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Copyright e 1994 by Annual Reviews Inc. All rights reserved

INDUCTION OF SYSTEMIC
ACQUIRED DISEASE
RESISTANCE IN PLANTS BY
CHEMICALS
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Helmut Kessmann, Theo Staub, Christina Hofmann,

Thomas Maetzke, Jiirg Herzog
by University of Guelph on 05/06/13. For personal use only.

Plant Protection Division, Ciba-Geigy Ltd., CH-4002 Basel, Switzerland

Eric Ward, Scott Uknes and John Ryals

Agricultural Biotechnology, Ciba-Geigy Corporation, Research Triangle Park, North
Carolina 27709

KEY WORDS: induced resistance. integrated pest management. disease control.

plant/pathogen interactions. fungicides

INTRODUCTION

Plants defend themselves from pathogen infection through a wide variety of

(32,
mechanisms that can be either local or systemic, constitutive or inducible
70, 108, 109). In most cases, the extent to which these various systems affect
disease progression is poorly understood, and is an area of extensive biochem­
ical and genetic research. One particular inducible systemic response, known
as systemic acquired resistance (SAR), has become a subj ect of increasing
inquiry. SAR is a b road, physiological immunity that results from infection
with a necrogenic pathogen. In addition, certain natural and synthetic chemical
compounds can trigger similar plant responses. This chapter reviews the liter­
ature on chemicals that apparently act by stimulating the natural defense
response in the plant. To put this information in context, we first describe what
is known at present about the occurrence of SAR in various species, and our
current concept of pathogen-induced SAR. Other recent reviews related to
biologically induced SAR and signal transduction complement our discussion
(40, 73, 84, 99, 108)
439

0066-4286/94/0901-0439$05.00
 440 KESSMANN ET AL

SAR INDUCED BY PATHOGEN INFECTION

Historical Development

The natural phenomenon of resistance development in response to pathogen

infection or plant immunity was first recognized in 1901 by Ray & Beauverie,
who both worked with Botrytis cinerea (6, 101). Beauverie had found pre­
viously that the virulence of a sterile strain of Botrytis cinerea could be varied
by environmental parameters like heat, cold, or cultural conditions (5). Both
researchers then used such attenuated fungal strains to induce SAR in Begonia,
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either by planting in soil inoculated with the attenuated strain or by injecting

inoculum into the plants at many points. In both cases, resistance developed
to subsequent infections with highly virulent strains of the same fungus. Thirty­
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one years later Carbonne & Kalaljev confirmed those studies and showed that
acquired resistance also depends on the general fitness of the host (14). In
1933, Chester reviewed research on "the problem of acquired physiological
immunity in plants" and determined that this phenomenon "may play an
important role in the preservation of plants in nature" (22). His review sum­
marized additional field observations of plant protection against diseases, some
of which were probably further examples of bona fide SAR. However, the
detailed analysis of SAR started in the 1960s after reproducible biological
models were developed.

Phenomenology of SAR in Various Plant Species

The first carefully controlled laboratory study of SAR was published in 1961,
when Ross used tobacco mosaic virus (TMV) on a local lesion host (Xanthi-nc
tobacco) and found that subsequent infections were reduced in severity. He
coined the term SAR for the resistance that developed in the distal, untreated
portions of TMV-inoculated plants (107). Resistance that arose in the same
leaf that had been TMV-inoculated he called local acquired resistance (LAR)
(106, 107).
Extending work on SAR to fungi, Cruickshank & Mandryk showed
high-level resistance in field-grown tobacco against blue mold (Peronospora
tabacina) when plants were injected in the stem with a spore suspension of
the same fungus (28). Cohen & Kuc subsequently showed that resistance takes
approximately.three weeks to develop; heat-killed conidia and other pathogens
of tobacco failed to induce SAR when inoculated in this fashion (27). The
SAR induced by spore injection from P. tabacina caused severe dwarfing,
premature senescence, and symptoms resembling nitrogen deficiency (27).
However, if the spores were injected external to the cambium, rather than
internal as in the previous studies, the resulting SAR led to an increase in plant
weight and leaf number (84, 132, 133). In field studies, this SAR was effective
 CHEMICAL INDUCTION OF SAR 441

even against strains of blue mold resistant to metalaxyl, the most common
fungicide used to control this disease (131).
In 1964, Hecht & Bateman showed that inoculation of tobacco leaves with
Thielaviopsis basicola leads to necrosis and subsequent, systemic resistance
to other pathogens, TMV, and tobacco necrosis virus (TNV) (57). Surprisingly,
necrosis induced in the roots did not induce SAR. These authors also confirmed
the previous studies of Ross using TMV as an inducing pathogen. The SAR
response in tobacco gives broad-spectrum disease resistance to fungal, bacte­
rial, and viral pathogens, but is ineffective against aphids and tobacco horn­
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worm, (Manduca sexta) (1, 121). Treatments such as wounding or phyto­

hormone treatment have no significant effect on the development of SAR in
dicots (135; J Ryals et aI, unpublished).
Well-characterized examples of biologically induced SAR have been re­
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corded for cucumber, muskmelon, and watermelon (for review, see 15-17, 47,
63, 64, 84, 122). Localized infections of cucumber with either TNV, Pseu­
domonas lachrymans, or Colletotrichum lagenarium lead to broad-spectrum,
systemic resistance within a few days time. Cucumber plants expressing SAR
are protected against at least 13 diseases including fungi, bacteria, and viruses.
A single inducing infection protects cucumber for 4-6 weeks; a booster inoc­
ulation, 2-3 weeks after the primary infection, leads to season-long, broad­
spectrum resistance (75). SAR cannot be induced after onset of flowering and
fruiting (52). The number of lesions produced on the induced leaf correlates
well with the level of SAR until a saturation point of inoculum or lesion number
is attained (16, 17, 63, 75). (40 sec, 50DC)
A heat-shock treatment of cucumber
results in some resistance to Cladosporium cucumerinum (126).
Green bean plants become resistant to virulent races of Colletotrichum
lindemuthianum after preinfection of hypocotyls with spores of avirulent races
of the same species (35-38, 98, 129). A bean cultivar normally susceptible to
all races of C. lindemthianum could also be made anthracnose-resistant by
preinfection with the cucumber pathogen, Colletotrichum lagenarium. This
result shows that the presence of a strain-specific resistance gene is apparently
not required for SAR to develop. Recently, Kutzner et al described SAR in
bean against TNV using bean rust as inducer (77).
Arabidopsis thaliana was recently developed as an experimental system for
SAR. Uknes et al showed that infection of ecotype Dijon with turnip crinkle
virus (TCV; to which the plant responds with a hypersensitive-like necrosis
(118» could lead to resistance against further infection by TCV or Pseudo­
monas syringae (136, 138). Cameron et al demonstrated that an inducing
infection with an avirulence gene-bearing strain of P. syringae could induce
resistance against subsequent inoculation with a virulent strain of P. syringae
(13).
Additional species in which SAR has been shown include red clover (72),
 442 KESSMANN ET AL

soybean (151), potato (21, 128), tomato (58, 74), pearl millet (76), and alfalfa
(93).
In monocotyledonous plants, there are well described SAR systems estab­
lished in both rice and wheat. In rice, Smith & Metraux (120) reported that
inoculation of the first, fully developed leaf with Pseudomonas syringae pv.
syringae, which causes a rapid hypersensitive necrosis, results in systemic
resistance against Pyricularia oryzae (causal agent of rice blast). The onset of
SAR required a few days, very similar to the results with dicot species. LAR
in barley has frequently been reported over the past 20 years (23, 51, 61, 95-97,
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111, 130) using different microorganisms as inducer and mainly powdery

mildew as the challenge pathogen. Heitefuss and coworkers showed systemic
resistance induction in barley using spores of Erysiphe graminis f. sp. hordei
suspended in an oily solution (heptacosa-fluotributylamin) for application to
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the primary leaf (61). Systemic resistance occurred some days later against the
same fungus. Unfortunately, no further data are available regarding the use of
this method. According to Smedegaard-Peterson and coworkers (23, 51, 130),
both virulent and avirulent races of Erysiphe graminis f.sp. hordei could induce
resistance in barley towards virulent strains of this fungus.

Mechanisms of SAR Maintenance: Dicots

The defense responses at the site of attempted penetration of pathogenic fungi,
bacteria, and viruses, as well as the genetic factors involved in plant/pathogen
interactions, have been reviewed recently in detail (7, 9, 32, 70). Although a
variety of pathogen-inducible responses are known in plants, relatively few
strictly correlate with SAR. Thus, many so-called "defense responses" that are
induced locally by pathogen infection (e.g. expression of certain genes, phy­
toalexin accumulation, cell-wall cross-linking) are clearly not associated with
the resistant state found in the noninoculated portion of the infected plant (84,
78). Therefore, these responses are not markers for the systemic resistant state
induced by pathogens in the particular species for which data are available.
In 1970, the groups of Van Loon (140) and Gianinazzi (48) showed that
viral infection of tobacco induced the accumulation of a distinct set of proteins,
called pathogenesis-related proteins (PR proteins). Van Loon & Antoniw (139)
demonstrated that a subset of the PR proteins (the acidic-extracellular forms)
accumulated during the onset of resistance. In 1991, steady-state mRNA levels
from at least nine families of genes were shown to be coordinately induced in
uninfected leaves of inoculated plants; these gene families are now known as
SAR genes (145). Several SAR gene products have direct antimicrobial activity
or are closely related to classes of antimicrobial proteins. These include 13-1,3-
glucanases, chitinases (86), cysteine-rich proteins related to thaumatin (144,
150), and the PR- l proteins, which lack known biochemical function, but have
in vitro activity against Phytophthora infestans (112). However, all 13-1,3-
 CHEMICAL INDUCTION OF SAR 443

glucanases should not be considered associated with SAR, rather a gene-spe­

cific subset consisting of mostly acidic isoforms is precisely correlated with
SAR (145).
Corroboration for the involvement of SAR genes and their homologues in
resistance comes from transgenic plant experiments. Seedlings of tobacco
and Brassica, which express a chitinase from bean, are significantly protected
against damping-off caused by Rhizoctonia sp. (11). Furthermore, constitutive
high-level expression of tobacco PR-la in transgenic tobacco plants results
in increased tolerance to two oomycete pathogens, Peronospora tabacina
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(causal agent of blue mold disease) and Phytophthora parasitica (black shank
disease) (2). These two pathogens are effectively controlled by SAR, and
PR-I is the most abundant protein associated with the resistant state. Thus,
the findings that several SAR genes encode direct antimicrobial activities
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and that certain proteins expressed in transgenic plants impart partial patho­
gen tolerance strengthen the case that these genes play a direct role in
maintaining SAR.
At the molecular level, the set of SAR genes that are induced may differ
between species. For example, in cucumber a class III chitinase is the most
highly induced SAR gene, while in tobacco and Arabidopsis, PR-l is the
predominant SAR gene expressed (89-91, 137, 138, 145). Although cucumber
possesses a PR-l homologue in its genome (J Ryals et aI, unpublished data),
the gene is not expressed at detectable levels in response to pathogen infection.
Such differences between species may reflect different evolutionary or breed­
ing constraints that have selected for the most effective SAR response to the
particular pathogen spectrum to which the species is subject. The correspon­
dence between the different sets of SAR genes that are expressed in each
species and the diseases against which the response is effective has not yet
been firmly established among different species. Although, PR-I appears to
have activity against Oomycete pathogens (2). To date, bona fide SAR genes
have been characterized in only a few plant species, including tobacco, cu­
cumber, and Arabidopsis.
Other morphological and biochemical changes that result from pathogen
infection have been investigated for their relevance to SAR. Microscopic
studies revealed that germination and appressoria formation of Colletotrichum
lagenarium are not affected by biological induction of SAR in cucumber (84,
153). However, penetration was drastically reduced in systemic tissue, most
likely due to papilla-like material beneath the appressoria. Using labeled lignin
precursors, Dean & Kuc (30) showed that the lignification response is signif­
icantly faster in plants showing systemic resistance, which corresponds with
an increase in peroxidase activity (119). Recently it was shown that these
papilla contain not only lignin but also silicon (124). These studies may
indicate that plants expressing SAR are somehow sensitized to respond faster
 444 KESSMANN ET AL

to microbial attack. However, the molecular basis of such a mechanism is still

unknown.
Following stem injection with Peronospora tabacina, Salt et al (110) ob­
served a significant increase in glucose and fructose in systemic tissue as well
as an accumulation of fungi-toxic j3-ionone derivatives (111, 152). Injection
of �-ionone into tobacco stems protected tobacco against blue mold and en­
hanced growth of the plants (111). A local infection with TMV on Xanthi nc
caused a systemic induction of lipoxygenase (121), which may indicate an
important role of fatty acid derivatives in SAR, as appears to be the case in
Annu. Rev. Phytopathol. 1994.32:439-459. Downloaded from www.annualreviews.org

rice (see below).

In green bean, phytoalexin induction was increased in preinoculated plants
compared to controls, but no accumulation was observed in systemically pro­
tected tissue (38). However, no similar sensitizing effect on phytoalexin accu­
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mulation was observed in tobacco after SAR induction (127). Chai & Doke
(18) showed that superoxide dismutase and peroxidase are systemically in­
duced in potato after local infection with Phytophthora infestans. The systemic
activation of an Oz-generating system is thought to play an important role in
SAR in this species. Heat-shocked cucumber seedlings exhibit an increase in
insoluble, hydroxyproline-rich glycoprotein (126), which corresponds to pre­
vious studies showing a correlation between accumulation of this type of cell
wall protein and resistance of cucurbits towards pathogens (41, 55).

Mechanisms of SAR Maintenance: Monocots

In the rice/Po syringae SAR model system, no induction of new proteins could
be detected, as assayed by polyacrylamide gel electrophoresis or by monitoring
activities of various defense-related enzymes (120). However, P. syringae pv.
syringae induces lipoxygenase activity in local and systemic tissue (60).
Wen Xin Li et al (148) showed that, after infection of rice with Pyricularia
oryzae, hydroxylated fatty acid accumulated prior to phytoalexins of the
monilactone class. Nordihydroguaiaretic acid, an inhibitor of lipoxygenase,
not only inhibited the accumulation of the fatty acids but also of the
phytoalexins. The hydroxylated fatty acids were therefore postulated to act
not only as antimicrobial compounds but also as endogenous elicitors of
monilactone induction. In addition, a lipoxygenase pathway is induced that
is more pronounced in a incompatible reaction than in a compatible reaction
of P. oryzae with rice (94).
Based on these studies, there is now considerable evidence that antimicrobial
fatty acid derivatives play a role in constitutive as well as inducible resistance
of rice against blast disease (67, 68, 92, 94). However, other mechanisms, such
as an increase in lignification at sites of pathogen ingress, may also be involved
in SAR in rice (54, 120). This would be very similar to resistance mechanisms
obtained by classical breeding (66, 105). Furthermore, it would be interesting
 CHEMICAL INDUCTION OF SAR 445

to evaluate another biological model of SAR in rice in more detail, where

"buff pigment mutants" of Pyricuiaria oryzae were induced for resistance
(116).
In barley, strong correlations exist between host cell fluorescence (hyper­
sensitive response), papilla formation, and LAR. Several induced mRNAs have
been cloned and characterized (50). In addition, in wheat infected with both
barley and wheat strains of E. graminis, several cDNAs have been cloned that
appear to be specifically induced by pathogen infection (12, 103, 104).
The discovery of resistance-inducing chemicals now makes it possible to
Annu. Rev. Phytopathol. 1994.32:439-459. Downloaded from www.annualreviews.org

characterize SAR in monocot species in more detail (see below). However,

because the criteria for what constitutes a true SAR-inducing chemical rely on
analogy to events triggered by biological SAR, good biological models of SAR
in monocot crops are important.
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Systemic Signaling in SAR

In 1979, White showed that the exogenous application of salicylic acid (SA)
and certain other benzoic acid derivatives induces both resistance to TMV and
the accumulation of PR-proteins (149). In more recent experiments, SA was
found in the phloem of cucumbers infected with either tobacco necrosis virus
or Colletotrichum lagenarium before the onset of acquired resistance (87).
TMV treatment of tobacco can also induce the accumulation of endogenously
synthesized SA (82, 85). The levels of endogenous SA have been closely
correlated to the induction of the PR-proteins (73, 154). Moreover, exogenous
application of SA induces the same sets of SAR genes that are expressed
following biological SAR induction (137, 138, 145). These observations have
led to the idea that SA could be an endogenous signal responsible for triggering
resistance.
The involvement of SA in signaling SAR has been clearly demonstrated in
recent experiments with transgenic tobacco that express the salicylate hydrox­
ylase gene (nahG) from Pseudomonas putida (46). This enzyme catalyzes the
conversion of SA to catechol, which has no SAR-inducing activity. The NahG­
expressing plants do not accumulate SA in response to pathogen infection and
they show no SAR gene or resistance expression in the distal portions of the
plant. These experiments indicate the direct involvement of SA and SAR-gene
expression in SAR, but do not bear on the question of whether SA is the
vascular-mobile signal that moves throughout the plant after initial infection.
Previous studies had shown that disruption of phloem transport by girdling
inhibits the systemic induction of resistance in response to a local, pathogen­
induced necrosis (29). Moreover, a healthy scion grafted onto an infected
rootstock can become induced for SAR (65). These experiments were inter­
preted to mean that a mobile, phloem-transported signal traveled from the site
of initial infection to distal plant parts. Two more recent studies have addressed
 446 KESSMANN ET AL

more directly the question of whether SA is the long-distance SAR signal (100,
1 43).
First, using cucumber infected with P. syringae, Rasmussen et al (100)
showed that. very high levels of SA could be detected in phloem exudate.
However, they also showed that the infected leaf could be removed several
hours after inoculation, well before significant SA accumulation was detect­
able, without inhibiting the systemic expression of an acidic peroxidase gene
that serves as a marker for SAR in this species. This result suggests that a
signal other than SA is responsible for systemic expression of SAR.
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Second, Vemooij et al (143) performed grafting experiments using wild-type

and salicylate-hydroxylase-expressing plants to further test whether SA is a
systemic signal. They found that a NahG transgenic rootstock induces SAR in
scion tissue equally as well as a wild-type rootstock. In addition, scions that
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express salicylate hydroxylase are unable to become resistant, regardless of

the rootstock to which they are grafted. The conclusion therefore is that SA is
not the primary long-distance signal required for SAR, and production of this
systemic signal is not dependent on SA accumulation. However, SA must be
present in order for the signal to be transduced into gene expression and
resistance.
The exact nature of the systemic signal has not yet been determined. How­
ever, in a recent experiment by Hammerschmidt, Davies and coworkers, elec­
trical signals were not detected when plants were induced to develop SAR (E
Davies, personal communication).
Recently, Chen et al isolated a SA-binding protein with catalase activity
(19, 20). The activity of this enzyme was inhibited by mM concentrations of
SA. The authors suggest that SA perception by the plant cell may involve the
generation of active oxygen species. Further experiments should determine the
role of reactive oxygen in SA signaling and SAR.

SAR INDUCED BY CHEMICAL APPLICATION

The Case for SAR-Inducing Chemicals

Several disease-control options are available to growers; these include resistant
cultivars, biological control, crop rotation, tillage, and chemical pesticides.
Among the chemical pesticides, or fungicides, many compounds are available
but nearly all are based on a direct antibiotic principle. A second potential
principle for chemically mediated disease control could be based on com­
pounds that would induce the SAR response. The concept of a new principle
for disease control provides an exciting prospect. The availability of a long­
lasting, broad-spectrum, stable solution to disease control would undoubtedly
have an enormous positive impact on food production. In this section we
 CHEMICAL INDUCTION OF SAR 447

review the case for the existence of such chemical SAR-inducers. A chemical
will be considered an "activator" of the SAR response if the chemical induces
resistance to the same spectrum of pathogens and induces expression of the
same biochemical markers as in the biological model. Furthermore, the chem­
ical should have no direct antimicrobial activity. In the case of antimicrobial
activity, an SAR-inducing activity could be established by demonstrating re­
sistance to pathogen isolates that are genetically resistant to the antibiotic
effects of the chemical.

Salicylic Acid
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SA plays a central role in SAR-signal transduction after pathogen infection

(discussed above), and has long been known as an exogenous inducer of PR
protein accumulation and resistance (149). Thus, one can reasonably ask
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whether SA is a useful candidate for an exogenous applied SAR activator.

Clearly, the application of SA will induce local resistance to the same spectrum
of pathogens as seen with TMV-induced SAR in tobacco. Also, the same set
of genes are induced in the treated tissue to levels comparable to those observed
with TMV-induced SAR. Furthermore, neither SA nor its metabolites have
significant antibiotic activity. Thus, SA fulfills all of the criteria of an activator.
However, there are some problems with SA. First, although SA is clearly
required for SAR, it is not the translocated signal molecule (discussed in detail
above). More importantly, reports of SA-mediated resistance are restricted to
effects in the treated tissue, indicating that SA does not translocate efficiently
when applied exogenously. These results have been confirmed and given a
biochemical basis by Raskin and coworkers, who showed that exogenous SA
becomes rapidly conjugated, mostly into �-glucosides (39). These conjugates
lack the phloem mobility of free salicylate. This inability to deliver significant
amounts of free SA to systemic tissue after exogenous application seriously
detracts from the usefulness of SA as an exogenous activator. Finally, severe
crop-tolerance problems are associated with SA use. Only a narrow safety
margin separates the rates at which the compound is efficacious and the rate
at which it is strongly phytotoxic. Because of these limitations SA per se has
not been considered a practical solution to disease control.

2,6-dichloroisonicotinic Acid
In our laboratories, 2,6-dichloro-isonicotinic acid (CGA 41396) and its meth­
ylester (CGA 41397; both referred to as INA) were discovered as agents able
to induce systemic resistance in plants (71, 88,121). These compounds provide
good protection against fungal and bacterial pathogens on cucumber, rice, and
other crops, in the greenhouse as well as under field conditions (Table 1). As
shown in detail for cucumber, the spectrum of activity is identical to the
resistance observed after local preinfection with inducing microorganisms
 448 KESSMANN ET AL

Table 1 Activity of eGA 41396 in field trials

% infected leaf area

Host/pathogen INA Rate check eGA 41396 Standard

TobaccolPeronospora 20 g/hl 29 12 17a

PearlErwinia 25 g/hl 45 18 4b
Pepper/Xanthomonas 25 g/hl 66 10 65c
d
RicciPyricularia I kg/ha 12 3.5 0.5
Rice/Xanthomonas 2 kg/ha 8.2 0.2 O.le
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Application was foliar, except in rice where the compound was applied into water.
Standards used:Ridomil + mancozeb. 24 + 196 glhl ; b streptomycin, 25 g/hl; copper
a C

+mancozeb, 200 + 100 g/hl; dOryzemate (probenazole) 2.4 kg/ha; 'TF-130, 2 kg/ha
(modified from 88 and 121).
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(121). The compound has no significant in vitro activity and is not converted
in vivo into antimicrobial metabolites (88).
Detailed molecular studies then showed that in tobacco, infection with TMV
and treatment with INA induce the same set of nine gene families (145). Similar
correlations between the genes systemically induced by pathogen infection and
by INA application have been observed in other species, including cucumber
(88) and Arabidopsis (137). At the level of activity measurement, INA induces
/3-l,3-glucanases, chitinase, and 6-phosphogluconate-dehydrogenase (6-PGD)
in tobacco, whereas phenylalanine ammonia-lyase, acidic proteases, peroxi­
dases and polyphenoloxidases arc not affected by this compound (121). The
four enzymes not affected by INA are typical for a local defense response,
including hypersensitive response (local necrosis), Thus, INA apparently mim­
ics the biological induction of systemic disease resistance without affecting
any of the tested responses linked with local necrosis.
Histological studies showed that Arabidopsis plants treated with INA re­
spond to infection with Peronospora parasitica (137) by a single-cell necrosis
at the site of attempted penetration. The few hyphae that still penetrate become
surrounded by a cluster of necrotic cells and growth ceases, similar to the
observed HR that results from incompatible genotypes of host and pathogen.
Using lower concentrations of INA, more hyphae successfully invade the tissue
but infection still stops, although at later stages. A similar inhibition of infec­
tion at multiple sites during the infection process in biologically or chemically
induced plants was also observed in other plants (74, 84; 1. Ryals et aI,
unpublished data),
In addition to the induction of SAR genes and enzymes cited above, INA
and analogs are able to sensitize plant tissue to respond with additional defense
reactions faster than untreated plants. Kauss et al (69) showed that parsley cell
cultures pretreated with INA produce various phenylpropanoid-derived me-
 CHEMICAL INDUCTION OF SAR 449

tabolites much more rapidly following treatment with fungal elicitor than do
controls. In rice, INA induces a pronounced increase in lipoxygenase activity
within two days of application, whereas an inactive analog had no inducing
effect (60). Seguchi et al reported that the isonicotinic acid derivative N­
cyanomethyl-2-chloroisonicotinamide possesses a high level of activity against
rice blast (114). They showed that lipoxygenase(s) and general lipid metabo­
lism as well as peroxidase(s) are accelerated or increased in chemically treated
and blast-inoculated rice leaves compared to inoculated controls. These data
may indicate that mechanisms in addition to induction of the already charac­
Annu. Rev. Phytopathol. 1994.32:439-459. Downloaded from www.annualreviews.org

terized SAR genes are involved in action of INA and other inducers of SAR.
However, the molecular basis of such a "priming" or "sensitizing" mechanism
is still not known.
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Other Potential Resistance-Activating Chemicals

A number of reports have claimed resistance-inducing activity for certain
chemicals or extracts, but have failed to demonstrate that the compound in
question fulfills the criteria previously established for SAR activators.
Fosethyl-AI, metalaxyl (146) and, more recently, triazoles (56) are among
these compounds. Fosethyl-AI shows very weak antifungal activity in tradi­
tional in vitro assays (8, 42). Plants pretreated with this compound accumulate
phytoalexins faster (53, 102), and the effectiveness of metabolic inhibitors like
glyphosate (45) decreases. These experiments led to the speculation that
fosethyl-AI was a resistance-inducing compound. However, Fenn & Coffey
(43) showed that, depending on culture conditions, fosethyl-AI would degrade
to phosphoric acid, which is strongly antifungal in vitro. Both compounds
show no in vitro activity in media containing high concentrations of phosphate.
Synthetic media with no phosphate indicate strong in vitro activity since
phosphoric acid likely interacts with intracellular phosphate metabolism. The
most conclusive evidence against a resistance-inducing activity of fosethyl-AI
is the fact that fungal strains selected for insensitivity to fosethyl-AI in vitro
are no longer controlled by the compound in planta (33, 44).
2,2-dichloro-3,3-dimethylcyc1opropane carboxylic acid (DCP) was de­
scribed by Langcake & Wickins in 1975 (79, 80) as a compound for specific
control of rice blast. It is only weakly antifungal in vitro, and induces some
peroxidase activity in treated plants. Rice treated with DCP exhibited faster
tissue browning in response to picolinic acid (the putative pathotoxin of
Pyricularia oryzae) than did untreated controls (79). Upon infection, DCP­
treated plants accumulated monilactone phytoalexins faster and to higher levels
than untreated controls. Thus, the main evidence for resistance-inducing ac­
tivity of DCP comes from postinfection data, which resemble those seen for
contact fungicides. Furthermore, DCP and analogs provide significant control
of C. lagenarium in cucumber without inducing chitinase, a biochemical
 450 KESSMANN ET AL

marker of SAR for this plant (H Kessmann, unpublished data). DCP had effects
on melanization in vitro and weak antifungal activity is observed for all agents
that inhibit melanin biosynthesis since melanin is important for the formation
of plant-infection structures (appressoria) and not for growth on media (H
Dahmen, personal communication). Therefore, the strong specificity for mel­
anin-forming fungi together with the in vitro effects on melanization, the lack
of positive correlation with a biological model of SAR, and the lack of chitinase
induction in cucumber indicate that DCP may act directly, perhaps by inhib­
iting melanin biosynthesis. However, more studies are required to elucidate
Annu. Rev. Phytopathol. 1994.32:439-459. Downloaded from www.annualreviews.org

the mode of action of this class of compounds.

Probenazole is a systemic compound used successfully to protect rice against
Pyricularia oryzae and weakly against Xanthomonas oryzae. The compound
shows only very weak in vitro activity. Probenazole induces various defense­
by University of Guelph on 05/06/13. For personal use only.

related enzymes to a limited extent, but causes significant accumulation of

"anticonidial factors" (67). These factors were identified as fungi-toxic, unsat­
urated fatty acids, including linolenic acid (117). After infection with the blast
fungus a number of enzymes possibly involved in plant defense showed much
higher activity in probenazle-treated plants than in nontreated, infected controls
(62). Probenazole also potentiated the "respiratory burst" and accumulation of
superoxide anion radical normally observed after infection with blast fungus
(115). This is an interesting observation because evidence is emerging from
other systems that the respiratory burst and reactive oxygen species, which
play a central role in defense of macrophages in mammalian systems, may
also be important in plant-pathogen interactions (20, 78). However, proben­
azole does not significantly induce lipoxygenase, a molecular marker for SAR
in rice (C Hofmann, unpublished data). Therefore, the correlation with a
biological marker for SAR is still lacking for probenazole, despite evidence
that this chemical protects rice against P. oryzae.
An astonishing case of induced blast resistance was reported by Arimoto et
al (4). They claim that rice plants can be protected for several generations
when the seeds are soaked in a SOO-ppm solution of DL-alanine dodecylester
HCl. However, no further evidence of the validity of this concept has been
reported.
The ethylene-releasing agent ethephon did not induce resistance in tobacco
against TMV although it significantly induced the basic isoforms of PR-pro­
teins (10), indicating that these isoforms do not play a decisive role in SAR.
Recently, Lawton et al have shown that ethephon induces SAR-gene expres­
sion via a SA-dependent pathway (81). Most importantly, ethylene did not
appear to be required for the development of SAR in Arabidopsis because
ethylene-insensitive mutants developed SAR in response to SA and INA treat­
ment.
Recently, Cohen and coworkers reported that jasmonic acid (JA) and its
 CHEMICAL INDUCTION OF SAR 451

methylester induces resistance in tomato towards Phytophthora infestans (26).

However, no data on the accumulation of any molecular markers for SAR
were reported. Additionally, Mosinger et al reported on significant in vitro
activity of JA and concluded that the protective effect observed for JA on
barley against powdery mildew is due to direct antifungal activity (113). In
addition, JA and JA methylester do not induce the molecular markers for SAR
in tobacco or cucumber (H Kessmann, unpublished data). Furthermore, the
proposed systemic inducer of wound-induced/JA-induced genes, systemin,
does not induce the SAR genes or resistance in tomato against downy mildew
Annu. Rev. Phytopathol. 1994.32:439-459. Downloaded from www.annualreviews.org

(P Ahl-Goy, personal communication).

DL-3-arnino-n-butanoic acid has also been implicated as an inducer of
resistance in tomato against downy mildew (24). Since the in vitro antifungal
activity of this compound is low, inducing activity was implicated. However,
by University of Guelph on 05/06/13. For personal use only.

as described for fosethyl-AI, lack of in vitro activity may depend entirely upon
media conditions. Furthermore, SAR-gene expression was not analyzed in
tomato. DL-3-arnino-n-butanoic acid appears to induce some of the PR-pro­
teins associated with SAR in tobacco (83). However, pathogen resistance and
the full spectrum of SAR-gene expression was not analyzed in tobacco. Further
work is required before DL-3-amino-n-butanoic acid can be characterized as
an activator.
The list of agents (both defined chemicals and extracts) with proposed
inducing activity includes various inorganic salts, silicon, oxalate, phosphate,
2-thiouracil, polyacrylic acid, nucleic acids, unsaturated fatty acids, N-Trime­
thyl-L-lysine (3, 34, 49, 25, 3, 131, 134, 21, 128, 31, 123). None of these
compounds fulfills the three criteria listed above for SAR-inducers. In many
cases, these agents may result in a local necrosis, which triggers an SA-de­
pendent pathway like that induced by pathogen infection. Rigorous analysis
of the other chemical inducers may uncover many similar stories. Moreover,
in most cases, the protection observed has not been proven to result from SAR,
and direct antimicrobial effects cannot be excluded. We strongly suggest that
the term SAR-inducer be used only in cases where the three criteria described
above are clearly demonstrated.

SAR INDUCED BY MICROBES

A special case of resistance inducers may be extracts from plants and microbes.
Herger et al (59) have used an extract of Rheynoutria sachalinensis and
observed good control of powdery mildews and, to lesser extent, other patho­
gens in a range of crops. However, the active principle(s) are not known.
Extracts from Bacillus subtilis have been reported to induce resistance in
barley, especially against powdery mildew (125). In all of these cases, the
agent has not yet been shown to mimic the biological induction of SAR and
 452 KESSMANN ET AL

mechanisms other than SAR may well be involved in its activity (direct or
indirect antimicrobial activity). Detailed biochemical, molecular, or phytopath­
ological data are needed in each case to confirm resistance-inducing activity.
Another interesting class of agents are plant growth-promoting rhizobacteria
(PGPR), apparently able to protect plants against foliar diseases when used as
a seed treatment or by seed soaking. Wei et al (147) reported on strains of
Pseudomonas able to protect cucumber against a range of diseases. A strain
of Pseudomonas also protects carnation against Fusarium wilt. Protection was
observed in a split-root system in wh ich the bacteria were applied only to one
Annu. Rev. Phytopathol. 1994.32:439-459. Downloaded from www.annualreviews.org

part; protection observed in the nonbacterized portion was attributed to an SAR

response (141). Lipopolysaccharides may be involved in this proposed induc­
tion process (142). Although promising, the three criteria for inducers of SAR
have not been fulfilled to date.
by University of Guelph on 05/06/13. For personal use only.

CONCLUSION AND PROSPECTS

Historically, more emphasis has been placed on the discovery of new resistance
genes by breeding and molecular techniques than on using the resistance
potential already present in existing cultivars. Recently, evidence has accumu­
lated showing the effectiveness of SAR in laboratory and field situations.
However, several important issues regarding the use of S AR-inducers are
apparent, including crop tolerance and curative application. Even considering
these possible limitations, SAR-inducing chemicals will provide novel benefits
over existing strategies of disease control: the mechanism of SAR is apparently
multifaceted, likely resulting in stable, broad-spectrum disease control; SAR
can be used preventatively to bolster general plant health; SAR can result in
long-lasting protection. In general, a S AR-inducing agent, whether chemical
or biological, will provide the farmer with an additional option for disease
control in crops.

Any Annual Review chapter, as well as any article cited in an Annual Review chapter,
may be purchased from the Annual Reviews Preprints and Reprints service.
1-800-347-8007; 415-259-5017; email: arpr@c1ass.org

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