may release elicitors that trigger defenses. This type of
response has been seen in soybean where metalaxyl pre-
treatment protects soybean against infection by Phyto-
phthora megasperma var. sojae, and part of the protection is
associated with a rapid production of glyceollin at the
infection site (presumably due to release of elicitors from
the metalaxyl-weakened pathogen) [74, 75 ].
In addition to direct effects on pathogens by PR
proteins, the induced plant tissues may be conditioned to
respond very quickly to infection [33–37, 60 ]. Cucumber
plants expressing SAR will lignify more rapidly in response
to wounding [12 ], and this enhanced lignification capacity
may be readily triggered by the wound induced by fungal
penetration. This enhanced ability to lignify may also
help explain the decrease in viral infection after mech-
anical (wound) inoculation with viruses. Callose de-
position has also been associated with cucumber induced
disease resistance, and SAR expressing plant have elevated
levels of a β-1,3-glucan synthase [57 ] which may
contribute to rapid callose synthesis at infection sites [39 ].
Cucumber plants pretreated with salicylic acid or syn-
thetic resistance activators that mimic salicylic acid
respond quickly to infection by production of hydrogen
peroxide [37 ]. The source of the hydrogen peroxide is not
known, although it is tempting to speculate that the
apoplastic peroxidases that are systemically induced in
cucumber may be involved [29 ].
CONCLUSIONS
It is clear that plants can express induced resistance to
pathogens after a prior infection or other resistance
activating treatment. Significant advances have been
made in understanding the genes that are involved in
regulating the resistant state as well as the chemical
signals that modulate the response. The lack of disease
expressed in induced plants can also be explained, at least
at one level by a lack of fungal, bacterial or viral
development in plants. However, these studies have not
conclusively revealed the mechanism or mechanisms that
actually stop pathogenesis.
To fully understand the induced resistance phenom-
enon, future research should focus on critically evaluating
82 R. Hammerschmidt
the roles of the putative defenses identified thus far in the
expression of resistance. Use of transgenic plants that are
suppressed in the production of PR proteins is one
approach that can be used to evaluate the relative
contribution of these proteins in the defense response. In
addition, attempts should be made to find mutants that
cannot express a specific defense. These mutants should
ideally not be regulatory mutants that affect a number of
defenses or defenses expressed to only a few pathogens
types, but rather the mutants should each specifically
block a single defense. Phytoalexin biosynthetic mutants
would be ideal to test the role of these compounds in
induced disease resistance (as well as other forms of
resistance). Understanding which defenses are causally
involved in induced resistance should also allow for the
better development of sound strategies to develop trans-
genic plants that resist disease, as well as provide new
insight into how plants expressing other forms of resistance
[31 ] restrict pathogen development.
Support from the Michigan Agricultural Experiment
Station and the USDA NRICGP is gratefully acknow-
ledged.
REFERENCES
1. Alexander D, Goodman RM, Gut-Rella M, Glascock
C, Weyman K, Friedrich L, Maddox D, Ahl-Goy P,
Luntz T, Ward E, Ryals J. 1993. Increased tolerance to
two oomycete pathogens in transgenic tobacco expressing
pathogenesis-related protein 1a. Proceedings of the National
Academy of Sciences, USA 90 : 7327–7331.
2. Bowling SA, Guo A, Cao H, Gordon AS, Klessig DF,
Dong X. 1994. A mutation in Arabidopsis that leads to
constitutive expression of systemic acquired resistance.
The Plant Cell 6 : 1845–1857.
3. Cameron RK, Dixon R, Lamb CJ. 1994. Biologically
induced systemic acquired resistance in Arabidopsis thaliana.
The Plant Journal 5 : 715–725.
4. Cameron RC, Paiva NL, Lamb CJ, Dixon RA. 1999.
Accumulation of salicylic acid and PR-1 gene transcripts
in relation to the systemic acquired resistance (SAR)
response acquired by Pseudomonas syringae pv. Syringae in
Arabidopsis. Physiological and Molecular Plant Pathology 55 :
121–130.
5. Cao H, Bowling SA, Gordon AS, Dong X. 1994.
Characterization of an Arabidopsis mutant that is non-
responsive to inducers of systemic acquired resistance. The
Plant Cell 6 : 1583–1592.
6. Cao H, Glazebrook J, Clarke JD, Volko S, Dong X.
1997. The Arabidopsis NPR1 gene that controls systemic
acquired resistance encodes a novel protein containing
ankyrin repeats. Cell 88 : 57–63.
7. Caruso FL, Kuc! J. 1979. Induced systemic resistance of
cucumber to anthracnose and angular leaf spot by
Pseudomonas lachrymans and Colletotrichum lagenarium. Physio-
logical Plant Pathology 14 : 191–201.
8. Chivasa S, Murphy AM, Naylor M, Carr JP. 1997.
Salicylic acid interferes with tobacco mosaic virus rep-
lication via a novel salicylhydroxamic acid-sensitive
mechanism. The Plant Cell 9 : 547–557.
9. Cloud AME, Deverall BJ. 1987. Induction and expression
of systemic resistance to the anthracnose disease in bean.
Plant Pathology 36 : 551–557.
10. Conti G, Bassi M, Carminucci D, Gatti L, Bocci AM.
1990. Preinoculation with tobacco necrosis virus enhances
peroxidase activity and lignification in cucumber as a
resistance response to Sphaerotheca fuliginea. Journal of
Phytopathology 128 : 191–202.
11. Dalisay RF, Kuc! JA. 1995. Persistence of reduced pen-
etration by Colletotrichum lagenarium into cucumber leaves
with induced systemic resistance and its relation to
enhanced peroxidase and chitinase activities. Physiological
and Molecular Plant Pathology 47 : 329–338.
12. Dean RA, Kuc! J. 1987. Rapid lignification in response to
wounding and infection as a mechanism for induced
systemic protection in cucumber. Physiological and Molecular
Plant Pathology 31 : 69–81.
13. Delaney TP, Uknes S, Vernooij B, Friedrich L,
Weymann K, Negrotto D, Gaffney T, Gut-Rella M,
Kessmann H, Ward E, Ryals J. 1994. A central role of
salicylic acid in plant disease resistance. Science 266 :
1247–1250.
14. Delaney T. 1997. Genetic dissection of acquired resistance
to disease. Plant Physiology 113 : 5–12.
15. Delaney TP, Friedrich L, Ryals J. 1995. Arabidopsis signal
transduction mutant defective in chemically and bio-
logically induced disease resistance. Proceedings of the
National Academy of Sciences, USA 92 : 6602–6606.
16. Dietrich RA, Delaney TP, Uknes SJ, Ward ER, Ryals
JA, Dangl JL. 1994. Arabidopsis mutants simulating
disease response. Cell 77 : 565–577.
17. Doss M, Hevisi M. 1981. Systemic acquired resistance of
cucumber to Pseudomonas lachrymans as expressed in
suppression of symptoms, but not in multiplication of
bacteria. Acta Phytopathologica Scientarum Hungaricae 16 :
269–272.
18. Du H, Klessig DF. 1997. Role for salicylic acid in the
activation of defense responses in catalase-deficient trans-
genic tobacco. Molecular Plant-Microbe Interactions 10 :
922–925.
19. Elliston J, Kuc! J, Williams EB. 1976. A comparative
study of the development of compatible, incompatible, and
induced incompatible interactions between Colletotrichum
spp. and Phaseolus Šulgaris. Phytopathologische Zeitschrift 87 :
289–303.
20. Elliston J, Kuc! J, Williams EB. 1971. Induced resistance
to bean anthracnose at a distance from the site of the
inducing interaction. Phytopathology 61 : 1110–1112.
21. Elliston J, Kuc! J, Williams EB. 1976. Protection of
Phaseolus Šulgaris against anthracnose by Colletotrichum
species nonpathogenic to bean. Phytopathologische Zeitschrift
86 : 117–126.
22. Elliston J, Kuc! J, Williams EB, Rahe JE. 1977.
Relationship of phytoalexin accumulation to local and
systemic protection of bean against anthracnose. Phyto-
pathologische Zeitschrift 88 : 114–130.
23. Fodor J, Gullner G, Adam AL, Barna B, Komives T,
Kiraly Z. 1997. Local and systemic responses to anti-
oxidants to tobacco mosaic virus infection and to salicylic
acid to tobacco. Role in systemic acquired resistance. Plant
Physiology 114 : 1443–1451.
24. Friedrich L, Lawton K, Ruess W, Masner P, Specker
N, Rella MG, Meier B, Dincher S, Staub T, Uknes S,
Me! traux JP, Kessmann H, Ryals J. 1996. A benzo-
thiadiazole derivative induces systemic acquired resistance
in tobacco. The Plant Journal 10 : 61–70.
 Induced disease resistance : how do induced plants stop pathogens ?
25. Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye
G, Uknes S, Ward E, Kessmann H, Ryals J. 1993.
Requirement of salicylic acid for the induction of systemic
acquired resistance. Science 261 : 754–766.
26. Gorlach J, Volrath S, Knauf-Beiter G, Hengy G,
Beckhove U, Kogel KH, Oostendorp M, Staub T,
Ward E, Kessmann H, Ryals J. 1996. Benzothiadiazole,
a novel class of inducers of systemic acquired resistance,
activates gene expression and disease resistance in wheat.
The Plant Cell 8 : 629–643.
27. Hammerschmidt R, Becker JS. 1997. Acquired resistance
to disease. Horticultural ReŠiews 18 : 247–289.
28. Hammerschmidt R, Dann EK. 1997. Induced resistance
to disease. In : Rechcigl NA, Rechcigl JE, ed. EnŠiron-
mentally Safe Approaches to Plant Disease Control. Boca Raton,
FL, U.S.A. : CRC Lewis Publishers, 177–199.
29. Hammerschmidt R, Nuckles EM, Kuc! J. 1982. As-
sociation of enhanced peroxidase activity with induced
systemic resistance of cucumber to Colletotrichum lagenarium.
Physiological Plant Pathology 20 : 73–82.
30. Hammerschmidt R, Kuc! J. 1982. Lignification as a
mechanism for induced systemic resistance in cucumber.
Physiological Plant Pathology 20 : 61–71.
31. Heath MC. 1995. Thoughts on the role and evolution of
induced resistance in natural ecosystems, and its re-
lationship to other types of plant defenses. In : Hammer-
schmidt R, Kuc! J, eds. Induced Resistance to Disease in Plants.
Kluwer : Dordrecht, 141–151.
32. Jakobek JL, Lindgren PB. 1993. Generalized induction of
defense responses in bean is not correlated with the
induction of the hypersensitive reaction. The Plant Cell 5 :
49–56.
33. Kastner B, Tenhaken R, Kauss H. 1998. Chitinase in
cucumber hypocotyls is induced by germinating fungal
spores and by fungal elicitor in synergism with inducers of
acquired. The Plant Journal 13 : 447–454.
34. Katz VA, Thulke OU, Conrath U. 1998. A benzothia-
diazole primes parsley cells for augmented elicitation of
defense responses. Plant Physiology 117 : 1333–1339.
35. Kauss H, Franke R, Krause K, Conrath U, Jeblick W,
Grimming B, Matern U. 1993. Conditioning of parsley
Petroselinum crispum L. suspension cells increases elicitor-
induced incorporation of cell wall phenolics. Plant Physi-
ology 102 : 459–466.
36. Kauss H, Jeblick W. 1995. Pretreatment of parsley
suspension cultures with salicylic acid enhances spon-
taneous and elicited production of H O . Plant Physiology
# #
108 : 1171–1178.
37. Kauss H, Jeblick W. 1996. Influence of salicylic acid on
the induction of competence for H O elicitation : com-
# #
parison of ergosterol with other elicitors. Plant Physiology
111 : 755–763.
38. Kessmann H, Staub T, Hofmann C, Maetzke T, Herzog
J, Ward E, Uknes S, Ryals J. 1994. Induction of
systemic acquired disease resistance in plants by chemicals.
Annual ReŠiew of Phytopathology 32 : 439–459.
39. Kovats K, Binder A, Hohl HR. 1991. Cytology of induced
systemic resistance of cucumber to Colletotrichum lagenarium.
Planta 183 : 484–490.
40. Kuc! J. 1982. Induced immunity to plant disease. BioScience
32 : 854–860.
41. Lawton KA, Friedrich L, Hunt M, Weymann K,
Delaney T, Kessmann H, Staub T, Ryals J. 1996.
Benzothiadiazole induces disease resistance in Arabidopsis
by activation of the systemic acquired resistance signal
transduction pathway. The Plant Journal 10 : 71–82.
83
42. Lazarovits G, Sto$ ssel P, Ward EWB. 1981. Age-related
changes in specificity and glyceollin production in the
hypocotyl reaction of soybeans to Phytophthora megasperma
var. sojae. Phytopathology 71 : 94–97.
43. Lindgren PB, Peet RC, Panopoulos N. 1986. Gene
cluster of Pseudomonas syringae pv. phaseolicola controls
pathogenicity of bean plants and hypersensitivity on
nonhost plants. Journal of Bacteriology 168 : 512–522.
44. Linthorst HJM, Meuwissen RLJ, Kauffmann S, Bol
JF. 1989. Constitutive expression of pathogenesis-related
proteins PR-1, GRP, and PR-S in tobacco has no effect on
virus infection. The Plant Cell 1 : 285–291.
45. Liu D, Raghothama KG, Hasegawa PM, Bressan RA.
1994. Osmotin overexpression in potato delays devel-
opment of disease symptoms. Proceedings of the National
Academy of Sciences, USA 91 : 1888–1892.
46. Lozano JC, Sequeira L. 1970. Prevention of the hy-
persensitive reaction in tobacco by heat-killed bacterial
cells. Phytopathology 60 : 875–879.
47. Mauch-Mani B, Slusarenko AJ. 1994. Systemic acquired
resistance in Arabidopsis thaliana induced by a predisposing
infection with a pathogenic isolate of Fusarium oxysporum.
Molecular Plant-Microbe Interactions 7 : 378–383.
48. Mauch-Mani B, Slusarenko AJ. 1996. Production of
salicylic acid precursors is a major function of phenyl-
alanine ammonia-lyase in the resistance of Arabidopsis to
Peronospora parasitica. The Plant Cell 8 : 203–212.
49. Me! traux JP, Burkhart W, Moyer M, Dincher S,
Middlesteadt W, Williams S, Payne G, Carnes M,
Ryals J. 1989. Isolation of a complementary DNA
encoding a chitinase with structural homology to a
bifunctional lysozyme\chitinase. Proceedings of the National
Academy of Sciences, USA 86 : 896–900.
50. Mur LAJ, Bi YM, Darby RM, Firek S, Draper J. 1997.
Compromising early salicylic acid accumulation delays
the hypersensitive response and increases viral dispersal
during lesion establishment in TMV-infected tobacco.
The Plant Journal 12 : 1113–1126.
51. Naylor M, Murphy AM, Berry JO, Carr JP. 1998.
Salicylic Acid Can Induce Resistance to Plant Virus
Movement. Molecular Plant-Microbe Interactions 11 :
860–868.
52. Pieterse CMJ, van Wees SCM, van Pelt JA, Knoester M,
Laan R, Gerrits H, Weisbeek PJ, van Loon LC. 1998.
A novel signaling pathway controlling induced systemic
resistance in Arabidopsis. The Plant Cell 10 : 1571–1580.
53. Rathmell WG, Sequeira L. 1975. Induced resistance in
tobacco leaves : the role of inhibitors of bacterial growth in
the intercellular fluid. Physiological Plant Pathology 5 : 65–73.
54. Richmond S, Elliston JE, Kuc! J. 1979. Penetration of
cucumber leaves by Colletotrichum lagenarium is reduced in
plants systemically protected by previous infection with
the pathogen. Physiological Plant Pathology 14 : 329–338.
55. Ross AF. 1961. Systemic acquired resistance induced by
localized virus infection in plants. Virology 14 : 340–358.
56. Ryals J, Weymann K, Lawton K, Friedrich L, Ellis D,
Steiner H-Y, Johnson J, Delaney T, Taco J, Vos P,
Uknes S. 1997. The Arabidopsis NIM1 protein shows
homology to the mammalian transcription factor inhibitor
IkB. The Plant Cell 9 : 425–439.
57. Schmele I, Kauss H. 1990. Enhanced activity of the
plasma membrane localized callose synthase in cucumber
leaves with induced resistance. Physiological and Molecular
Plant Pathology 37 : 221–228.
84 R. Hammerschmidt
58. Shah J, Tsui F, Klessig DF. 1997. Characterization of a
salicylic acid-insensitive mutant sai1 of Arabidopsis thaliana,
identified in a selective screen utilizing the SA-inducible
expression of the tms2 gene. Molecular Plant-Microbe
Interactions 10 : 69–78.
59. Showalter AM, Bell JN, Cramer CL, Bailey JA, Varner
JE, Lamb CJ. 1985. Accumulation of hydroxyproline-
rich glycoprotein messenger-RNAs in response to fungal
elicitor and infection. Proceedings of the National Academy of
Sciences, USA 82 : 6551–6555.
60. Siegrist J, Jeblick W, Kauss H. 1994. Defense responses
in infected and elicited cucumber Cucumis satiŠus L.
hypocotyl segments exhibiting acquired resistance. Plant
Physiology 105 : 1365–1374.
61. Skipp RA, Deverall BJ. 1973. Studies on cross-protection
in the anthracnose disease of bean. Physiological Plant
Pathology 3 : 299–314.
62. Smith JA, Fulbright DW, Hammerschmidt R. 1991.
Rapid induction of systemic resistance in cucumber by
Pseudomonas syringae pv. Syringae. Physiological and Molecular
Plant Pathology 38 : 223–235.
63. Stein BD, Klomparens KL, Hammerschmidt R. 1993.
Histochemistry and ultrastructure of the induced re-
sistance response of cucumber plants to Colletotrichum
lagenarium. Journal of Phytopathology 137 : 177–188.
64. Stermer BA, Hammerschmidt R. 1987. Association of
heat shock induced resistance with increased accumulation
of insoluble extensin and ethylene synthesis. Physiological
and Molecular Plant Pathology 31 : 453–461.
65. Sticher L, Mauch-Mani B, Me! traux JP. 1997. Systemic
acquired resistance. Annual ReŠiew of Phytopathology 35 :
235–270.
66. Stumm D, Gessler C. 1986. Role of papillae in the induced
systemic resistance of cucumber against Colletotrichum
lagenarium. Physiological and Molecular Plant Pathology 29 :
405–410.
67. Summermatter K, Sticher L, Metraux JP. 1996.
Systemic responses in Arabidopsis thaliana infected and
challenged with Pseudomonas syringae pv. syringae. Plant
Physiology 108 : 1379–1385.
68. Szira! ki I, Bala! sz E, Kira! ly Z. 1980. Role of different
stresses in inducing systemic acquired resistance to TMV
and increasing sytokinin level in tobacco. Physiological
Plant Pathology 16 : 277–284.
69. Turner JG, Novacky A. 1974. The quantitative relation
between plant and bacterial cells involved in the hy-
persensitive reaction. Phytopathology 64 : 885–890.
70. Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams
S, Dincher S, Chandler D, Slusarenko A, Ward E,
Ryals J. 1992. Acquired resistance in Arabidopsis. The
Plant Cell 4 : 645–656.
71. VanLoon LC. 1997. Induced resistance in plants and the
role of pathogenesis-related proteins. European Journal of
Plant Pathology 103 : 753–765.
72. VanLoon LC, Bakker PAHM, Pieterse CMJ. 1998.
Systemic resistance induced by rhizosphere bacteria.
Annual ReŠiew of Phytopathology 36 : 453–483.
73. Vijayan P, Shockey J, Levesque CA, Cook RJ, Browse
J. 1998. A role of jasmonate in pathogen defense of
Arabidopsis. Proceedings of the National Academy of Sciences,
USA 95 : 7209–7214.
74. Ward EWB. 1984. Suppression of metalaxyl activity by
glyphosate : evidence that host defence mechanisms con-
tribute to metalaxyl inhibition of Phytophthora megasperma
f. sp. glycinea in soybeans. Physiological Plant Pathology 25 :
381–386.
75. Ward EWB, Lazarovits G, Stossel P, Barrie SD, Unwin
CH. 1980. Glyceollin production associated with control
of Phytophthora rot Phytophthora megasperma sojae of
soybeans by the systemic fungicide, metalaxyl. Phyto-
pathology 70 : 738–740.
76. Weyman K, Hunt M, Uknes S, Neuenschwander U,
Lawton K, Steiner H-Y, Ryals J. 1995. Suppression
and restoration of lesion formation in Arabidopsis lsd
mutants. The Plant Cell 7 : 2013–2022.
77. Yoshikawa M, Tsuda M, Takeuchi Y. 1993. Resistance
to fungal disease in transgenic tobacco plants expressing
the phytoalexin elicitor-releasing factor, β-1,3-glucanase,
from soybean. Naturwissenschaften 80 : 417–420.
78. Yu IC, Parker J, Bent AF. 1998. Gene-for-gene disease
resistance without the hypersensitive response in Arabi-
dopsis dnd1 mutant. Proceedings of the National Academy of
Sciences, USA 95 : 7819–7824.