During the past year genetic and pharmacological experiments have revealed a molecular basis for the cross-talk between signaling pathways mediating pathogen and herbivore
resistance. These findings provide considerable insight into the apparently contradictory results reported for trade-offs between pathogen and herbivore resistance.
Addresses
Department of Entomology, University of Arkansas, Fayetteville, Arkansas 72701, USA;
*e-mail: gfelton@comp.uark.edu †e-mail: kkorth@comp.uark.edu
Current Opinion in Plant Biology2000, 3:309–314 1369-5266/00/$ — see front matter
© 2000 Elsevier Science Ltd. All rights reserved.
Abbreviations
Avr9 avirulence 9
BTH benzothiadiazole-7-carbiothioic acid S-methyl ester
Cf-9 resistance to Cladosporium fulvum JA jasmonic acid
MAP mitogen-activated protein
npr nonexpressor of PR
PAL phenylalanine ammonia lyase
PDF1.2 plant defensin1.2 PR pathogenesis-related
SA salicylic acid
SAR systemic acquired resistance
ssi1 suppressor of SA insensitivity 1 TMV tobacco mosaic virus
Introduction
Trade-offs are based on the fitness costs incurred when a favorable change in one life history trait is coupled to a harmful change in another trait. The reciprocal effects of induced resistance to pathogens and to herbivores may rep-resent such a trade-off. It is generally assumed that systemic acquired resistance (SAR) and induced resistance are not constitutively expressed because the activation of these defense pathways involves the massive, coordinated expression of numerous genes that imposes energetic and fitness costs. Fitness costs of induced resistance or jasmonic acid (JA)-induced resistance have been observed [1,2••], although fitness costs associated with SAR are largely unknown. The term SAR is normally associated with induced responses to pathogens, whereas ‘induced resis-tance’ is associated with wound responses to herbivory.
A more complete understanding of trade-offs between resistance to pathogens and herbivores at the cellular level will require knowledge of the signal transduction networks that are triggered in response to insects and microbes. Jasmonic acid, salicylic acid (SA) and ethylene are central players in mediating responses to pathogens and wounds (Figure 1). Jasmonate is usually associated with wounding pathways, whereas salicylate is most often thought to func-tion in pathogen responses. Several recent reviews provide
excellent coverage of the literature on the cross-talk that occurs between these pathways [3–5]. There is ample evi-dence to show that wound signaling pathways sometimes function independently of jasmonate, and likewise, that there are salicylate-independent responses to pathogens [3]. Moreover, the induction of the tomato transcription factors Pti4 and Pti5 by bacteria can occur independently of salicylate, jasmonate, or ethylene [6]. This review attempts to cover what is known of the trade-offs between costs associated with induced resistance responses to pathogens and to herbivores. The complexity of signaling pathways is illustrated by reviewing findings obtained in experiments using biological, pharmacological and biologi-cal approaches. Recent characterization of insect derived elicitors, which are being used to shed light on the speci-ficity of induced responses to herbivores, is also discussed.
Biological evidence for trade-offs
Evidence for trade-offs between resistance to pathogens and herbivores were reported recently. Inoculation of tobacco with tobacco mosaic virus (TMV), which resulted in increased endogenous salicylic acid, caused an increased susceptibility to leaf consumption by the larvae of Manduca sexta [7••]. TMV-infected plants had attenuat-ed wound-inducattenuat-ed JA and nicotine responses [7••]. Conversely, cross-resistance between herbivores and pathogens was reported in tomato [8••]. Inoculation of leaves with Pseudomonas syringaepv. tomato induced sys-temic accumulation of transcripts for protease inhibitors and pathogenesis-related proteins, and induced systemic resistance to both P. syringae and larval Helicoverpa zea [8••]. Similarly, feeding by H. zea induces systemic resistance to both H. zeaand P. syringae. Infection of leaves with the fungal pathogen Phytophthora infestans, however, had no effect on resistance to H. zea. Infection of field-grown cucumber with the scab fungus Cladosporium cucumerinum had no effect on the herbivore densities of cucumber beetles or melon aphids feeding on it [9]. Thus, biological evidence for trade-offs between insect and pathogen resistance is equivocal. The relationship between insect and pathogen resistance appears to be idiosyncratic and to depend upon the particular species of plant, insect herbivore and pathogen involved.
Pharmacological evidence for trade-offs
Pharmacological approaches utilizing SA (or mimics of SA) or JA/methyl-JA reveal that antagonism between defense pathways is a probable mechanism responsible for defense trade-offs. Treating tomato with the SA-mimic benzothiadi-azole-7-carbiothioic acid S-methyl ester (BTH) suppressed wound- or JA-inducible proteinase inhibitor (PIN II) tran-scription [8••,10•]. BTH also attenuates the JA-inducible defense-related protein polyphenol oxidase and compromis-es rcompromis-esistance to the beet armyworm Spodoptera exigua[11•].
Trade-offs between pathogen and herbivore resistance
Conversely, JA reduces pathogenesis-related (PR) protein gene induction by BTH and partially suppresses the protec-tive effect of BTH against P. syringaepv. tomato [11•]. SA also suppresses wound-induced trypsin inhibitor synthesis in Brassica napus and in Arabidopsis (D Cipollini, C Clemmons, J Bergelson, personal communication).
Other studies in tomato show no evidence of trade-offs. Applications of BTH to field-grown tomato plants at three-week intervals reduced larval populations of the leafminers Liriomyzaspp. during portions of the growing season, but did not significantly impact whiteflies (Bemisia argentifolii) [12]. Conversely, treatments with SA had no significant impact on these herbivores. These studies indicate that induced resis-tance to these diverse herbivores (H.zea, S.exigua, whiteflies and leafminers) may be mediated by different signaling pathways and defense responses.
Experiments using Arabidopsisreveal both interspecific dif-ferences in resistance signaling and difdif-ferences between systemic signaling pathways and signaling pathways within local tissues. The addition of oligosaccharides, that is com-ponents of the plant cell wall, represses JA-inducible gene expression but not the expression of other wound-respon-sive genes, in local tissues [13]. Oligosaccharide treatment does not, however, inhibit JA-responsive gene expression in systemic tissues. Oligosaccharides therefore serve as pri-mary signals in a JA-independent pathway, and their role, along with JA, in Arabidopsisis somewhat different than in Solanaceous species where the two compounds act sequen-tially. The role of ethylene also differs between Arabidopsis
and the Solanaceous species. In the Solanaceous species, ethylene potentiates the effects of JA and oligosaccharides, whereas in Arabidopsis, it is required for the repression of the JA-inducible genes by oligosaccharides. Thus, there are clear differences in wound-responsive signaling pathways within local and systemic tissues. Furthermore, even though the same signaling compounds might be involved, there can be fundamental differences in the roles that they play in different plant species.
Although pharmacological experiments are valuable for demonstrating potential cross-talk among defense path-ways, their usefulness is limited because in situsignaling may be markedly different from that observed in these experimental systems. For example, the timing of signal-ing events (e.g. JA and SA biosynthesis) may be sufficiently different to avoid cross-talk in situ [14•]. Indeed certain pathogens may induce both SA and JA-dependent pathways [8••,14•,15]. Likewise, aphid, whitefly and leafminer infestations may elicit SA-depen-dent PR gene and protein expression without inducing JA-pathways ([5,16]; D Puthoff, L Walling, personal com-munication). These differences in elicitation among herbivores may be explained by differences in their sali-vary components (see below) or differences in feeding damage. Many caterpillars are leaf chewers, whereas whiteflies and aphids insert their stylets to feed on phloem, and leafminers feed within the leaf mesophyll. Although the SA- and JA-pathways have been associated with disease and herbivore resistance, respectively, a strict dichotomy between these pathways may not exist.
_
_
PI, PPO, secondary compounds, unique
volatiles, etc. Herbivores (e.g. caterpillars)
and elicitors (e.g. volicitin)
JA, ethylene and ? production
PI, PPO, secondary
compounds (e.g. alkaloids), etc.
Wounding responses
JA and ethylene production
SA-inducible PR-proteins Pathogen infection or herbivores (e.g. aphids, whiteflies and leafminers)
(SA-dependent)
SA production JA and ethylene production
SA-non-inducible PR-proteins, thionins, etc. Pathogen infection (non-SA-dependent)
Current Opinion in Plant Biology
SAR IR Indirect defense
IR
Simplified model showing signaling pathways associated with induced resistance to pathogens and herbivores. ‘—’ denotes a negative effect on the pathway and ‘?’ denotes an unknown endogenous signal for elicitation. Adapted from references [3,5,10•,36]. IR, induced resistance;
Spatial differences in signals may influence possible antag-onism between pathways. Potato plants infected with potato virus Y show altered distribution and concentration of endogenous JA [15]. In healthy plants, JA synthesis is located primarily in the shoots, but in infected plants JA synthesis shifts primarily to the roots. Moreover, most studies employ a single elicitor dose and have not tested for concentration-dependent effects that would result from natural infestations/infections.
Genetic evidence for trade-offs
The use of mutants and transgenics is a powerful approach for investigating the molecular basis of defense trade-offs. Transgenic tobacco expressing varying levels of phenyl-alanine ammonia lyase (PAL) were used to show that levels of induced resistance to pathogens and insects in the same plant lines can be inversely correlated. Tobacco plants overexpressing PAL accumulate higher than normal con-centrations of SA, whereas plants with low PAL levels (owing to homology-dependent gene silencing) have cor-respondingly low SA concentrations [17,18]. These plants show an inverse correlation in concentrations of SA and JA, and also show inversely proportional levels of induced resistance to the pathogen TMV and the insect (Heliothis virescens) [19]. Tobacco plants with high-SA/low-JA con-centrations show greater SAR and lower levels of induced insect resistance. Conversely, low-SA/high-JA plants have decreased SAR and enhanced insect resistance, suggesting cross-talk between, and inhibitory action by, SA- and JA-mediated pathways [19].
Multiple functions for other components of signaling path-ways have been demonstrated by work on resistance-gene interactions with avirulence genes. The interaction of the tomato Cf-9 (resistance to Cladosporium fulvum) gene with its corresponding pathogen avirulence gene, Avr9 (aviru-lence 9), results in the rapid induction of tobacco protein kinases in transgenic plants expressing Cf-9 [20]. Although this kinase acitivity depends on the specificity of the inter-action between Cf-9 and Avr9, the kinases are not involved in the synthesis of active oxygen species produced during a Cf-9–Avr9 interaction [21]. This evidence suggests that the specific interaction between Cf-9 and Avr9 can trigger sev-eral distinct defense-signaling pathways. The induced MAP (mitogen-activated protein) kinases are very similar to those induced in tobacco by wounding and SA [22]. Therefore, signaling pathways with the specificity of a gene-for-gene interaction could be linked via MAP kinases to pathways with less biotic specificity, such as wounding.
Plant mutants, especially in Arabidopsis, have provided information about the signaling components involved in pathogen responses. The npr (i.e. nonexpressor of PR) mutants of Arabidopsis do not express PR genes or SAR, and cannot be rescued by added SA or BTH [23], indicating that the functional NPR1 product is necessary for SA-mediated SAR. The dominant Arabidopsis mutation ssi1(i.e. suppressor of SA insensitivity 1) causes SA-dependent constitutive
expression of some PR genes, and restores resistance to an avirulent strain of bacteria in the nprmutant [24••]. This indicates that ssi1 functions in a parallel SA-signaling path-way that does not depend on NPR1. Although the defensin gene PDF1.2 (plant defensin1.2) is constitutively expressed in ssi1 lines, its levels of expression are low in ssi1/npr1–5 plants that have the salicylate-hydroxylase-encoding nahG gene. Expression of PDF1.2had been shown to be inde-pendent of SA [25], but application of BTH can restore expression of PDF1.2in ssi1/npr1-5/nahGplants. The find-ings suggest that ssi1 could serve as a switch at an intersection between the SA- and JA/ethylene-mediated signaling pathways, and could, therefore, be valuable for fur-ther studies of tradeoffs. The presence of the NPR1 protein greatly enhances the binding of a TGA transcription factor to promoter elements of the PR-1 gene, whereas npr1 mutant proteins, which are associated with disease suscepti-bility, did not enhance TGA binding [26]. Interactions of proteins that regulate pathways, such as NPR1, with classes of transcription factors could represent yet another point of cross-talk between JA- or SA-mediated pathways.
Role of elicitors in mediating trade-offs
Plant responses to artificial damage and insect damage can differ widely, possibly because of the presence of compo-nents of insect oral secretions that act as signals of herbivore damage. Pathogen-derived elicitors are compar-atively well characterized, but insect-derived elicitors of plant defenses have only recently been identified. Identifying insect-specific elicitors provides an invaluable tool for dissecting plant responses to herbivores, and there-fore for improving understanding of the interplay between plant defenses against pathogens and herbivores.
The best-characterized insect elicitors are those isolated from Lepidopteran oral secretions that elicit a systemic release of volatile plant compounds [27•]. These volatiles attract natural enemies of herbivores, such as parasitoid wasps and predatory mites. One of the first insect elicitors to be identified, N-(17-hydroxylinolenoyl)-L-glutamine, was first found in S. exigua and named ‘volicitin’ [28]. Volicitin elicits the release of volatiles when added to dam-aged corn leaves; wounding alone does not cause the same amounts of compounds to be emitted.
parasitoid attraction [31], and its isolation and in vitro chemical synthesis [32]. Besides volicitin, other related amino-acid–fatty-acid conjugates with varying activity levels are present in the oral secretions of herbivorous insects. The ratio of these compounds, and possibly oth-ers, may ultimately determine the volatile signature of the plant. Linolenic- and linoleic-acid levels found in insect regurgitant are not sufficient to provide the
fatty-acid signal associated with the accumulation
wound-induced genes, such as the protease inhibitor II gene in tomato [33]. The profiles of volatiles released after treatment with JA or JA precursors are significantly different from herbivore-induced responses [34], and again, suggest that the overall blend of elicitors and even signaling molecules within the plant can play a determining role.
Herbivore elicitors may impact multiple signal transduc-tion pathways. For example, Kahl et al. [35•] found that when oral secretions from M. sexta were applied to Nicotiana attenuata large increases in JA- and ethylene-accumulation resulted, and suppressed nicotine induction. The release of volatile terpenoids was not, however, inhib-ited. M. sexta secretions contain several volicitin-like amino-acid conjugates of fatty acids, which elicit JA and volatile synthesis (R Halitschke et al., personal communi-cation; HT Alborn, MM Brennan, JH Tumlinson, personal communication). The elicitation of volatiles involves addi-tional signaling components that are separate from nicotine production [36]. In addition to volicitin-like signals, it is likely that there are many other classes of insect-derived elicitors to be discovered. A low molecular weight peptide-type class of pathogen and insect elicitors, called the peptaibols, was recently discovered and shown to stimu-late all of the major defense pathways (i.e. the JA, SA and ethylene pathways) [37].
Whereas the role of oral secretions in triggering antiherbivore defenses is becoming clearer, the role of oral factors in medi-ating plant responses to phytopathogens is less well understood. Saliva from noctuid caterpillar species such as H. zeacontains high concentrations of a glucose oxidase [38]. The glucose oxidase acts as a signal to the plant, triggering a local oxidative burst, the accumulation of SA, and in soybean, SAR to P. syringaepv. glycinea(GW Felton, unpublished data). The salivary glucose oxidase may explain H. zea-induced resistance to P. syringaepv. tomato [8••].
The speed and extent of responses to pathogen attacks may be critical in determining whether the plant or the pathogen prevails. The same may be true of responses to insects. Transcript accumulation around a wound site occurs more rapidly after insect damage than after artificial wounding [39]. This shortened response time can be mimicked when
The activity of one of the key enzymes in the biosynthesis of some volatile terpenes has been characterized [40]. Nerolidol synthase, which catalyzes the formation of (3S)-(E)-nerolidol, is strongly induced after insect damage but not in response to artificial wounding. The cloning of the genes encoding such differentially controlled enzymes and their promoters could provide valuable tools for the elu-cidation of the signaling pathways and regulatory proteins involved in insect-specific responses. Likewise, PR genes and proteins have facilitated the study of pathogen defense.
Conclusions
The evidence for trade-offs between herbivore and pathogen defense has appeared to be capricious. It had been assumed that defense signaling associated with her-bivores and pathogens is primarily restricted to the JA and SA pathways, respectively. Recent evidence, provided by the characterization of signals in herbivore saliva, indi-cates a much greater degree of specificity than had generally been assumed, and that JA-independent responses may be triggered by herbivory. Because multi-ple pathways are elicited during attack by either herbivores or pathogens, a clear dichotomy between pathogen- and herbivore-specific defense pathways does not always exist [4,5,8••,14•,16,41,42••]. The use of gain- and loss-of-function molecular genetics is revealing how multiple signaling pathways interact and function as defense-signal networks. Increased efforts in characterizing herbivore elici-tors and their interaction with particular signaling pathways will further our understanding of the interplay between her-bivore and pathogen defense. Understanding cross-talk between these two seemingly disparate defense pathways might foster a more effective application of plant treatments aimed at inducing pest defenses.
Update
Recently, a cDNA microarray technique was used to com-pare the expression of 150 defense-related genes in mechanically wounded Arabidopsis leaves to expression in leaves wounded by larvae of the cabbage butterfly Pieris rapae [43••]. Feeding by the larvae specifically induced only one gene that encoded a hevein-like protein. Many wound-induced genes were induced either to a lesser extent or not at all by feeding, thus indicating that larval feeding strategies may minimize the induction of defense-related genes. Using JA- and ethylene-insensitive mutants, the authors also showed that several signal pathways regu-late insect-induced gene expression [43••]. Scores of JA-independent genes were induced by insect feeding, but none of these genes required ethylene to respond.
and herbivores attacking Rumex spp. They have shown that rust infection of Rumex reduces the fitness of the bee-tle Gastrophysa viridula. Conversely, beetle herbivory induces systemic and local resistance to the rust [44••].
Acknowledgements
We thank the Samuel Roberts Noble Foundation, the National Science Foundation and the United States Department of Agriculture for supporting research in our laboratories. We are grateful to colleagues who shared results prior to publication.
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
• of special interest
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