Signal conflicts and synergies in induced resistance to multiple attackers

Physiological and Molecular Plant Pathology (1999) 55, 99–109 Article No. pmpp.1999.0218, available online at http:\\www.idealibrary.com on

M I N I-R E V I E W

Signal conflicts and synergies in induced resistance to multiple attackers R . M . B O S T O C K* Department of Plant Pathology, UniŠersity of California, One Shields AŠe., DaŠis, CA 95616, U.S.A. (Accepted for publication May 1999)

INTRODUCTION Plants are often simultaneously challenged by pathogens and insects capable of triggering an array of systemic responses that may be beneficial or detrimental to plant health and productivity. Inducible defenses in plants against pathogens and insect herbivores can be strongly influenced by the mix of signals generated by external biotic factors as well as by abiotic stresses such as drought, nutrient limitation, or high soil salinity. Our ability to capitalize on inducible defenses and utilize them optimally in agriculture depends, in part, upon a fundamental knowledge of their biochemical nature, and of the specificity and compatibility of the signaling systems that regulate their expression. The importance of the phytohormones salicylic acid and jasmonic acid as critical signals in induced resistance responses in plants is recognized [39, 57, 74, 92 ]. As these chemicals can strongly influence other processes in plant growth and development, it would not be unexpected that interactions could occur between them and with other phytohormones and signal molecules [52, 84, 103 ]. The literature on induced plant resistance to pathogens and insects has historically concentrated on studies of one type of challenger. As the area has matured, studies have adopted an expanded perspective to include the mix of attackers that a plant species might encounter in the field, although, for logistical reasons, the mix included just pathogens or just insects, but generally not both. Numerous studies in the plant pathology and entomology literature describe vector relationships involving insects and pathogens, but relatively few have considered insects and pathogens simultaneously with respect to their comparative signaling of, and impact on, inducible host * All correspondence should be addressed to R. M. Bostock, email : rmbostock!ucdavis.edu ; Tel : 530 752 0308 ; Fax : 530 752 5674 ; Department of Plant Pathology, University of California, One Shields Ave., Davis, CA 95616, U.S.A. Abbreviations used in text : ABA, abscisic acid ; CK, cytokinin ; PR, pathogenesis-related ; SA, salicylic acid ; SAR, system acquired resistance. 0885–5765\99\080099j11 $30.00\0

defense. Prior investigations of plant-mediated interactions between plant pathogens and arthropod herbivores have yielded mixed results [2, 3, 6, 54, 62, 76 ]. The evidence for interactions—positive and negative— among pathways controlling resistance to different types of attackers provides the topic for this review. As we enter an era of opportunity for deploying induced resistance strategies in the field, I think it useful to consider interactions that may occur among candidate signaling molecules. The literature often puts a positive spin on induced resistance, which is well-founded, but is all too often silent on potential complications. What is unclear is the cost of induced resistance to plants in terms of defense against different types of challengers and in relation to fitness (natural populations) and productivity (crop yield). Some studies reveal synergies between wounding and signals generated by pathogen infection in inducing host responses and resistance [51, 53 ]. However, other studies point to a potential increased vulnerability when plants must contend with different types of attackers that apparently harness different response pathways [44, 112 ]. Relevant to any discussion of systemic signaling and defense is also the extensive literature on predisposition to pathogens and pests by abiotic stresses capable of systemically modifying the balance of phytohormones such as abscisic acid, cytokinins, and ethylene [1, 15, 18 ]. My intent is not to play the role of devil’s advocate, but rather to provoke discussion and research that considers signal interactions and potential trade-offs in defense to different types of attackers that may occur in the field. In this review, I discuss plant responses to different types of pathogens and insects, with emphasis on phytohormone signals and their interactions that may condition inducible resistance or susceptibility. SALICYLATE SIGNALING IN DISEASE RESISTANCE Salicylic acid (SA) is now recognized as a critical signal for the expression of induced resistance to many pathogens. Systemic acquired resistance [SAR ; 53, 66, 92 ] is typically # 1999 Academic Press

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used in the context of salicylate-mediated induced resistance, although there are examples of apparently salicylate-independent systemic resistance, such as that induced in some plants by rhizobacteria [117 ]. The evidence for a role of SA in SAR is compelling. This discovery has stimulated innovative approaches to the study of induced disease resistance and has provided a basis for synthetic chemistry leading to novel compounds for field application [65 ]. Treatment of tobacco and other plant species with SA and related chemicals triggers a spectrum of pathogenesis-related (PR) proteins and induces resistance to pathogens [50, 65 ]. Perhaps the most compelling line of evidence derives from studies where SA levels have been modified transgenically through introduction of nahG, a gene encoding salicylate hydroxlase from Pseudomonas putida [31, 47 ]. Tobacco plants containing nahG have negligible levels of SA, do not express SAR, and display a hypersusceptibility to a variety of disease agents [31 ]. Disease resistance can be induced in plants by spray treatments with SA or more potent synthetic mimics such as isonicotinic acid and benzothiadiazole [39 ]. The SA pathway in resistance expression to pathogens is being further characterized with a number of SA synthesis and response mutants in Arabidopsis [30, 33, 49, 93 ]. In tobacco, the amount of SA produced in the plant appears to be related to the amount of necrotic lesion development [123 ], consistent with earlier studies in cucurbits showing a semi-quantitative relationship between the inducing inoculum dose and the degree of protection following challenge with the anthracnose fungus [59 ]. These findings also suggest that a particular type of injury, e.g. hypersensitive response (HR) or necrotic lesion, is a principal stimulus for SA generation, although SA does not appear to be a critical stimulus for cell death [63 ]. The evidence for SA as an important local signal is solid. However, it is questionable that SA is the systemically mobile signal traveling from the inducing leaf to systemically condition the resistance response. This evidence is primarily based on elegant experiments on the timing of appearance of SA in the vascular system of cucumber plants in relation to systemic resistance expression [85 ] and reciprocal grafting of salicylatecompetent and salicylate-deficient tobacco shoots and roots [118 ]. This evidence supports the notion that a different mobile signal is generated by the inducing leaves to trigger the production of SA elsewhere in the plant. SA is not reported to induce resistance to insects [61 ], although certain insects can induce SA-triggered responses in plants. For example, we have found that aphid injury elicits a pattern of host responses in tomato leaves that are typical of pathogen-induced responses, including the accumulation of PR proteins, but not proteinase inhibitors typically observed in response to wounding by noctuid larvae like the corn earworm [46, 106 ]. Mite feeding will

induce systemic resistance to Verticillium dahliae in cotton [62 ], although it is unknown if this is a SA-based resistance. These findings indicate that feeding damage by certain insects (e.g. sucking insects) triggers signaling pathways that are more characteristic of pathogens than insects that have been used traditionally for induced resistance studies (e.g. chewing insects). Clearly, there is a need for additional studies that assess the performance of insects of different feeding guilds on salicylate-modified plants. SA’s role in conditioning defense responses to certain pathogens is well-established. However, the mechanism(s) by which it does so is unclear. SA and related hydroxybenzoates interact with Fe#+ in heme and non-heme containing proteins, either through chelation or as an electron donor to generate a highly reactive salicylate radical [39, 48, 91 ]. For example, a SA binding protein was characterized in tobacco as a catalase [24 ], and allene oxide synthase [102 ] is a step in jasmonate synthesis that appears to be a site for SA inhibition (see below). Both are heme proteins. However, the basis for SA’s effect on SAR expression is unresolved, and it is likely that SA has multiple targets in the cell to regulate SAR [39 ]. Critical for study of functional targets of SA in induced resistance is consideration of the kinetic parameters and cellular concentrations of the interacting factors. Also unresolved is the issue of SA having a more profound effect on cellular homeostasis. Recently, we have observed a lesion mimic phenotype in tomato plants expressing nahG (unpublished observations). The phenotype can be partially complemented by exogenous treatment with benzothiadiazole. DNA extracted from symptomatic leaves of these plants displays a fragmentation pattern on gels characteristic of that observed in cells undergoing programmed cell death [120 ]. The implication of this observation is that dysregulation of SA metabolism may impact cellular functions that are involved in apoptosis.

JASMONATE SIGNALING IN PLANT DEFENSE Induced resistance to insects The octadecanoid pathway leading to jasmonic acid biosynthesis has been studied extensively in relation to the wound-induced systemic induction of proteinase inhibitors and resistance to insect herbivores. The jasmonates, derived from peroxidized linolenic acid, are members of a large class of oxygenated lipids [‘‘ oxylipins ’’ sensu Hamberg and Gardner, 52 ] generated by the action of lipoxygenases on polyunsaturated fatty acids. Jasmonic acid and its volatile ester methyl jasmonate are potent inducers of proteinase inhibitors [42, 43, 94 ] and of other factors such as polyphenol oxidase and lipoxygenase [37, 105 ], and can protect plants from insects of different feeding guilds in both greenhouse and field tests [61, 111 ].

Resistance to multiple attackers Systemin is a polypeptide released during wounding of tomato leaves by herbivores and capable of systemic movement within the plant. Current models place systemin as an initiator of a cascade that triggers the release of linolenate from membrane lipids and the synthesis of jasmonic acid to activate genes encoding the proteinase inhibitors and other anti-herbivore defenseassociated factors [10, 96, 121 ]. Direct experimental evidence strongly supports most of the elements of this model, with some of the most compelling experiments being those which have demonstrated that transgenic suppression of proteinase inhibitors [60 ] or of the signaling components that regulate their expression markedly enhances suitability of plant foliage to insect herbivores [74, 75 ]. To my knowledge, a thorough comparative study of the types of feeding damage that elicit oxylipin production has not been conducted, although inferences can be made from expression studies of jasmonate-responsive genes and activities [for example see 46, 86 ]. It is unknown if systemin-like molecules with similar function are present in other plant species. The capacity for jasmonate and related oxylipin synthesis is highly conserved among plants, but the molecular triggers for oxylipin production in the context of responses to pests and pathogens, except perhaps in the case of systemin in tomato, are not characterized. It should also be noted that there is evidence for wound-induced gene expression that is jasmonate independent in Arabidopsis [114 ]. By analogy with arachidonate release and oxygenation in mammalian systems, models have been presented that invoke a scenario wherein a stimulus activates a Ca#+-mediated phospholipase that releases linolenate for peroxidation by a specific lipoxygenase and further metabolism of the fatty acid hydroperoxide to jasmonic acid. Studies in Arabidopsis support a chloroplastic location as a site for jasmonate synthesis [9 ], although it is unresolved if there are additional subcellular sites enlisted in different stress contexts in different species. Jasmonate synthesis and response mutants in Arabidopsis have been used to discern jasmonate function in plant defense against insects [74, 104 ]. McConn et al. [74 ] challenged linolenate-deficient mutants (that are consequently jasmonate-deficient) with larvae of the fungal gnat, Bradysia impatiens. The mutants were heavily damaged compared to the wild-type plants, providing evidence that affirms an important role for jasmonate action in defense, although the nature of the resistance factors in this system are unknown. Since peroxidation of linolenate to 13-hydroperoxyoctadecatrienoic acid is an essential first step in the path to jasmonate synthesis, there has been a surge of interest in the isolation and characterization of plant lipoxygenases. Lipoxygenases occur as gene families in higher plants with as many as three (Arabidopsis) to eight or more

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isoforms (soybean) [45, 101 ]. A number of studies have reported lipoxygenase activation following wounding, pathogen infection, or challenge by insect herbivores. The recent cloning of different lipoxygenase isoforms has permitted expression studies that discriminate among lipoxygenase genes that are induced by wounding, jasmonates or other stimuli [for example, see 56, 89 ]. A recent study by Royo et al. [90 ] showed that insects (i.e. Colorado potato beetle and beet armyworm) gain more weight and cause more damage on transgenic potato plants displaying antisense suppression of a specific leaf lipoxygenase compared to wild-type plants. The transgenic plants were also compromised in their expression of a wound-induced proteinase inhibitor. Surprisingly, wound-induced jasmonate levels in the antisensed plants were not different from those in the wild-type controls, raising the possibility that a different lipoxygenase from the one suppressed is involved in jasmonate synthesis and that the modified lipoxygenase contributes to host resistance by an additional mechanism(s) distinct from octadecanoid signaling. It is also possible that lipoxygenase is not rate limiting, and a study in Arabidopsis points to allene oxide synthase, the next enzyme in the oxylipin pathway, as a key regulatory step [70 ]. What is clear thus far from expression studies and the phenotypes of lipoxygenase-modified plants is that the role of lipoxygenases is complex, and further studies are needed to ascribe functional relevance to the various lipoxygenase isoforms and their products. Abscisic acid (ABA) and ethylene also factor into the mix of signals that modulate wound-induced gene activation in Solanaceous plants [121 ]. ABA involvement was suggested by studies with ABA-deficient tomato and potato mutants in which the wound- and systemininduced levels of proteinase inhibitor II in leaves were markedly reduced compared to wild-type plants [79, 81 ]. ABA is believed to operate upstream of the octadecanoid pathway, possibly through an effect on release of the JA precursor linolenic acid [121 ]. A study by Dammann et al. [29 ] indicates that ABA modulation of wound-responsive genes in potato is complicated, and provides evidence for a jasmonate-independent pathway for ABA induction of wound-inducible genes in certain organs. A role for ethylene, a well-known product of wounded plant tissue, has been suggested through experiments in which its synthesis or action has been modified. Ethylene can positively regulate jasmonate levels in the plant [78 ], and jasmonate and ethylene appear to be required together to induce a defensin gene in Arabidopsis [82 ].

Induced resistance to pathogens Investigations during the past decade or so have provided some credence to the notion of a dichotomy in signaling

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for defense against pathogens and insects [see for example 37, 41, 46 ], with distinct pathways for each type of attacker. In fact, frequently researchers would employ a wound treatment as a control for biochemical studies of responses to pathogens. It is clear that jasmonate and wounding trigger a different set of responses than those associated with salicylate and many pathogenic agents [13 ]. In spite of this evidence, there have been attempts at a ‘‘ unified field theory ’’ for defense signaling to pathogens and pests that posits jasmonate as an early and critical signal [86 ]. We now know that the notions of either a single pathway or of separate response pathways conditioning defense against all types of pathogens and all types of insects are simplistic and certainly not borne out by current studies. A compelling study using signaling mutants in Arabidopsis illustrates neatly the case for different signaling pathways for different types of pathogens [113 ]. Several recent papers support the participation of jasmonate in plant defense to some pathogens. For example, resistance induced by certain rhizosphere bacteria requires jasmonate and ethylene perception [117 ]. Another study revealed that jasmonate synthesis and perception mutants in Arabidopsis are highly susceptible to the root pathogen Pythium mastophorum, and that this resistance is due to jasmonate-induced responses in the plant [119 ]. Jasmonic acid has been reported to induce local and systemic resistance in potato and tomato to the late blight pathogen Phytophthora infestans, although it is unclear if the relatively high concentrations required may have induced some necrosis to trigger other signals [27 ]. Jasmonic acid is produced rapidly (within hours of inoculation) during the HR in tobacco to Pseudomonas syringae pv. phaseolicola [64 ], although its contribution to the HR phenotype is unknown and jasmonate treatment does not elicit cell death at concentrations capable of inducing defense-associated responses such as proteinase inhibitors. Jasmonates induce a number of proteins (JIPs) in plants, most of which are of unknown function, but some may have antimicrobial activity [86 ]. Jasmonate treatment of barley plants induces JIPs and provides some protection against Erysiphe graminis f. sp. hordei, but the effect appears to be due to a direct inhibition by jasmonic acid on appressorium formation [97 ].

Interaction between octadecanoid and salicylate signaling pathways Signal generation and decay is fundamental to circuits that govern cellular responses (e.g. the ‘‘ creative tension ’’ between kinases and phosphatases in phosphorylation cascades). One would expect that the same would be the case for octadecanoid and salicylate signaling, although the turnover of these signals in plants following challenge

has received relatively little attention thus far (except perhaps as artificially engineered with nahG expression). However, the evidence for a negative interaction between the SA and jasmonate pathways receives short shrift in models of defense signaling. This is indicated by the levels of biochemical response and, recently in resistance responses to biotic challenge in greenhouse and field experiments. SA applied exogenously to tomato plants will inhibit wound-induced proteinase inhibitor synthesis [35, 80 ] possibly through the inhibition of jasmonate biosynthesis and action [34 ]. There is also evidence for inhibition of salicylate action by jasmonic acid [95 ]. Studies in potato and tobacco have shown that microbial elicitors such as arachidonic acid and mycelial cell wall preparations—which can also trigger SA production— invoke different isoprenoids than jasmonate treatment or artificial wounding [22, 25, 26, 125 ]. These shifts in secondary metabolism are manifested at the level of mRNA abundance of different HMG-CoA reductase isoforms which respond rapidly and inversely to jasmonate and elicitors. These and other changes in the acetatemevalonate pathway result in the apparent channeling of precursors to different antimicrobial isoprenoid endproducts. Perhaps the stress-induced shifts in isoprenoid metabolism observed in the Solanaceae reflect a fundamental program in plants to segregate processes for wound repair from those directed to cell death. Since SA can diminish expression of wound-responsive genes encoding anti-herbivore activity, one would predict that SA and its analogs should have a corresponding impact to enhance insect performance on plants expressing SAR. In recent studies, we found that stimulation of SAR with benzothiadiazole in greenhouse and field grown tomato plants attenuated the jasmonate-induced expression of proteinase inhibitors and polyphenol oxidase, and resulted in increased performance of noctuid larvae of the corn earwarm (HelicoŠerpa zea) and beet armyworm (Spodoptera exigua) [106, 112 ]. Conversely, treatment of plants with jasmonic acid at concentrations that induce resistance to insects reduced PR protein gene expression induced by benzothiadiazole, and partially reversed the protective effect of benzothiadiazole against bacterial speck disease caused by Pseudomonas syringae pv. tomato (Pst). Hence, in the tomato system there appears to be a reciprocal attenuation of signaling pathways that condition resistance to insects and a bacterial pathogen. Complicating these observations is evidence that salicylate and octadecanoid signaling may be complementary in some plants. In rice, jasmonic acid enhances the induction by the salicylate-mimic isonicotinic acid of pathogenesis related gene expression [99 ], although treatment with jasmonate alone will not induce resistance to the rice blast pathogen, Magnaporthe grisea [98 ]. In Arabidopsis, SA induces allene oxide synthase activity, a critical step in jasmonic acid biosynthesis, albeit without

Resistance to multiple attackers increasing jasmonic acid levels [70 ]. During the HR in tobacco, jasmonic acid accumulation precedes and temporally parallels the localized accumulation of SA [64 ]. Tobacco, engineered to express a heterologous resistance gene (Cf-9 from tomato), will produce both a woundactivated MAP kinase and a salicylate-activated MAP kinase in response to elicitor treatment, suggesting some convergence in signaling [88 ]. Also complicating interpretation of our results is that Pst infection induced both PR proteins and proteinase inhibitors, as well as resistance to itself or H. zea, indicating that under certain conditions of induction both pathways may be operative and seemingly compatible [46, 106 ]. It is difficult to rationalize these apparently conflicting results, which underscore the need for research that critically assesses the concentrations and cellular sensitivity to salicylates and octadecanoids, the kinetics of their accumulation, and the tissue and cellular sites of synthesis and accumulation. The tissue level analyses conducted cannot resolve separate cells within tissues that could be enlisted for synthesis of and response to different signals. Furthermore, biotic agents likely generate a complex mixture of signals that may not be generated by treatment with pure chemical inducers like benzothiadiazole and jasmonic acid. PREDISPOSING ABIOTIC STRESS : A CASE FOR DAMPENED RESISTANCE SIGNALING ? Plants have common mechanisms for responding to diverse stresses. A centralized system of stress response [20 ] is suggested by common traits associated with plants adapted to low-resource environments and by physiological studies that have shown changes in the balance of phytohormones, notably ABA and cytokinins, during plant response to most stresses. The results of such changes are reduced growth, low photosynthetic rate and reduced capacity for nutrient uptake [21 ]. It is not surprising, then, that the signals that are apparently enlisted to engage defense responses following biotic challenge include the same ones that can impact other systems in the plant in a profound manner following episodes of other types of stress. This is apparent from studies with jasmonates, ethylene, and ABA, where their application to plants can reduce growth or induce senescence [5, 40, 67, 83, 116 ]. SA application also can have a number of physiological effects besides its impact on disease resistance, such as floral induction, reduction of transpiration, and effects on membrane potentials and ion uptake, but one that seems most relevant to the present discussion is a reversal of certain ABA-regulated responses [84 ]. Interactions and trade-offs in the integration of plant stress responses provide a valuable perspective for understanding potential limitations and possibilities of induced resistance strategies in agriculture where plants experience

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multiple stresses [20, 21 ]. This integration involves consideration of shifts in resource allocation and utilization that occur when conditions become suboptimal for plant growth. Such potential interactions and trade-offs raise important questions. Are resistance mechanisms against pathogens and herbivores compatible in all cases ? Will moderate abiotic stresses commonly encountered in crops during the growing season influence the activity of chemicals that induce defense against pests ? An understanding of the interaction of signals operative following episodes of abiotic stresses and during expression of induced resistance would be informative for deployment of chemical or biological inducers of resistance. These interactions could be positive or negative with respect to crop protection. For example, an important study by Xu et al. [122 ] illustrates the potential for synergy between specific combinations of signals in their elicitation of certain PR proteins. Ethylene may be synergistic with jasmonate in its induction of the stress-induced protein osmotin, and SA and jasmonate can be synergistic in PR-1 induction. The authors suggest that specific combinations of signals provide ‘‘ signature ’’ sets to initiate an appropriate response to a specific stress. Signal synergy is also indicated for other environmental signals, such as that reported for ABA and NaCl [14 ]. The influence of abiotic stresses on plant defense are particularly well-studied in stress predisposition to root pathogens. Plant stresses resulting from prolonged soil saturation [low O ; 11 ], or cycles of drought [38, 87 ] or # salinity [71, 107 ] can increase the severity of diseases caused by Phytophthora spp. and other pathogens. Collectively, this research has shown that significant predisposition can occur as a result of relatively minor stresses, and that the pathogenic species of concern function effectively in soil during (or, in the case of drought, immediately after) the stresses that cause predisposition [12 ]. The stress levels which are thresholds for predisposition can occur routinely in agriculture and, in the absence of a pathogen, plants usually recover rapidly and fully. There is evidence that predisposition results from suppressed host resistance reactions [108 ], but little is known of underlying signals or mechanisms. Predisposing responses could be mediated in part by elevated levels of ABA and perhaps other phytohormones\signals induced in stressed plants that operate in concert with ABA to compromise resistance. Salinity, drought and low O are similar in their physiological # effects in that all three induce some degree of water stress [15, 23 ], which can trigger rapid change in the systemic levels of ABA, ethylene, and cytokinin [CK ; 17, 18, 124 ]. ABA levels in leaves [124 ] and roots of mesophytic plants [28 ] increase rapidly after imposition of water stress, and decline after recovery. The increase in ABA and decline in CK, which opposes ABA action, reduces internal water stress primarily by causing stomatal closure and increasing

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root hydraulic conductance [16, 72, 124 ]. If increased levels or sensitivity to ABA contribute to stress-induced predisposition to pathogens, other treatments that alter ABA level or response sensitivity in roots and stems should also yield changes in disease proneness. Indeed, in experiments with chrysanthemum and tomato, we have found that exposing the roots of nonstressed plants to exogenous ABA shortly after inoculation significantly increased lesion expansion by Phytophthora cryptogea on chrysanthemum and P. parasitica on tomato (unpublished observations). The resulting root rot in ABA-treated plants was as severe as that in salt-stressed plants. Another strategy for altering plant ABA levels is with ABA-deficient mutants. The wilty mutants of tomato, flacca, sit, and not, segregate to three separate loci, and the lesions in ABA biosynthesis caused by these mutations have been partially characterized [77 ]. Following stress episodes, these mutants accumulate only a small percentage of the ABA present in the wild-type cultivar, and they do not show the adaptive responses to water stress [16, 109, 110 ]. Since the mutants do not accumulate high levels of ABA in response to salt, one would predict that under equivalent stresses they may be predisposed less to disease than the wild-type. Indeed, in preliminary experiments using Phytophthora capsici as a challenge we have found this to be the case. These results are consistent with the hypothesis that salt-induced predisposition to disease operates in part through ABA. Since abiotic stresses and the resulting signals generated within the plant can modify host plant resistance to pathogens [also see 8, 19 ], it is also true and not surprising that insect performance can be impacted by physiological stress to the host [55, 73 ]. Moderate to severe water stress results in numerous physiological and morphological changes in plants that can result in improved performance of phytophagous insects [73 ]. Many of these studies deal with insect outbreaks in plant populations (e.g. forests) within a stress context of some prolonged duration, and have tended to focus on insects of a particular feeding guild [69 ]. The performance of insects of different feeding habits may be impacted differently depending on the magnitude of the stress and their feeding specialization [69 ]. What is unclear is how brief episodes of water or osmotic stress, such as the disease predisposing conditions described above, impact insect herbivory and performance, particularly in mesophytic crop plants like tomato growing with optimal nutrients and little competition. Mild stresses, resulting in transiently elevated ABA levels in roots and shoots, might actually stimulate proteinase inhibitor accumulation and other factors that contribute to defense against certain arthropods. Such an outcome would be in accordance with the evidence that plants adapted or responding to stressful environments shift resources towards defensive compounds [21 ]. Nonetheless, explicit definition of the type and degree of stress to the

plant and consideration of the differences in feeding and parasitic habits are vital for interpretation of experimental results. These issues would seem to be crucial to any rationally based deployment of induced resistance in the field, or for any hypothetical model that attempts to draw congruence from the data on defense-related signals and responses. CONCLUSIONS AND PERSPECTIVES Induced resistance to pathogens and insects is viewed as a desirable crop protection strategy with a relatively benign environmental impact. The recent development of synthetic compounds like benzothiadiazole for field application attests to the keen interest in, and potential for incorporating, induced resistance in pest management programs [50, 65 ]. In addition to chemical agents, biological agents that induce resistance to insects and pathogens are also under scrutiny for use in crop protection. Crucial to the success of induced resistance in agriculture is an understanding of the range and limitations of this form of pest control, especially in different stress contexts. There is sufficient evidence to indicate potential constraints at the level of specific signal interactions whereby it may not be possible to simultaneously maximize defense against all kinds of attackers. Indeed, induction of resistance to one pest may result in an increased vulnerability to another. I would propose that these constraints derive in part from the balance of interacting regulatory signals, all of which can be strongly influenced by abiotic stresses typically encountered in agriculture. The degree to which salicylate- and jasmonate-based resistances are counteractive or synergistic within the larger network of regulatory signals is unresolved. The potential for interaction among abiotic and biotic stressors provokes a number of intriguing issues that could impinge on our ability to deploy or optimize induced resistance strategies. Figure 1 illustrates signal generation and interaction during responses to insects, pathogens, and abiotic stresses. The primary paths of signal\ phytohormone induction by ‘‘ classical ’’ damaging agents (e.g. chewing insects, necrotrophic pathogens) are indicated by solid arrows ; secondary paths (arrows with dotted lines) give recognition to the fact that some agents do not fit these classical injury modes. The connection with the question mark illustrates the potential for positive and negative interactions (e.g. SA interference with jasmonate synthesis and response ; ABA interference with resistance to pathogens but enhancement of jasmonateregulated responses). These signals trigger gene expression and metabolism that may or may not contribute to defense against a particular pest, and may actually compromise resistance to some. The model also recognizes that host plants have ‘‘ susceptibility ’’ factors influenced

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Resistance to multiple attackers Pathogen signals Elicitors Aphid injury

Insect herbivory wounding

Salinity Drought Anoxia Abiotic stresses

JA ABA ethylene CK( )

Altered gene expression and metabolism

Induced resistance Suppression of host “susceptibility” factors to insects

?

Salicylic acid Ethylene Other signals ?

Altered gene expression and metabolism

Compromised host defense metabolism Induction of host “susceptibility ” factors

Systemic acquired resistance Suppression of host “susceptibility” factors to pathogens

F. 1. Signal generation and interaction during responses to insects, pathogens and abiotic stresses.

by these signals that may contribute to the demise of the plant if expressed inappropriately (e.g. endogenous cell wall degrading enzymes and genes that regulate programmed cell death ; [120 ]). An assumption of this model is that effective plant resistance to most insects and pathogens involves multiple genes and mechanisms, hence it emphasizes more general signals or mechanisms that regulate responses to pest challenge. I would view the model as most relevant for mesophytic plants experiencing stresses of a temporary nature. Studies of SAR to pathogens and induced resistance to insects have proceeded with relatively little consideration of possible interactions between the two [39, 61 ]. Our research indicates that plant-mediated interactions occur in tomato leaves challenged with different insect herbivores and pathogens that can impact insect performance and disease severity [106, 112 ]. An interaction between salicylate and jasmonate signaling is evident from gene expression and biochemical studies and is manifested at the level of defense to certain pests. There is a potential increased vulnerability of tomato foliage to insect herbivory when plants are chemically induced with benzothiadiazole to express SAR to pathogens. Unresolved is the degree of reciprocity among signal-response pathways, as well as the interplay of other stress-induced regulatory signals on the inducibility of host resistance to insects and pathogens. Inhibition of jasmonate-mediated signaling by salicylates might also interfere with the attraction by wounded plants of the natural enemies of herbivores [32, 36, 100, 115 ]. Recent work has shown that production of volatile parasitoid attractants are regulated by a branch of the octadecanoid pathway [4 ]. An advantage of inducible defenses over constitutively expressed defenses may be to allow the plant to engage

signal–response pathways that will be most effective against the respective challengers, and it would seem then that there is some evolutionary selective advantage for induced resistance. This reasoning is predicated on the notion that such defensive traits evolved to fulfill this hypothesized function, but it is naı$ ve to make this assumption. They may or may not have been maintained for this purpose. I quote from an excellent discussion of this issue by Karban and Baldwin [61 ] : ‘‘ … traits we presume to haŠe been preserŠed because they proŠide defense, may haŠe been pulled along by pleitropy, in which one gene affects many different traits, or by linkage, in which genes are bound together and not inherited as distinct entities. We must be willing to consider and deŠelop other plausible eŠolutionary scenarios, what Kitcher [58] called riŠal Darwinian histories, to explain why we find induced defenses. We must also be willing to accept that some current traits may not result in the highest fitness but may persist because of lack of Šariation, as a consequence of genetic drift, or because of selection on another correlated trait. ’’ A consideration of alternative evolutionary scenarios could underscore a more holistic viewpoint of physiological functions of induced ‘‘ defenses ’’, and would be useful as we design experiments that address possible ramifications and trade-offs in plant metabolism that may undermine or enhance induced resistance in certain contexts. We know little about the fitness costs of induced resistance conditioned by SA or jasmonate, although some work is beginning to emerge on this topic [7 ]. Systems that are readily manipulable for genetic, molecular, biochemical and physiological studies are requisite to resolve issues concerning signaling conflicts and synergies in induced resistance. Tomato provides a reasonably good model, and Arabidopsis affords advantages

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at the genetic and molecular levels, but suffers from the fact that many of the pathogens selected for study are rather contrived and unnatural for this host. Mutants are powerful, but for the types of regulatory signals in question can suffer from the ‘‘ problem of pleiotropy ’’, i.e. the general consequences to the physiology and health of the plant of prolonged alterations in the synthesis or perception of a given signal can make it difficult to draw conclusions about cause and effect. Just as deployment of other strategies to pest and disease management presented challenges, so too will induced resistance as we attempt to integrate this approach in plant health programs [68 ]. To meet these challenges the collective expertise in entomology, plant pathology, and plant biology will be crucial to address the issues at the different levels of complexity, ranging from the molecular biology and biochemistry of signaling to whole plant and field studies of plant performance to multiple attackers. I would like to thank my colleagues, Richard Karban, Jennifer Thaler, Ana Fidantsef, Michael Stout, David Gilchrist, John Duniway and James MacDonald for discussions over the years of various aspects of some of the ideas presented here. I also acknowledge my late colleague, Sean Duffey, for his insights, friendship, and an all too short but productive collaboration. The author’s research is supported by the USDA National Research Initiative Competitive Grants Program and by CEPRAP, the NSF Center for Engineering Plants for Resistance Against Pathogens. REFERENCES 1. Abeles FB, Morgan PW, Saltveit ME Jr. 1992. Ethylene in Plant Biology, 2nd edn. San Diego : Academic Press. 2. Ajlan AM, Potter DA. 1991. Does immunization of cucumber against anthracnose by Colletotrichum lagenarium affect host suitability for arthropods ? Entomologia Experimentalis et Applicata 58 : 83–91. 3. Ajlan AM, Potter DA. 1992. Lack of effect of tobacco mosaic virus-induced systemic acquired resistance on arthropod herbivores in tobacco. Phytopathology 82 : 647– 651. 4. Alborn T, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, Tumlinson JH. 1997. An elicitor of plant volatiles from beet armyworm oral secretion. Science 276 : 945–949. 5. Albrechtova JTP, Ullmann J. 1994. Methyl jasmonate inhibits growth and flowering in Chenopodium rubrum. Biologia Plantarum 36 : 317–319. 6. Apriyanto D, Potter DA. 1990. Pathogen-activated induced resistance in cucumber : response of arthropod herbivores to systemically protected leaves. Oecologia 85 : 25–31. 7. Baldwin IT. 1998. Jasmonate-induced responses are costly by benefit plants under attack in native populations. Proceedings of the National Academy of Sciences U.S.A. 95 : 8113–8118.

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