REVIEWARTICLE

Phytohormone Mediation of Interactions Between Herbivoresand Plant Pathogens

Jenny Lazebnik & Enric Frago & Marcel Dicke &

Joop J. A. van Loon

Received: 7 May 2014 /Revised: 3 July 2014 /Accepted: 7 July 2014 /Published online: 25 July 2014# Springer Science+Business Media New York 2014

Abstract Induced plant defenses against either pathogens orherbivore attackers are regulated by phytohormones. Thesephytohormones are increasingly recognized as important me-diators of interactions between organisms associated withplants. In this review, we discuss the role of plant defensehormones in sequential tri-partite interactions among plants,pathogenic microbes, and herbivorous insects, based on themost recent literature. We discuss the importance of pathogentrophic strategy in the interaction with herbivores that exhibitdifferent feeding modes. Plant resistance mechanisms alsoaffect plant quality in future interactions with attackers. Wediscuss exemplary evidence for the hypotheses that (i)biotrophic pathogens can facilitate chewing herbivores, unlessplants exhibit effector-triggered immunity, but (ii) facilitate orinhibit phloem feeders. (iii) Necrotrophic pathogens, on theother hand, can inhibit both phloem feeders and chewers. Wealso propose herbivore feeding mode as predictor of effects onpathogens of different trophic strategies, providing evidencefor the hypotheses that (iv) phloem feeders inhibit pathogenattack by increasing SA induction, whereas (v) chewing her-bivores tend not to affect necrotrophic pathogens, while theymay either inhibit or facilitate biotrophic pathogens. Puttingthese hypotheses to the test will increase our understanding ofphytohormonal regulation of plant defense to sequential attackby plant pathogens and insect herbivores. This will providevaluable insight into plant-mediated ecological interactionsamong members of the plant-associated community.

Keywords Tripartite interactions . Phytohormones . Plantpathogens . Herbivorous insects . Trophic strategy . Feedingmode . Plant-mediated indirect interactions

Introduction

Plant growth, reproduction and defense against biotic andabiotic stressors are regulated by phytohormones (Pieterseet al. 2012). The most common and diverse biotic stressorsof plants are pathogens and herbivores (Pieterse and Dicke2007; Schoonhoven et al. 2005). The populations of theseorganisms have their intrinsic dynamics, yet they influenceone another indirectly through changes in quality of the sharedplant, i.e., plant-mediated indirect interactions (Kaplan andDenno 2007; Ohgushi 2005; Stam et al. 2014; Utsumi et al.2010). Upon insect or pathogen attack, plants are able tomount defensive responses, which underlie plant-mediatedindirect interactions. These defenses are regulated mainly byphytohormones that are induced differently depending on theidentity, sequence, and intensity of attack of the differentstressors (Awmack and Leather 2002; Howe and Jander2008; Stam et al. 2014; Thaler et al. 2012). Plant responsesto pathogens and herbivores can affect the whole communitythrough changes in phytohormones and their downstreamsignaling pathways (Poelman et al. 2008; Tack and Dicke2013). Plants are at the core of terrestrial ecosystems andunderstanding how phytohormones modulate interactionsamong different members in the community can yield impor-tant insight into ecological interactions.

The role of phytohormones in signal-transduction path-ways underlying induced defense has been well documented(Gimenez-Ibanez and Solano 2013; Maffei et al. 2007;Pieterse et al. 2012; Stam et al. 2014; Walling 2009).Crosstalk between these pathways is one way in which plantscan fine-tune their responses by modulating gene expression.Ultimately, each plant-insect or plant-pathogen interaction is aproduct of its unique evolutionary history, and is the result ofan “arms-race” between the two parties in which plant sec-ondary metabolites play a central role (Ehrlich and Raven1964). However, phytohormonal pathways induced in plants

J. Lazebnik : E. Frago :M. Dicke : J. J. A. van Loon (*)Laboratory of Entomology, Wageningen University, P.O. Box 8031,6700 EH Wageningen, The Netherlandse-mail: joop.vanloon@wur.nl

J Chem Ecol (2014) 40:730–741DOI 10.1007/s10886-014-0480-7

can be partly predicted based on herbivore feeding mode: it iswell-documented that insects employing piercing-sucking orbiting-chewing feeding modes elicit different responses inplants (Bonaventure 2012; Broekgaarden et al. 2011).Induction of several defense signaling pathways is knownfor aphids, piercing-sucking insects that feed on phloem sap(De Vos et al. 2005; Kuśnierczyk et al. 2008; Mai et al. 2014).The same applies to pathogens employing different trophicstrategies, i.e. necrotrophic and biotrophic (Pieterse et al.2012). Within the same feeding-mode, whether the attackeris a generalist or specialist also may be an important factor,although this paradigm has recently been challenged in favorof feeding modes as better predictors of phytohormonal re-sponses (Ali and Agrawal 2012; Bidart-Bouzat andKliebenstein 2011). In addition to feeding mode, the suscep-tibility of a plant to a particular attacker also may influencephytohormonal response even within the same insect feedingmode; for example, after aphid attack, salicylic acid-reponsivetranscripts accumulated quicker and to higher levels in leavesof resistant plants than in susceptible ones (De Ilarduya et al.2003). Plant ontogeny also can affect the defense response ofplants to the same attacker; for example, seedlings may allo-cate more resources to defensive chemicals than mature plants(Barton and Koricheva 2010; Boege 2005; Lawrence et al.2003). Each of these factors results in hormonal responses thatinfluence the subsequent or concurrent attacker.Chronological order of stress initiation on plants as well asduration also come into play, leading to considerable variabil-ity in multi-partite interactions (Dicke et al. 2009).

In the case of multiple attacks on plants by organisms ofdifferent kingdoms, relatively little is known about the influ-ence of one attack on the next. Much work has been devotedto understand how plant hormones modulate interactions be-tween plants and their associated insect herbivores (Mithöferand Boland 2012) or pathogens (Glazebrook 2005), but planthormone modulation of three-way interactions among theseplayers is a field that has remained relatively unexplored(Biere and Bennett 2013; Hatcher et al. 2004). In this review,we explore if predictive factors can be identified thatinfluence the biosynthesis of plant defense hormones intri-partite interactions among plants, plant pathogenic mi-crobes, and herbivores. In order to arrive at testable hy-potheses, we focus especially on the most studied hor-mones, jasmonic acid, salicylic acid, and ethylene. Otherphytohormones such as auxin, giberellins, cytokinins, andbrassinosteroids also are involved in plant defense re-sponses, yet their roles in tripartite interactions have beenmuch less studied (Bari and Jones 2009; Pieterse et al.2012). To generate hypotheses about these interactions, itis important to first discuss what is known about regula-tion by phytohormones of plant responses to microbialstressors like bacteria, fungi, and viruses, and to insectherbivory and how it affects subsequent attacks.

Plant-Pathogen Interactions

Plant Responses to Pathogen Infection

Phytohormonal changes induced by pathogens differ depend-ing on their trophic strategy. Pathogens with a biotrophicstrategy usually overcome plant defenses and colonize theplant by producing virulence effectors that manipulate thedefense system of the plant, making it susceptible for infec-tion. Resistant plants, however, can recognize the virulenceeffectors of the pathogen, through resistance gene (R-gene)products. This initiates a defense response that arrests thepathogen before it can colonize any further. This often isreferred to as effector triggered immunity (ETI) (Fu andDong 2013; Glazebrook 2005), which is the product of closelyco-evolved species-specific interactions between plant patho-gens and their hosts (Mengiste 2012a; Pieterse et al. 2009). Atthe site of pathogen infection, ETI leads to a localized re-sponse usually related to the production of reactive oxygenspecies (ROS), or an oxidative burst leading to localizedprogrammed cell death, also known as hypersensitive re-sponse (HR) (Baxter et al. 2013; Kerchev et al. 2012;Kliebenstein and Rowe 2008; Overmyer et al. 2003; Torreset al. 2006; van Breusegem and Dat 2006). This process willultimately deprive the pathogen of water and nutrients andprevent its growth (Fu and Dong 2013; Glazebrook 2005).Recent evidence also demonstrates that in the absence of HR,ETI can still arrest the pathogen through other cell-wall-breaking defenses (Johansson et al. 2014). Effector triggeredimmunity against biotrophic pathogens commonly triggers thesynthesis of salicylic acid (SA), a phytohormone with a sys-temic effect in distal parts of the plant. This systemic responsecommonly upregulates defenses, or allows them to be trig-gered more quickly (i.e., priming), allowing the whole plant tobecome resistant to pathogen infection; this process is knownas systemic acquired resistance (Pieterse et al. 2012).

With few exceptions, ETI has not been demonstrated inplant responses to necrotrophic pathogens. As necrotrophicpathogens sustain themselves on dead tissue, programmed celldeath associated with ETI would benefit them, and be a poorplant defense (Mengiste 2012b; Oliver and Solomon 2010;Spoel et al. 2007). Necrotrophs can in fact trigger ROS asso-ciated with HR to their benefit. This shows that althoughmanipulation of plant defense is essential for biotrophic andnecrotrophic pathogens, the mechanisms they use are differ-ent. Necrotrophic pathogens actively destroy host tissuethroughout the infection with various toxins and cell-walldegrading enzymes (Laluk and Mengiste 2010; Veroneseet al. 2006). Biotrophs, however, manipulate plant defenses,thus maintaining the living cells required for their develop-ment (Laluk and Mengiste 2010; Mengiste 2012b; Veroneseet al. 2006). Hemibiotrophic pathogens like Pseudomonassyringae or Phytophthora infestans (potato late blight) have

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both a biotrophic and necrotrophic phase. This two-phasetrophic strategy is reflected in their interactions with plantdefenses. In resistant potatoes, the early biotrophic phase ofthe pathogen is recognized by the plant with effector-inducedHR leading to plant resistance. This cuts off resources to thepathogen before it can spread or switch to the necrotrophicphase (Vleeshouwers et al. 2011). In susceptible plants,P. infestans can evade the HR triggered by the plant with itsown effector protein that down-regulates ligases, enzymes thatjoin large cell-wall molecules. With the pathogen’s switch tonecrotrophy, the effector protein accumulation is reduced andHR-related proteins increase, leading to the observed necroticlesions of the necrotrophic phase of P. infestans (Bos et al.2010).

Regardless of the pathogen lifestyle, plant resistance can betriggered by another species-specific route, which does notnecessarily involve gene-for-gene recognition, as with ETI.Plants may recognize the pathogen through molecular signals,known as microbe- or pathogen-associated molecular patterns(MAMPs/PAMPs), leading to pattern-triggered immunity(PTI) (Glazebrook 2005; Lai and Mengiste 2013; Mengiste2012b). These patterns emerge from highly evolutionary con-served areas in the pathogen’s molecular patterns (Huffakeret al. 2013; Laluk and Mengiste 2010). Pattern recognitionactivates specific signaling cascades tightly shaped by plant-pathogen coevolutionary history, which can in some casesalso contribute to systemic acquired resistance (Mishina andZeier 2007).

The Importance of Pathogen Trophic Strategyfor Plant-Mediated Effects on Insect Herbivores

To predict outcomes of plant-mediated interactions betweenpathogens and insect herbivores, it is especially important toconsider the trophic strategy of the pathogen. Since biotrophsand necrotrophs induce plant responses in very different ways(Pieterse et al. 2012; Spoel et al. 2007), their effects on plantswill influence the phytochemical environment the insect at-tacker will encounter. In the case of hemibiotrophs, consider-ing in which trophic phase of the pathogen the interaction istaking place is of importance, since the phase switch also canaffect the plant’s hormonal profile. Conceivably, a susceptibleplant will be sensitive to pathogens manipulating its defensiveresponses. These plants will have an altered defense systemrelative to a resistant plant, and thus certain immunity-relatedhormones and their downstream products may be under-expressed. A resistant plant rather may have a higher concen-tration of immunity-related hormones in its tissues. Sinceplants have limited resources to mount defensive responses,and different hormonal routes may antagonize each other, thiscan have varying effects on insect attackers (Table 1). Plant-mediated indirect effects of pathogens on herbivores also willvary based on the feeding mode of the insect (See Fig. 1). It

previously was believed that phloem feeders were more af-fected by SA-mediated responses (Goggin 2007; Li et al.2006); thus, biotrophic pathogens are likely to negativelyimpact them, whereas the opposite might be expected forchewing insects as the result of the SA-JA pathway antago-nism (Thaler et al. 2012). Recent evidence from studies onplant-aphid (Hogenhout and Bos 2011), and plant-pathogencompatibility (Gururani et al. 2012), suggests that the highlyspecific R-gene mediated resistance may be more relevant inpredicting effects on phloem feeders than phytohormones.

Effects of Pathogens on Chewing Insects

Although little information on the effect of necrotrophic path-ogens on chewing insects is available, it might be expectedthat necrotrophic pathogens like Botrytis cinerea affect insectsat the local level only. This a priori expectation is based on thefact that these pathogens do not commonly cause systemicacquired resistance (Govrin and Levine 2002). This effect wasreported by Rostás and Hilker (2002) who found that thenecrotroph Alternaria brassicae deterred the leaf beetlePhaedon cochleariae at the local level. Athough the mecha-nisms were not fully elucidated, the authors attributed suchlocal effects to toxins released by the fungus. Conversely, wehave found five examples of bio- or hemibiotrophic pathogensthat cause systemic induced susceptibility (SIS) leading tofacilitation of chewing insects (Table 1). For example, thestem-boring weevil Apion onopordi exhibited better survivalon Cirsium arvense plants affected by the biotrophic rustfungus Puccinia punctiformis (Bacher et al. 2002), andPseudomonas syringae infection increased herbivory by thefly Scaptomyza nigrita on bittercress (Humphrey et al. 2014).The finding of SIS to insects after pathogen attack also hasbeen observed in several other biological systems (Rostáset al. 2003), though the biochemical mechanisms were notstudied in all cases (see Table 1 for recent examples andRostás et al. 2003 for an extensive list of examples).

One important model species for testing plant responses topathogenic bacterial attacks is the hemibiotroph P. syringae.Plant defense to this pathogen is mediated mainly by the SA-signaling pathway, although other pathways like JA and eth-ylene also are involved (Fu and Dong 2013; Groen et al. 2013;Moran and Thompson 2001). Early work showed that patho-gen attack mainly induced SA in Arabidopsis thaliana, whichresulted in SIS to chewing insects (Cui et al. 2002). Mutantswith elevated levels of SA were more susceptible to thecabbage looper, Trichoplusia ni after pathogen attack (Cuiet al. 2002). However, plants with higher constitutive levelsof SA and known R-gene mediated resistance showed resis-tance to T. ni after pathogen treatment (Cui et al. 2002, 2005).Furthermore, plants with and without functional genes in-volved in SA-signaling were both more susceptible to herbiv-ory by T. ni after initial infection by P. syringae. This suggests

732 J Chem Ecol (2014) 40:730–741

that the SA pathway is not the only factor mediating SIS to theinsect. In this system, plant responses against the pathogenimportantly are mediated by ethylene signaling. Recent re-search with Arabidopsismutants has revealed that plants withdisrupted ethylene signaling, are more resistant to herbivory(Groen et al. 2013). Interestingly, ethylene also is required inthis system to mediate interactions between chewing insectsand the SA-inducing phloem feeder Bemisia tabaci (Zhanget al. 2013). Since ethylene often acts in concert with JA(Pieterse et al. 2009; Thaler et al. 2012; Xu et al. 1994;Zhang et al. 2013), it is important to take this latter pathwayinto account. Plant hormones interact through complex path-ways, but JA is triggered chiefly in plants attacked bynecrotrophic pathogens, chewing herbivores, and certainphloem feeders. Based on the JA/SA-antagonism (Thaleret al. 2012), Groen et al. (2013) hypothesized that pathogensthat can trigger ETI through bacterial effectors, also caninduce SIS to herbivory. However, these authors found thatwith ETI, the ethylene-signalling pathway is bypassed, whichtriggers a cascade independent of the main JA-SA pathways,cancels SIS, and induces resistance to chewing herbivores. Asimilar situation might apply when plants recognize patho-gens through molecular patterns (PTI). In susceptibleArabidopsis plants, for instance, SA is up-regulated after therelease of bacterial coronatine (COR), which antagonizes theJA response pathway while at the same time up-regulatesethylene biosynthesis (Brooks et al. 2004; Groen et al.2013). This process antagonizes the JA response but via aseparate pathway than through JA-SA crosstalk. In bothcases, JA downregulation increases susceptibility to chewingherbivores. If plants are resistant to the pathogen, however,SA is suppressed, and the pathogen-released COR disruptsethylene signaling, consequently inducing resistance to theherbivore (Groen et al. 2013). These examples are a cleardemonstration that plant defenses are triggered in a multi-layered process. This may reflect a plant’s trade-offs in thecontext of a complex community of attackers.

Effects of Pathogens on Phloem Feeding Insects

Based on five published studies, we did not find any cleareffect of pathogen trophic strategy on subsequent perfor-mance of phloem feeders (Table 1). In three studies withbiotrophic pathogens, inhibition and facilitation of aphidswas demonstrated (Al-Naemi and Hatcher 2013; Johnsonet al. 2003; Lee et al. 2012). These studies used differentpathogens and aphids, hampering generalizations about theeffect of biotrophs on subsequent attack by phloem feeders. Inone of the aforementioned studies, however, biotrophic andnecrotrophic pathogens induced opposing effects on aphiddevelopment, survival, and fecundity (Al-Naemi and Hatcher2013). The biotrophic rust fungus Uromyces viciae-fabaeenhanced the performance of the aphid Aphis fabae, whereasT

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J Chem Ecol (2014) 40:730–741 733

the necrotrophic fungus B. cinerea attenuated it. A decrease ofaphid fecundity after Botrytis infection also has been reportedfor the aphid Rhodobium porosum (Mouttet et al. 2011).These results might seem counterintuitive because biotrophsand aphids usually trigger the SA defense pathway (Goggin2007; Guerrieri and Digilio 2008; Li et al. 2006; Moran andThompson 2001). In a similar way, the necrotroph is expectedto stimulate the JA pathway at the cost of reduced SA expres-sion, which would in turn benefit the aphid- which is oppositeof the finding in the aforementioned paper. In certain cases,the observed aphid fitness did match our a priori expectations.For example, in comparison to uninfested leaves, the aphidEuceraphis betulae grew larger, developed faster, and pre-ferred the leaves of the silver birch Betula pendula previouslyinfested with the pathogenMarssonina betulae (Johnson et al.2003). These contrasting results could be explained by assum-ing a role for other plant defensive mechanisms. This down-plays the relevance of phytohormone-mediated mechanisms,or suggests still unknown intricate interactions among phyto-hormones. The aforementioned results, for instance, wereattributed to an increase in phenolic compounds and freeamino acids in the infected tissues that occurs downstreamof phytohormonal signaling (Johnson et al. 2003). Sinceaphids are known to be sensitive to changes in nitrogen levelsin plants, opposing results also could be explained by a

relative increase of nitrogen level when leaves are infectedwith the biotrophic rust fungus, whereas the opposite mighthappen as a result ofBotrytis infection (Al-Naemi and Hatcher2013). It is clear that different pathogens, which use the sametrophic strategy, have different effects on aphids (Table 1).

Since aphids are able to induce both the JA/ethylene andSA pathways (Thaler et al. 2010, 2012; Thompson andGoggin 2006), responses may be variable, or not solely deter-mined by the crosstalk in these pathways. Furthermore,phytohormonal interactions are not limited to crosstalk be-tween JA and SA. Aphids also are able to induce ethylene(Thaler et al. 2010; Thompson and Goggin 2006) or to ma-nipulate cytokinin levels and, therefore, source-sink nutrientflows in plants, ultimately allowing plant colonization (Gironet al. 2013; Mok and Mok 2001; Sakakibara 2006). Althoughdetailed information is available on how different plant hor-mones interact after pathogen infestation (Spoel et al. 2007),their consequences for the community of insects sharing theplant are still little understood.

Thus far, few studies have investigated sequential plant-fungus (or plant-oomycete)-insect interactions. In many casesinfections by fungi trigger defense mechanisms similar tobacterial pathogens (Jiang and Tyler 2012; Latijnhouwerset al. 2003), yet more examples of sequential tri-partite inter-actions with fungi or oomycetes are needed to better

Fig. 1 Overview of plant-mediated effects of pathogens on insects and ofinsects on pathogens of different trophic strategies or feeding modes;including hypothetical phytohormone-mediated mechanisms. Arrow end-ings represent findings from references discussed in this article, although

mechanisms are not necessarily addressed in each reference. Acronymsshown as follows: SA = Salicylic acid, JA = Jasmonic acid, ET =Ethylene, ETI = Effector triggered immunity

734 J Chem Ecol (2014) 40:730–741

understand the role of plant hormones in mediating indirectinteractions with herbivores. Jasmonic acid-deficient tomatoplants were more susceptible to the oomycete pathogenP. infestans, demonstrated by larger lesions and more spores(Thaler et al. 2004). This suggests that infection thatdownregulates JA (from biotrophy, for example) might alsoinduce susceptibility to chewing insects, whereas JA-inducingfungi might induce resistance. The aforementioned study,however, reported that plants may have variable responses toJA-deficiency, which do not necessarily correspond with ourpredictions based on trophic strategy of the pathogen. Thatbeing established, Thaler et al. (2004) concluded thatbiotrophy and necrotrophy are better viewed as a continuumrather than a dichotomy.

Proposed Hypotheses for Plant-Mediated Effectsof Pathogens on Insect Herbivores

The examples reported reveal that although general predic-tions can be made, the complexity of plant phytohormonalresponses hampers our understanding of how plants mediateinteractions between insects and pathogens with differenttrophic strategies. Based on the recent literature (Table 1),we propose the following hypotheses:

(i) Biotrophic pathogens facilitate chewing herbivores(though SIS) unless plants exhibit effector-triggered im-munity to the pathogen. Biotrophic pathogens can have afacilitating effect on chewing herbivores by upregulatingSA- and downregulating JA-mediated defenses.

(ii) Biotrophic pathogens facilitate or inhibit phloem feeders.The mechanisms are not yet clear but they may bemediated by the plants’ recognition of the pathogen orinsect attackers, in particular whether ETI or PTI istriggered.

(iii) Necrotrophic pathogens can inhibit both phloem feedersand chewers through mechanisms that are not yet clear(Mouttet et al. 2011; Rostás et al. 2003). More evidencefor the plant-mediated effects of necrotrophic pathogenson insects of the two feeding modes is particularlyneeded to formulate a more explicit hypothesis.

Plant-Insect Interactions

Plant Responses to Herbivory

The ETI-paradigm which often is associated with pathogenattack on plants also is becoming relevant to plant-herbivoresystems, especially with regard to piercing-sucking insectslike aphids and whiteflies (Cooper et al. 2004; Erb et al.2012; Hogenhout and Bos 2011). Although still limited to afew model systems, R-genes have been discovered that confer

resistance against particular clones of the Hessian fly (Groveret al. 1989), aphids, whiteflies, psyllids, and nematodes(Hogenhout and Bos 2011). There still is limited informationabout plant responses after R-gene mediated resistance, al-though more is known about how insect feeding mode affectsphytohormone signaling pathways. Several studies have con-cluded that phloem feeders and biotrophic pathogens cantrigger SA-mediated defenses (De Vos et al. 2005; Moranand Thompson 2001; Walling 2000), whereas herbivory bychewers and cell content-feeders are thought chiefly to induceJA (Bari and Jones 2009; De Vos et al. 2005; Howe and Jander2008; Mouttet et al. 2013; Schmelz et al. 2009). Althoughexceptions to these patterns have been found, we now havestrong empirical evidence that hormonal regulation is at leastpartially predicted by insect feeding mode. Specificity of theinsect-plant interaction also is considered a predictive factor,since specialists are expected to be more resistant to defensivephytochemicals of the specific plant taxon they exploit(Hopkins et al. 2009). However, recent reviews of this para-digm have demonstrated that even specialists suffer from highlevels of plant toxins, and that feeding mode has more predic-tive value for which plant defenses are induced (Ali andAgrawal 2012; Bidart-Bouzat and Kliebenstein 2011). Theseresponses, however, are dependent on many other variables,including the plant or insect developmental stage (Goggin2007; Mouttet et al. 2013; Walling 2000). For example, oneday after oviposition by the leafminer fly Liriomyza sativae,JA-inducible genes were upregulated, whereas after hatching,larval feeding induced SA-regulated genes in tomato (Kawazuet al. 2012).

The Importance of Insect Feeding Mode for Plant-MediatedEffects on Pathogens

Based on what we currently know on the effects of insectherbivores using different feeding modes and at certain den-sities, formulating hypotheses on tri-partite interactions be-tween plants, microbial pathogens and insects is difficult,considering the idiosyncrasies of each study system. It isexpected that phloem feeders, through induction of the SApathway, will facilitate colonization by biotrophic pathogens,while inducing resistance against necrotrophs. Thaler et al.(2010) tested this hypothesis in a study of the interactionsamong P. syringae, tomato mosaic virus, caterpillars, andaphids. Caterpillar feeding negatively affected both aphidsand the biotrophic pathogen through JA induction; aphidfeeding triggered both JA and SA induction, which benefittedcaterpillars yet hindered P. syringae infection. The predictionsand hypotheses tested in this study were limited to two path-ogen species, whereas important taxa like fungi andoomycetes were not considered.

We found thirteen examples (from ten different references)investigating effects of prior insect feeding on pathogen

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infection (Table 2). From these, the conclusion that effects onpathogens depend entirely on the insect feeding mode is notwarranted.

Effects of Phloem Feeding Insects on Pathogen Infection

Phloem feeders induce resistance in plants againsthemibiotrophic or biotrophic bacterial and fungal pathogens.For example, feeding by the green peach aphid Myzuspersicae on pepper plants reduced infection by the biotrophicbacterium Xanthomonas axonopodis (Lee et al. 2012). Thiswas attributed to the aphids triggering the SA-mediated path-way in the same way that biotrophic pathogens do. This effectalso was found for another phloem feeder, the silverleafwhitefly, Bemisia argentifolii, which reduced the incidenceof powdery mildew Erysiphe cichoracearum (Mayer et al.2002). Rice was less likely to contract the rice blast diseasePyricularia grisea, if previously exposed to the phloem-feeding white-backed leafhopper Sogatella furcifera (Kannoand Fujita 2003; Kanno et al. 2005). Another rice pathogenshowed a similar trend, as pre-infestation with S. furciferareduced infestation by the rice blast fungus, Magnaporthegrisea (Satoh et al. 2009). This evidence suggests that insectswith phloem feeding habits will upregulate SA and throughcrosstalk downregulate JA-mediated plant defenses, leadingto the inhibition of biotrophic pathogens.

The opposite might be expected in the case of necrotrophicfungi, as shown by Mouttet et al. (2011) who found that pre-infestation with Rhodobium porosum aphids on rose plantsinhibited Botrytis cinerea . In the same study, pre-infestationby cell-content feeding thrips did not reduce the size of lesionscaused by B. cinerea. Although no specific plant metaboliteswere measured, this study suggests that piercing-suckingaphids elicit signaling pathways different from cell content-feeding thrips. While thrips and chewing herbivores inducesimilarly elevated JA levels in Arabidopsis, they differ in theparticular downstream responsive genes they induce (De Voset al. 2005). In the study by De Vos et al. (2005), it wasconcluded that although the phytohormones JA, SA, andethylene were all important for the defense responses ofArabidopsis against biotrophs, necrotrophs, phloem feeders,cell-content feeders, and chewers, each attacker induced aunique phytohormonal signature and consequently a particu-lar set of genes.

Effects of Chewing Insects on Pathogen Infection

Chewing herbivores can either inhibit or facilitate biotrophicor hemibiotrophic pathogens. In only four studies necrotrophinfections were made after insect feeding, and in three ofthese, no effect on the pathogen was found. Having fewexamples available makes it difficult to develop a generalizedhypothesis about the outcome of a necrotrophic infection

following insect feeding. An emerging pattern may be thatcell content feeders or chewers (usually associated with JAinduction) may not have any effect on necrotrophic pathogens,whereas phloem feeders may inhibit them. Phytochemicalmechanisms have not yet been studied, and phytohormonesignaling is addressed in only three out of the thirteenexamples cited.

De Vos et al. (2006) demonstrated that Arabidopsismutants deficient in either JA, SA or ethylene signalingcould still inhibit the growth of the hemibiotrophP. syringae, after previous induction by the chewing her-bivore Pieris rapae. This indicates that caterpillar-inducedresistance to P. syringae does not depend exclusively onany of these phytohormones alone. Interestingly, P. rapaefeeding primes A. thaliana plants for SA-mediated defenseagainst turnip crinkle virus, and ethylene that was inducedby caterpillar feeding acted synergistically on this plantresponse (De Vos et al. 2006). Induction by chewing her-bivores also can systemically increase the growth (surfacearea of sporangia) of the biotrophic rust fungusMelampsora allii-fragilis (Simon and Hilker 2003, 2005).

Proposed Hypotheses for Herbivore Effects on Pathogens

To put forward hypotheses about plant-pathogen-insect inter-actions, more cases are needed in which the effect of differentinsect feeding modes on pathogens is evaluated in concertwith quantification of different phytohormones and the tran-scription of phytohormone-regulated genes. Additionally,more studies on the effects of chewing herbivores on subse-quent interactions with pathogens (particularly fungi) and themechanisms determining the outcomes of these interactionsare needed to provide a stronger basis for proposing testablehypotheses.

Even though few and conflicting findings are published wecan hypothesize that:

(i) Phloem feeding herbivores inhibit pathogen attack by SAinduction; but evidence for negative effects onnecrotrophs is still currently scant.

(ii) Chewing herbivores tend not to affect necrotrophic path-ogens and may either inhibit or facilitate biotrophicpathogens.

Future Perspectives

The molecular revolution has allowed ecologists to get adeeper understanding of the dialog between plants and theirassociated organisms. During the last few decades, this knowl-edge has revealed strategies of plants to fine-tune their re-sponses against different attackers, while balancing growth inthe face of abiotic stressors (Harrison 2012; Jones and Dangl

736 J Chem Ecol (2014) 40:730–741

Tab

le2

Insectfirst.overview

oftheeffectsof

insectsof

differentfeeding

guild

son

pathogensof

differenttrophicstrategies,showingknow

nmechanism

scausingtheseeffects

Firststress:insect

Feedingguild

Second

stress:p

athogen

Trophicstrategy

Plant

Effecto

npathogen

Mechanism

Citatio

n

Scaptomyzanigrita

chew

ing

Pseudom

onas

syringae

hemibiotroph

Cardaminecordifo

liafacilitation

Not

directly

tested

butS

Ainductionim

plied

Hum

phreyetal.2014

Plagioderaversicolora

chew

ing

Melam

psoraallii-fragilis

biotroph

Salix

cuspidata

(ahybrid

ofS.

fragilisandS.

pentandra)

facilitation

(systemically)

?Sim

onandHilk

er2003

Franklin

iella

occidentalis

cellcontentfeeding

Botrytis

cinerea

necrotroph

Rosahybrida

noeffect

?Mouttetetal.2011

Phaedon

cochleariae

chew

ing

Alternaria

brassicae

necrotroph

Brassicarapa

noeffect

?Rostasetal.2003

Pierisrapae

chew

ing

Alternaria

brassicicola

necrotroph

Arabidopsisthaliana

noeffect

Nospecificdependence

onJA

;itw

asinduced,though

noinhibitio

nobserved

DeVos

etal.2006

Pierisrapae

chew

ing

Xanthom

onas

campestris

hemibiotroph

Arabidopsisthaliana

inhibitio

nNospecificdependence

onJA

,SAor

Ethyleneas

deficient

mutantsstill

exhibitedresistance

topathogen

DeVos

etal.2006

Pierisrapae

chew

ing

Pseudom

onas

syringae

hemibiotroph

Arabidopsisthaliana

inhibitio

nNodependence

onJA

,SA

orEthyleneas

deficientm

utantsstill

exhibitedresistance

topathogen

DeVos

etal.2006

Myzus

persicae

phloem

feeding

Xanthom

onas

axonopodis

biotroph

Capsicumannum

inhibitio

nSA

induction,attracted

beneficialbacteria

Bacillus

subtilis

toroots

Lee

etal.2012

Bem

isia

tabaci

phloem

feeding

Xanthom

onas

axonopodis

biotroph

Capsicumannum

inhibitio

nSA

induction,attracted

beneficialbacteriato

roots

Yangetal.2011

Sogatella

furcifera

phloem

feeding

Pylicuralia

grisea

hemibiotroph

Oryza

sativa

inhibitio

n?

Kanno

andFu

jita2003

Sogatella

furcifera

phloem

feeding

Magnaporthe

grisea

hemibiotroph

Oryza

sativa

inhibitio

nPR

-protein

expression,

likelySA

induction

Kanno

etal.2005;

Satoh

etal.2009

Bem

isia

argentifo

liiphloem

feeding

Erysiphecichoracearum

biotroph

Solanum

lycopersicum

inhibitio

n?Possiblyfoliarchitinases,

peroxidase

Mayer

etal.2002

Rhodobium

porosum

phloem

feeding

Botrytis

cinerea

necrotroph

Rosahybrida

inhibitio

n?

Mouttetetal.2011

J Chem Ecol (2014) 40:730–741 737

2006; Pieterse et al. 2009, 2012). We now know that thisdialog is not limited to pairwise interactions between plantswith either insects or pathogens (Biere and Bennett 2013). Abroader approach that takes into account how plants deal withthe whole community of organisms colonizing them willprovide new breakthroughs in our understanding of plant-based ecosystems.

Although many studies have explored plant-mediated inter-actions between insect herbivores and plant pathogens (Biereand Bennett 2013; Pieterse and Dicke 2007; Ponzio et al. 2013;Stout et al. 2006) the mechanisms, and in particular the rolesthat phytohormones play in such indirect interactions are stillpoorly understood. Many studies lack concrete evidence ofinduced pathways, or they attribute the effects tophytohormonal signalling without having directly measuredhormone levels. Knowledge on pairwise interactions can helpmake general predictions, but available evidence suggests thattri-partite interactions are much more complex than we previ-ously thought. The few examples for which phytohormones aremeasured reveal that the general predictions do not alwayshold. The best-studied phytohormones act in concert withothers, and downstream metabolic pathways also are likely tohave a stong impact on the resulting plant phenotype for theinsect or the pathogen of interest. It now has become feasible,thanks to the genomic revolution, to make globaltranscriptomic analyses, which provide insight into plant phys-iological responses to different stresses in non-model plants.

Insect herbivores and plant pathogens have a long evolu-tionary history in common, and coevolutionary forces haveshaped their effects on plant phenotype and morphology. Inthis review, we focussed on how these different attackersintroduced sequentially can interact through the plant, al-though recent evidence shows that insect herbivores and plantpathogens that are found simultaneously on the plant also canestablish intimate mutualistic symbiosis mediated by plantphysiology (Frago et al. 2012). As reviewed by Casteel andHansen (2014), insects can exploit bacteria to elicit plantresponses that will ultimately benefit the insect, and the sameis known for bark beetle-fungi-conifer interactions (Paineet al. 1997). Insects that vector plant pathogens (includingviruses, phytoplasmas and fungi) have established mutualisticsymbioses that modify plant physiology to the benefit of theinsect vector (Casteel and Hansen 2014; Sugio et al. 2011;Zhang et al. 2012; Ziebell et al. 2011). Although there is ampleevidence of herbivores vectoring plant pathogens (Hogenhoutet al. 2008; Paine et al. 1997), this type of interaction has notbeen discussed in detail in this review, as we focused onsequential infestations. Insect vectors, however, also may beinfluenced by prior infection of plants by pathogens they cantransmit. For example, in the wild gourd (Cucurbita pepo ssp.texana), previous infection by the zucchini yellow mosaicvirus induced high levels of SA, which slowed down thespread of the beetle-vectored bacterial wilt Erwinia

tracheiphila (Shapiro et al. 2013). Although this may beselected through a mutualistic interaction between the vectorand the bacterium, it also reveals the intricate interactionsbetween hormones underlying interactions among plant-associated community members. How plant pathogens havecolonized insects and evolved with them into mutualisticsymbionts is an intriguing question that will spark futurestudies. Insect herbivores are attacked by a diverse communityof natural enemies; after herbivore attack, for example, plantscan emit volatiles that attract natural enemies of the insect (i.e.,indirect defenses) (Turlings et al. 1995; Vet and Dicke 1992).However, how plant pathogens modulate these interactions isstill poorly understood (Ponzio et al. 2013, 2014).Understanding how plants can modulate the balance in theirsecondary metabolite-based responses against pathogens andinsect herbivores, and between direct and indirect defensesagainst herbivores will surely provide a new view on howefficient plant responses operate in multitrophic systems.Ultimately, such studies will require data from field studiesto take into account not only different trophic levels, but alsohighly diverse communities.

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