J Chem Ecol (2014) 40:657–675 DOI 10.1007/s10886-014-0468-3

REVIEW ARTICLE

Jasmonate-Triggered Plant Immunity

Marcelo L. Campos & Jin-Ho Kang & Gregg A. Howe

Received: 22 April 2014 /Revised: 6 June 2014 /Accepted: 17 June 2014 /Published online: 28 June 2014 # Springer Science+Business Media New York 2014

Abstract The plant hormone jasmonate (JA) exerts direct strategy is highlighted by its capacity to shape natural popu- control over the production of chemical defense compounds lations of plant attackers, as well as the propensity of plant- that confer resistance to a remarkable spectrum of plant- associated organisms to subvert or otherwise manipulate JA associated organisms, ranging from microbial pathogens to signaling. As both a cellular hub for integrating informational vertebrate herbivores. The underlying mechanism of JA- cues from the environment and a common target of pathogen triggered immunity (JATI) can be conceptualized as a multi- effectors, the core JA module provides a focal point for stage signal transduction cascade involving: i) pattern recog- understanding immune system networks and the evolution nition receptors (PRRs) that couple the perception of danger of chemical diversity in the plant kingdom. signals to rapid synthesis of bioactive JA; ii) an evolutionarily conserved JA signaling module that links fluctuating JA levels Keywords Plant immunity . Hormone signaling . Effector . to changes in the abundance of transcriptional repressor pro- Jasmonate . Alternative splicing . Plant-herbivore teins; and iii) activation (de-repression) of transcription factors interactions . Plant-pathogen interactions . Salicylic acid that orchestrate the expression of myriad chemical and mor- phological defense traits. Multiple negative feedback loops act in concert to restrain the duration and amplitude of defense responses, presumably to mitigate potential fitness costs of Introduction JATI. The convergence of diverse plant- and non-plant- derived signals on the core JA module indicates that JATI is Plants are a source of nutrition for a vast biota in terrestrial a general response to perceived danger. However, the modular environments. Selective pressure imposed by pathogens and structure of JATI may accommodate attacker-specific defense herbivores has shaped the evolution of an astonishing array of responses through evolutionary innovation of PRRs (inputs) specialized plant defense compounds that exert direct toxic, and defense traits (outputs). The efficacy of JATI as a defense anti-nutritional, or repellant effects on plant consumers. Other defensive compounds work indirectly by attracting natural : : enemies of plant-associated organisms. Strategies to deploy M. L. Campos J.

Intensive research efforts to understand the molecular A second major question surrounding induced immunity mechanisms and evolutionary ecology of induced immunity concerns the extent to which cellular recognition of a given have focused on the question of how plants recognize foreign threat is translated into a host response that specifically neu- threats. Significant insight has come from molecular genetic tralizes the attacking pathogen or herbivore. Indeed, genome- analyses of plant-pathogen interactions. Pattern-triggered im- wide transcriptome studies indicate a significant degree of munity (PTI) confers basal resistance and is mediated by cell overlap in molecular responses triggered by different surface-localized pattern recognition receptors (PRRs) that MAMPs/HAMPs/DAMPs and effectors (Bidart-Bouzat and bind conserved foreign molecules, known collectively as Kliebenstein 2011; Caillaud et al. 2013; Gouhier-Darimont microbial/pathogen-associated molecular patterns (MAMPs) et al. 2013; Kim et al. 2014; Navarro et al. 2004;Reymond (Chisholm et al. 2006;DoddsandRathjen2010; Jones and et al. 2004; Tao et al. 2003; Thilmony et al. 2006; Tsuda et al. Dangl 2006). A second layer of induced resistance, referred to 2008, 2009;Wiseetal.2007;Zhurovetal.2014). There also as effector-triggered immunity (ETI), relies on polymorphic is evidence to indicate that PTI and ETI converge on similar intracellular resistance (R) proteins to detect effector mole- downstream signaling components, including MAP kinase cules that plant attackers deliver into host cells to counteract pathways, ROS production, and calcium-dependent signaling defense. ETI responses often include localized host cell death events (Romeis and Herde 2014;Satoetal.2010). Although and are qualitatively similar, though typically more robust, quantitative differences in the timing and strength of induction than PTI responses (Dodds and Rathjen 2010). Major concep- are likely to shape the outcome of specific plant-attacker tual contributions of the PTI/ETI paradigm include the dis- associations (De Vos et al. 2005; Katagiri and Tsuda 2010; tinction between plant defense responses triggered by con- Tao et al. 2003;Wiseetal.2007), most evidence indicates that served patterns versus effectors, and a theory to explain how specific danger signals trigger general host defense responses these forms of immunity drive the evolution of plant-pathogen that are effective against broad classes of pathogens and associations (Jones and Dangl 2006). The PTI/ETI model also herbivores (Erb et al. 2012). has influenced current views on how plants recognize attack The central role of small-molecule hormones in controlling by arthropod herbivores, which constitute the majority of the expression of chemical and morphological defense traits plant-consuming species on Earth (Erb et al. 2012;Howe provides an impetus for describing induced immunity from and Jander 2008). Accordingly, eliciting compounds pro- the perspective of phytohormone networks (Erb et al. 2012; duced by plant-eating animals have been dubbed herbivore- Pieterse et al. 2009; Reymond and Farmer 1998). It now is associated molecular patterns (HAMPs) (Felton and evident that diverse danger signals converge on the immune- Tumlinson 2008; Mithöfer and Boland 2008). promoting effects of two major defense hormones, jasmonic In addition to cell surveillance systems that recognize acid (JA) and salicylic acid (SA). Here, we focus on recent foreign threats in the form of MAMPs/HAMPs and effectors, advances in understanding JA-triggered immunity (JATI). We it has long been known that plant-derived (i.e., self) signals describe JATI as a multistage process in which a highly also are potent elicitors of local and systemic defense re- conserved core JA module links a variety of PRR-based sponses (Bergey et al. 1996; Green and Ryan 1972; Heil recognition systems (inputs) to the expression of specific et al. 2012; Huffaker et al. 2006, 2011; Krol et al. 2010; defense traits (outputs). Based on these considerations, we Mousavi et al. 2013). These endogenous elicitors are pro- propose that the regulatory structure of JATI has potential to duced in response to general cellular injury and may be create new specificities of host resistance through evolution- classified as damage-associated molecular patterns ary innovation of input and output modules. We also highlight (DAMPs). Because DAMPs are generated in response to the various ways in which plant-associated organisms manip- diverse types of tissue injury, their role in cellular recognition ulate JATI to their own advantage. These new mechanistic of pathogen attack traditionally has been ignored. However, insights will help to explain how JATI shapes patterns of the recent identification of DAMP receptors and associated chemical diversity and species interaction in the plant king- signal transduction components (Brutus et al. 2010;Choietal. dom, and how these relationships affect genome evolution to 2014; Mousavi et al. 2013; Yamaguchi et al. 2006, 2010)is modulate phenotypic plasticity. Our focus on JA is not shaping a broader view of how plant cells perceive and re- intended to minimize the role of other signals in coordinating spond to injurious threats (Boller and Felix 2009;; De Lorenzo plant defense responses, or to distract from the important et al. 2011;Heil2009; Koo and Howe 2009). The diversity of challenge of understanding the complexities of phytohormone conserved patterns that trigger local and systemic defense networks and their relationship to induced immunity (Ballaré reactions supports the concept that cellular perception of 2014; Kazan and Manners 2012; Kim et al. 2014;Mukhtar “danger”, regardless of its source, is a unifying principle of et al. 2011; Pieterse et al. 2009). Nevertheless, we subscribe to induced immunity in plants and animals (Boller and Felix the view that an accurate, and ultimately predictive, under- 2009; Koo and Howe 2009; Lotze et al. 2007; Matzinger standing of interconnected signaling networks depends on 2002). knowledge of how individual signals are produced and J Chem Ecol (2014) 40:657–675 659 perceived at the molecular level. Readers are referred to nutrients from living host tissues succumb to the effects of several excellent review articles for a comprehensive discus- SA-triggered immunity (SATI) (Caillaud et al. 2013; sion of JA-mediated signal transduction, its interaction with Glazebrook 2005; Pieterse et al. 2009). There is every indica- other signaling pathways, and the function of JA in develop- tion that JA promotes resistance of monocot and gymnosperm mental processes (Ballaré 2011;Browse2009;Huotetal. species to a wide range of pathogens and herbivores (Hudgins 2014 Kazan and Manners 2008, 2012;Kombrink2012; et al. 2004; Schmelz et al. 2014; Yan et al. 2012;Yeetal. Meldau et al. 2012; Pauwels and Goossens 2011; Robert- 2012; Zulak and Bohlmann 2010). In contrast to the biotroph/ Seilaniantz et al. 2011; Wasternack and Hause 2013). necrotroph dichotomy that has emerged from studies with Arabidopsis, it is noteworthy that JA is required for induced immunity of rice to (hemi)biotrophic parasites, including the JATI Confers Broad-spectrum Resistance in Dicots root knot nematode (Meloidogyne graminicola)and and Monocots Xanthomonas oryzae (De Vleesschauwer et al. 2013; Nahar et al. 2011). This conclusion is consistent with the ability of JA The central role of JA as an activating signal for induced to elicit expression of many PR genes and defensive second- immunity is grounded in three general observations. First, ary metabolites in rice and maize (Mitsuhara et al. 2008; biotic attack and other forms of tissue injury result in the rapid Schmelz et al. 2011, 2014; Yamane 2013). Given these find- synthesis of JA and its receptor-active derivative, jasmonoyl- ings, together with the high endogenous levels of free SA in L-isoleucine (JA-Ile). Stress-induced accumulation of JA-Ile rice leaves (Silverman et al. 1995), the precise role of SA as a occurs in both above- and below-ground tissues and, depend- signal for induced immunity in monocots awaits further clar- ing on the eliciting signal and tissue type, is a systemic ification (De Vleesschauwer et al. 2013; Schmelz et al. 2014). response (Chauvin et al. 2013; Fragoso et al. 2014;Grebner The serendipitous discovery that JA mutants maintained in et al. 2013; Koo et al. 2009; Mousavi et al. 2013;Schilmiller artificial growth environments often succumb to attack by and Howe 2005). Second, JA promotes the expression of unsuspected pathogens and herbivores vividly demonstrates virtually all major classes of secondary metabolites and pro- the robust protection afforded by JATI (Browse and Howe teins that have established roles in defense, including alka- 2008). Elegant field studies have employed natural and syn- loids, terpenoids, phenylpropanoids, amino acid derivatives, thetic genetic variation to demonstrate this phenomenon in anti-nutritional proteins, and some pathogenesis-related (PR) natural habitats, and have established the ecological impor- proteins (Browse and Howe 2008;DeGeyteretal.2012;De tance of JATI in shaping herbivore community composition Vleesschauwer et al. 2013; Farmer and Ryan 1990;Gonzales- (Kallenbach et al. 2012; Kessler et al. 2004;Thaleretal.2001; Vigil et al. 2011; Mohan et al. 2006; Van Loon et al. 2006). Züst et al. 2012). We employed this unbiased “ask the plant” The JA pathway also promotes the development of morpho- genetic approach to query the biological role of JA in medi- logical structures, including glandular trichomes, resin ducts, ating interaction of cultivated tomato (S. lycopersicum)with and nectaries that produce a rich variety of compounds serving potential biotic attackers in the field. Previous studies at this direct and indirect roles in defense (Dicke and Baldwin 2010; field site showed that glandular trichomes, whose develop- Hudgins et al. 2004;Lietal.2004; Peiffer et al. 2009;Qietal. ment on tomato leaves is controlled in part by the JA pathway 2011; Radhika et al. 2010; Traw and Bergelson 2003;Van (Boughton et al. 2005;Lietal.2004; Peiffer et al. 2009), Poecke and Dicke 2002; Yoshida et al. 2009). Finally, studies provide an important layer of anti-insect defense (Kang et al. employing JA mutants have demonstrated the crucial role of 2010a, 2010b, 2014). Replicated field trials showed that a this hormone in plant protection against diverse biota (Browse tomato mutant (jai1) lacking the JA-Ile receptor suffered and Howe 2008). Among the plant-associated organisms 100 % mortality from root rot disease caused by the oomycete whose fitness is curtailed by JATI are necrotrophic and pathogen Pythium (Fig. 1). Similar results have been reported (hemi)biotrophic pathogens, mutualistic fungi, nematodes, for JA mutants of Arabidopsis and maize (Staswick et al. leafhoppers, beetles, caterpillars, aphids, thrips, spider mites, 1998; Vijayan et al. 1998; Yan et al. 2012). These collective fungus gnats, slugs, crustaceans, and some vertebrate herbi- studies demonstrate the efficacy of JATI in protecting highly vores (Table 1). Indeed, it is reasonable to think that the diverse plants against the same soil-borne pathogen. number of plant-eating species affected by JATI may exceed the total number of plant species on Earth. Much of our knowledge about the protective effects of Core JA Signaling Module JATI comes from studies on a limited number of dicot plants, including Arabidopsis, tomato, and tobacco. These studies The signal transduction events that couple perception of dan- have led to the generalization that tissue-consuming insect ger signals at the cell surface to the expression of JA- herbivores and necrotrophic pathogens are particularly sensi- responsive defense genes relies on an evolutionarily con- tive to JATI, whereas biotrophic organisms that obtain served core apparatus to synthesize and perceive JA-Ile 660 J Chem Ecol (2014) 40:657–675

Table 1 Examples in which there is genetic evidence for JA-medi- Organism Host plant Reference ated plant resistance to pathogens and herbivores Pathogenic bacteria Erwinia carotovora Arabidopsis thaliana (Brassicaceae) Norman-Setterblad et al. 2000 Xanthomonas oryzae Oryza sativa (Poaceae) Yamada et al. 2012 Necrotrophic fungi/oomycetes Alternaria brassicicola A. thaliana (Brassicaceae) Thomma et al. 1998 Botrytis cinerea A. thaliana (Brassicaceae) Thomma et al. 1998 Pythium spp A. thaliana (Brassicaceae) Vijayan et al. 1998; Staswick et al. 1998; Zea mays (Poaceae) Yan et al. 2012 Solanum lycopersicum (Solanaceae) This study Nematodes Meloidogyne graminicola O. sativa (Poaceae) Nahar et al. 2011 Mollusks Arion lusitanicus A. thaliana (Brassicaceae) Falk et al. 2014 Crustaceans Porcellio scaber A. thaliana (Brassicaceae) Farmer and Dubugnon 2009 Armadillidium vulgare O. sativa (Poaceae) Cell content feeders Tetranychus urticae (Acari) S. lycopersicum (Solanaceae) Li et al. 2004 Frankliniella occidentalis A. thaliana (Brassicaceae) Zhurov et al. 2014 (Thysanoptera) S. lycopersicum (Solanaceae) Li et al. 2002 A. thaliana (Brassicaceae) Abe et al. 2009 Piercing-sucking insects Myzus persicae (Hemiptera) A. thaliana (Brassicaceae) Ellis et al. 2002 Empoasca sp. (Hemiptera) Nicotiana attenuata (Solanaceae) Kessler et al. 2004 Leafminer insects Scaptomyza flava (Diptera) A. thaliana (Brassicaceae) Whiteman et al. 2011 Leaf/root chewing insects Manduca sexta (Lepidoptera) N. attenuata (Solanaceae) Howe et al. 1996; Kessler et al. 2004; Spodoptera frugiperda (Lepidoptera) S. lycopersicum (Solanaceae) Campos et al. 2009 Bradysia impatiens (Diptera) A. thaliana (Brassicaceae) McConn et al. 1997 Spodoptera exigua (Lepidoptera) Z. mays (Poaceae) Yan et al. 2012 Vertebrate herbivores Eurotestudo boettgeri A. thaliana (Brassicaceae) Mafli et al. 2012

(Fig. 2)(Chicoetal.2008;Katsiretal.2008a). A crucial subsequent reduction and β-oxidation steps that give rise to feature of JA-Ile as an endogenous trigger of immune re- JA (Howe and Schilmiller 2002; Schaller and Stintzi 2009; sponses is its rapid and reversible accumulation in vegetative Wasternack and Hause 2013). JA is conjugated to Ile in the tissues that are frequently targeted for attack. Unstressed cytosol to produce JA-Ile (Kang et al. 2006; Staswick and leaves of Arabidopsis, for example, contain extremely low Tiryaki 2004). As the receptor-active form of the hormone or undetectable amounts of bioactive JA (Glauser et al. 2008; (Fonseca et al. 2009;Katsiretal.2008b; Sheard et al. 2010; Koo and Howe 2009). JA synthesis is initiated in plastids from Staswick 2008; Thines et al. 2007), JA-Ile presumably dif- the pre-existing C18 precursor linolenic acid (LA). LA is fuses into the nucleus where it is perceived by its receptor. converted to a cyclic 12-oxo-phytodienoic acid (OPDA) in- Many genes required for JA-Ile biosynthesis are coordinately termediate, which is then transported to the peroxisome for upregulated by the JA signaling pathway (Browse 2009;Koo J Chem Ecol (2014) 40:657–675 661

A C

B D

Fig. 1 Jasmonate perception by the COI1 receptor system is essential for transcribed spacer region in infected tomato tissue confirmed the presence resistance of cultivated tomato to the oomycete pathogen Pythium. Wild- of Pythium ultimum. Of several hundred wild-type (Jai1/Jai1)plants type (cv Castlemart) and jai1 mutant plants grown for three weeks in a grown side-by-side at the same field site, none showed symptoms of growth chamber without visible signs of disease were transplanted to a the disease. The figure shows photographs of representative wild-type (a field plot at Michigan State University, East Lansing, MI. Two weeks and b)andjai1 mutant (c and d) plants two weeks after transplantation. after transplanting, all jai1 plants (N=30) died from a disease that was Identical results were obtained in three independent trails performed at the diagnosed as Pythium stem/root rot by the MSU Diagnostics Lab. Se- same site quencing of PCR products derived from 5.8S ribosomal gene and internal et al. 2006; Wasternack and Hause 2013). Although this independently of NINJA (Shyu et al. 2012). A rapidly observation suggests a positive feedback loop to amplify JA expanding list of JAZ- and MYC2-interacting regulatory pro- responses, the existence of JA-inducible negative feedback teins that participate in other hormone-response pathways loops (see below) highlights the complexity of processes indicates that the JAZ-TF interactome is a cellular hub for involved in JA-Ile homeostasis. integrating diverse environmental and developmental signals JA-Ile controls defense gene expression by promoting the (Ballaré 2014; Hou et al. 2010;Huetal.2013a; Kazan and destruction of JAZ (JAsmonate ZIM domain) transcriptional Manners 2013;Nakataetal.2013; Pauwels et al. 2010;Qi repressors via the ubiquitin–26Sproteasomesystem(Chini et al. 2011, 2014;Songetal.2011, 2014;Todaetal.2013; et al. 2007;Thinesetal.2007; Yan et al. 2007). JAZ proteins Yang et al. 2012b; Zhu et al. 2011). are defined by two highly conserved sequence motifs referred In response to perception of signals that trigger JA-Ile to as ZIM (or TIFY) and Jas (Browse 2009; Chung et al. 2009; synthesis, JA-Ile promotes direct binding of JAZ repressors Yan et al. 2007). In the absence of stress, low levels of JA-Ile to the F-box protein COI1 (CORONATINE INSENSITIVE1), permit JAZ proteins to bind and repress transcription factors which is the specificity determinant of the E3 ubiquitin ligase (TFs) in the nucleus. The basic helix-loop-helix TF MYC2 SCFCOI1 (Katsir et al. 2008b; Melotto et al. 2008; Sheard et al. and its closely related paralogs (MYC3 and MYC4) are the 2010; Thines et al. 2007; Xie et al. 1998). Ubiquitin- most extensively studied JAZ-interacting TFs having a direct dependent degradation of JAZ proteins relieves repression of role in JATI (Fernández-Calvo et al. 2011; Kazan and TFs, thereby allowing expression of JA-response genes Manners 2013; Schweizer et al. 2013). Nuclear localization (Fig. 2). The amplitude and duration of JA responses appear of some JAZ repressors is dependent on physical association to be controlled primarily by the intracellular level of JA-Ile with MYC2 (Withers et al. 2012). Within the nucleus, the (Koo et al. 2009;Staswick2008). Moreover, the speed with repressive activity of some JAZ requires the NINJA (Novel which danger signals are transmitted to gene activation via the Interactor of JAZ) protein to mediate interaction with core- core pathway may be remarkably fast. Crush-type wounds pressors such as TOPLESS (TPL) (Acosta et al. 2013; inflicted to Arabidopsis leaves, for example, result in in- Pauwels et al. 2010). NINJA contains an EAR (ERF- creased JA-Ile levels within minutes of tissue damage, with associated amphiphilic repression) motif that binds TPL and increased accumulation of primary JA-response transcripts TPL-related corepressors (Pauwels et al. 2010; Szemenyei observed within 5 min of wounding (Chauvin et al. 2013; et al. 2008). Other JAZ proteins (e.g., JAZ8) contain an Chung et al. 2008). Mechanical tissue damage also triggers EAR motif, thereby allowing direct recruitment of TPL rapid systemic responses, including JA-Ile accumulation, 662 J Chem Ecol (2014) 40:657–675

Danger perception Damaged cell Physical signals MAMPs HAMPs Pathogen DAMPs effectors

?

2+ Cytosol Ca Calcium MAPK ROS Sensors ?

JAMs JA TFs response Defense LA Plastid genes stable JAZs OPDA JAZ

COI1 OPDA Nucleus Peroxisome ω-oxidation 12COOH-JA-Ile β-ox JA JA JA-Ile hydrolysis JA

Core JA module Signal attenuation

Fig. 2 Model of jasmonate-triggered plant immunity (JATI). Danger and morphological defense traits (Defense). Several mechanisms to at- signals (MAMPs/HAMPs) derived from attacking organisms and dam- tenuate signaling through the core module have been elucidated, includ- aged plant cells (DAMPs) are recognized by pattern recognition receptors ing catabolism of JA-Ile via ω-oxidation and hydrolysis, de novo syn- (PRRs) at the cell surface. PRR activation is coupled to intracellular thesis of JAZ repressors that are stable in the presence of JA-Ile, and signaling systems involving MAP kinase pathways, calcium ion-sensing accumulation of JAM TFs that negatively regulate transcription. Patho- proteins, and reactive oxygen species (ROS), among others. How these gen-derived effectors target the core JA signal module to disrupt hormon- signaling events are connected to activation of the core JA signal module, al balance and induced immune responses. Abbreviations: Microbe-as- which includes JA biosynthesis from its precursor linolenic acid (LA), is sociated molecular patterns (MAMPs); Herbivore-associated molecular largely unknown (?). Plastidic and peroxisomal enzymes convert LA to patterns (HAMPs); Damage-associated molecular patterns (DAMPs), Mi- jasmonic acid (JA), which is the substrate for synthesis of JA-Ile in the togen-activated protein kinase (MAPK); 12-oxo-phytodienoic acid cytosol. Within the nucleus, JA-Ile promotes JAZ-COI1 interaction and (OPDA), β-oxidation (β-ox), jasmonoyl-L-isoleucine (JA-Ile), targets JAZs for proteolytic degradation by the ubiquitin-proteasome JASMONATE-ZIM domain (JAZ), JA-related transcription factor (TF), system. Removal of JAZ alleviates TFs from repression, thereby activat- JASMONATE-ASSOCIATED MYC2-LIKE (JAM), 12-carboxy-JA-Ile ing the expression of JA-responsive genes and the expression of chemical (12COOH-JA-Ile) degradation of JAZ proteins, activation of JA-response genes, flagellin, elongation factor-Tu (EF-Tu), and chitin, for which and induced resistance (Acosta et al. 2013; Green and Ryan the cognate PRRs have been identified, indicate that these 1972; Koo et al. 2009; Mousavi et al. 2013; Zhang and Turner conserved bacterial and fungal patterns activate multiple 2008). branches of induced immunity, including JATI (Kim et al. 2014). Several HAMPs, including fatty acid-amino acid con- jugates (FACs), also amplify JA responses via unknown Activation of the Core JA Module mechanisms (McCloud and Baldwin 1997; Schmelz et al. 2003, 2007). Elicitation of JA-mediated defense responses MAMPs, HAMPs, and DAMPs Available evidence indicates by DAMPs, including the 18-amino-acid peptide systemin that JA/JA-Ile synthesis is controlled at the post- and cell wall-derived oligogalacturonides (OGs), is consistent transcriptional level via activation of pre-existing JA biosyn- with the ability of these compounds to stimulate endogenous thetic enzymes (Wasternack and Hause 2013). Although the JA synthesis (Doares et al. 1995;LeeandHowe2003). precise mechanism of activation remains to be determined, a Likewise, endogenous peptide elicitors from Arabidopsis wide range of endogenous (DAMP) and foreign (AtPep1) and maize (ZmPep3) exert potent stimulatory effects (MAMP/HAMP) signals have been implicated in the process on JATI (Table 2) (Huffaker et al. 2006, 2013). Identification (Fig. 2; Table 2). Analysis of phytohormone production and of plant receptors for OGs and AtPep1 marks a major advance defense gene expression in response to elicitors such as in efforts to understand the contribution of DAMPs to plant J Chem Ecol (2014) 40:657–675 663

Table 2 Select examples of danger signals and effectors that modulate JA-mediated plant defense responses

Signal Mechanism of perception/action References

DAMPs AtPep1 LRR-RK receptors PEPR1 and PEPR2. Activates JA- and Huffaker et al. 2006; SA-dependent innate immune responses. Yamaguchi et al. 2006 Systemin Unknown receptor (presumed LRR-RK). Elicits JA synthesis Pearce et al. 1991 and production of defense compounds. ZmPep3 Unknown receptor. Activates JA synthesis and production of Huffaker et al. 2013 defense compounds. Oligogalacturonides WAK1 receptor. Activates JA synthesis and production Doares et al. 1995 of defense compounds. Brutus et al. 2010 Extracellular ATP DORN1 receptor. Activates transcriptional responses that are Choi et al. 2014 similar to wound responses. MAMPs/HAMPs Flagellin (bacterial pathogens) LRR-RK receptor FLS2. Activates the JA and other Chinchilla et al. 2006; branches of induced immunity. Kim et al. 2014 Elongation factor-Tu (bacterial pathogens) LRR-RK receptor EFR. Activates the JA and other Zipfel et al. 2006; sectors of induced immunity. Kim et al. 2014 Chitin (fungal pathogens) LysM-RK receptor CERK1. Predominately activates the JA Wan et al. 2008; sector of induced immunity. Kim et al. 2014 Volictin and other fatty acid-amino acid Unknown receptor. Released from insect oral secretions to Alborn et al. 1997; conjugates (Lepidopteran herbivores) stimulate JATI. Halitschke et al. 2001 Inceptin (Lepidopteran herbivores) Unknown receptor. Activates JA accumulation and associated Schmelz et al. 2007 defense responses. Physical signals Electrical potentials (Herbivory/wounding) Wound-induced electrical signals are propagated by Mousavi et al. 2013 glutamate-like receptors to activate JA biosynthesis. Microbial effectors Coronatine (Pseudomonas syringae) JA-Ile analog that promotes formation of COI1-JAZ co-receptor Katsir et al. 2008b; complexes and JAZ degradation. Sheard et al. 2010 HopZ1a (Pseudomonas syringae) Putative acetytransferase that promotes COI1-dependent Jiang et al. 2013 JAZ degradation. HopX1 (Pseudomonas syringae) A cysteine protease that promotes COI1-independent JAZ Gimenez-Ibanez et al. 2014 degradation. MiSSP7 (Laccaria bicolor) An effector from a mutualistic fungus that binds to and protects Plett et al. 2014b JAZ6 from JA/COI1-induced degradation. HaRxL44 (Downy mildew) Promotes degradation of Mediator subunit 19a to activate JA Caillaud et al. 2013 responses and suppress SATI.

immunity (De Lorenzo et al., 2011;Kroletal., JATI concerns the molecular events that link perception 2010;Yamaguchi et al., 2006). Equally exciting is the recent ofMAMP/HAMP/DAMPsbyPRRstoaccumulationof discovery of the receptor for extracellular ATP, which exhibits JA-Ile (Fig. 2). Among the intracellular signals impli- properties of a danger signal released by damaged cells (Choi cated in this process are calcium ions, reactive oxygen et al. 2014;Songetal.2006). species (ROS), and mitogen-activated protein (MAP) kinase cascades. Ca2+ signaling, ROS and MAPKs It generally is accepted that Calcium ions have long been recognized as ubiquitous JA synthesis is initiated in the plastid by stress-induced acti- second messengers in signal transduction pathways. The in- vation of lipases that release fatty acid precursors of JA volvement of Ca2+ in JATI is supported by studies showing (Bergey et al. 1996;Hyunetal.2008;Wasternackand that cytosolic Ca2+ levels increase in response to herbivore Hause 2013). Alternatively, there is evidence to suggest that feeding and treatment with exogenous MAMP/HAMP/ tissue damage may stimulate JA synthesis from an existing DAMPs (Arimura and Maffei 2010; Jeter et al. 2004; Maffei pool of OPDA (Koo et al. 2009). Regardless of the precise et al. 2004, 2006). Changes in membrane polarization caused mechanism involved, a major gap in our understanding of by wounding and insect attack also increase the level of 664 J Chem Ecol (2014) 40:657–675 cytosolic Ca2+ (Maffei et al. 2006). Ca2+ fluxes and associated (Mousavi et al. 2013; Salvador-Recatalà et al. 2014). The Ca2+-binding proteins, including calmodulin and Ca2+-depen- ability of mechanical leaf wounding and insect chewing to dent protein kinases (CDPKs), exert control during the acti- elicit comparable changes in electrical activity indicates that vation of JA-response genes (Bonaventure et al. 2007; insect-derived factors are not required for this response. Boudsocq et al. 2010;Levyetal.2005; Romeis and Herde Current evidence thus indicates that insect feeding generates 2014;Yangetal.2012a). Dynamic changes in cytosolic Ca2+ long-distance electrical signals through the action of GLRs, levels during plant-attacker interactions are linked to the pro- and that decoding of this signal in systemic responding leaves duction of ROS, including hydrogen peroxide (Arimura and results in JA-Ile synthesis, JA-Ile perception via the COI1- Maffei 2010). Alterations in cellular redox status are associ- JAZ co-receptor system, and activation of defense gene ex- ated with local and systemic JATI, and are associated with the pression. The JATI-eliciting electrical signal thus has all the activity of the respiratory burst oxidase homolog D (RBOHD) hallmarks of a DAMP (Fig. 2). The mechanism by which the (Miller et al. 2009; Orozco-Cárdenas et al. 2001). Direct propagating signal is perceived and subsequently linked to JA phosphorylation of RBOHD by the PRR-associated kinase biosynthesis remains to be determined. However, there is BIK1 provides a mechanism to integrate MAMP perception evidence to suggest that calcium ions may be involved in with calcium-based regulation of immune function (Kadota propagating and/or interpreting the signal in responding target et al. 2014;Lietal.2014). cells (Felle and Zimmermann 2007;Maffeietal.2006;Qi MAP kinase signaling cascades serve a prominent role in et al. 2006) and a role for RBOHD-dependent ROS produc- the early steps of induced immunity (Asai et al. 2002; tion was excluded (Mousavi et al. 2013). Schweighofer et al. 2007; Seo et al. 2007; Wu and Baldwin 2010; Zhang and Klessig 2001). Plants silenced in the expres- sion of specific MAPKs showed reduced JA biosynthesis and decreased expression of JA-related defense genes, suggesting Negative Regulation of JATI that these kinases control an early step in the activation of JA synthesis (Kandoth et al. 2007;Wuetal.2007). The manner in Although JATI confers effective resistance to a broad spec- which MAPK cascades are linked to a specific step in the JA trum of pathogens and herbivores, hyperactivation of the biosynthesis pathway, however, remains unknown. pathway can negatively affect plant growth and fitness. Many specialized defense compounds, for example, are toxic Long-distance electrical signals and glutamate-like recep- to the plant that produces them (Baldwin and Callahan 1993; tors - One of the most fascinating and least understood as- Gog et al. 2005). In addition, increased allocation of limited pects of JATI concerns the mechanism by which mechanical metabolic resources to defense compounds may reduce the tissue injury, including that elicited by chewing herbivores, extent to which these resources can be used to fuel plant results in rapid systemic induction of JA biosynthesis and growth and reproduction (Agrawal 1999;Baldwin1998; defense gene expression (Koo and Howe 2009). Studies in Herms and Mattson 1992; Yan et al. 2007; Zhang and Arabidopsis, for example, show that a signal generated at the Turner 2008). JATI may, therefore, provide a cost-saving site of leaf injury travels rapidly (2–3 cm/min) to trigger JA-Ile strategy to coordinate the timing of chemical defense produc- synthesis and associated JA responses in undamaged leaves tion with perceived threats from the environment. Until re- (Glauser et al. 2008; Koo et al. 2009). Despite the importance cently, relatively little attention has been paid to understanding and wide-spread occurrence of this phenomenon, the mechanisms that restrain defense signaling pathways or de- molecular and genetic basis of rapid systemic JATI signaling sensitize plant cells to the presence of eliciting signals. As has been uncertain. A recent study by Mousavi et al. (2013) described below, molecular studies have elucidated several built on previous work showing that leaf damage causes JA-induced negative feedback loops within the core JA sig- changes in electrical activity and membrane depolarization naling module. in undamaged systemic leaves (Mousavi et al. 2013;Wildon et al. 1992; Zimmermann et al. 2009). A screen for mutants Catabolism of JA-Ile The dependence of JATI on intracellular that exhibit reduced wound-triggered changes in electric po- accumulation of JA-Ile suggests that turnover of the hormone tential showed that members of the GLUTAMATE could provide a mechanism to attenuate JA responses. Initial RECEPTOR-LIKE (GLR) family of ion channel proteins are support for this hypothesis came from studies showing that required for the response; glr3.3 and glr3.6 mutants are defi- various oxidized and conjugated derivatives of JA-Ile accu- cient in electrical activity in wounded leaves and show re- mulate in wounded leaves (Glauser et al. 2008; Miersch et al. duced expression of JA-responsive genes in distal undamaged 2008; Paschold et al. 2008). Recent studies have employed leaves (Mousavi et al. 2013). Systemic depolarization events genetic approaches to elucidate two metabolic routes for JA- were triggered in a GLR3.3/GLR3.6-dependent manner by Ile catabolism, referred to as the JA-Ile ω-oxidation and caterpillar feeding but not by caterpillar walking on the leaf hydrolysis pathways (Fig. 2) (Koo and Howe 2012). The latter J Chem Ecol (2014) 40:657–675 665

pathway is catalyzed by aminohydrolases that cleave JA-Ile to (t1/2<2 min) in the presence of JA-Ile (Chini et al. JA and Ile (Bhosale et al. 2013;Widemannetal.2013; 2007;Grunewaldetal.2009; Pauwels et al. 2010; Woldemariam et al. 2012). This reaction is readily reversible Thines et al. 2007), recent studies have advanced the by the JA-conjugating enzyme JAR1 (Staswick and Tiryaki concept that other JAZs exhibit a wide range of stabil- 2004), suggesting that the relative level of conjugating and ity, which could allow fine-tuning of TF activity in aminohydrolase activity is an important factor in the control of response to fluctuating JA-Ile levels (Chung and Howe JA-Ile homeostasis. In contrast to JA-Ile hydrolysis, the ω- 2009; Chung et al. 2009, 2010;Shyuetal.2012). oxidation pathway provides a mechanism for permanent in- The conserved Jas motif of JAZ proteins contains a degra- activation of JA-Ile. This pathway involves at least two mem- dation signal (degron) that binds COI1 in a JA-Ile-dependent bers (CYP94B3 and CYP94C1) of the CYP94 family of manner (Katsir et al. 2008b; Melotto et al. 2008;Sheardetal. cytochromes P450 that oxidize the ω-carbon of JA-Ile to 2010; Yan et al. 2007). Point mutations within the degron produce 12OH-JA-Ile, which is further oxidized to disrupt JAZ-COI1 interaction without affecting JAZ binding 12COOH-JA-Ile (Heitz et al. 2012; Kitaoka et al. 2011;Koo to TFs, thereby stabilizing and enhancing the activity of the et al. 2011). 12OH-JA-Ile is less active than JA-Ile in promot- repressor (Melotto et al. 2008;Withersetal.2012). ing COI1 binding to JAZ proteins (Koo et al. 2011). The fact Natural sequence variation within degron also affects that 12OH-JA-Ile retains some activity in COI1-JAZ interac- JAZ stability and associated physiological outputs of tion assays, however, suggests that CYP94-mediated oxida- JATI (Shyu et al. 2012). JAZ8, for example, contains tion of 12OH-JA-Ile to 12COOH-JA-Ile, or conjugation of a non-canonical degron that evidently does not interact 12OH-JA-Ile to other small molecules (Gidda et al. 2003; with COI1 in the presence of JA-Ile. As a consequence, Kitaoka et al. 2014), is required for complete inactivation of JAZ8 maintains the ability to interact with target TFs JA-Ile. and repress transcription through recruitment of a co- Consistent with a role in negative feedback regulation of repressor complex. Stress-induced expression of JAZ8 JATI, genes encoding enzymes in both the ω-oxidation and may thus provide a mechanism to desensitize cells to hydrolysis pathways are rapidly induced in response to thepresenceofJA-Ile(Shyuetal.2012). wounding, herbivory, and JA treatment (Bhosale et al. 2013; JAZ repressors also are stabilized by alternative splicing Heitz et al. 2012; Kitaoka et al. 2011; Koo et al. 2011; (AS) events that remove or modify the Jas motif and its Widemann et al. 2013; Woldemariam et al. 2012). associated degron. AS of JAZ10 pre-mRNA produces several Remarkably, Bhosale et al. (2013) found that the IIL6 gene splice variants that differentially interact with COI1 in the encoding a JA-Ile aminohydrolase in Arabidopsis is co- presence of JA-Ile. These isoforms of JAZ10 exhibit a range expressed with other JA-response genes in plants grown under of stability in JA-stimulated cells and, when overexpressed in tightly controlled growth conditions in which stress treatments planta, attenuate JA signal outputs to varying degrees (Chung were not intentionally imposed. This finding highlights the and Howe 2009; Chung et al. 2010;Morenoetal.2013). A exquisite sensitivity of JA-associated surveillance and re- direct role for JAZ10 AS in negative feedback control of JA sponse systems, and suggests a broader role for JA signaling signaling is supported by the JA-hypersensitive phenotype of in modulating phenotypic plasticity in response to subtle jaz10 null mutants, as well as the ability of specific JAZ10 changes in the environment. It can be anticipated that future splice variants to complement the hypersensitive phenotype of research will uncover mechanisms by which JA responses are jaz10 mutants (Cerrudo et al. 2012; Demianski et al. 2012; integrated with various environmental perturbations, includ- Moreno et al. 2013; Yan et al. 2007). The AS event responsi- ing changes in light, water status, nutrient availability, soil ble for generating the stable JAZ10.3 isoform involves reten- microbe communities, and wind/touch (e.g., Chehab et al. tion of an intron whose location within the Jas motif results in 2012). truncation of the C-terminal end of the motif. Interestingly, this intron is present in most JAZ genes from diverse land Stable JAZ proteins Among the 12 JAZ genes in Arabidopsis, plants, suggesting that this conserved AS event provides a most are rapidly and strongly expressed in response to exog- general mechanism to desensitize cells to high JA-Ile levels enous JA or stress-induced accumulation of endogenous JA (Chung et al. 2010). It remains to be determined how stable (Chini et al. 2007; Chung et al. 2008;Thinesetal.2007;Yan JAZ repressors are removed from cells in order to reset full et al. 2007). This pattern of expression suggests that de novo sensitivity of the JA response. synthesis of JAZ proteins is part of a negative feedback system to desensitize cells to the presence of the hormone. Such a Transcriptional JAMming A third mechanism to negatively mechanism of feedback control, however, presumably de- regulate JA responses involves a phylogenetic clade of bHLH- pends on JAZ proteins that are relatively resistant to JA-Ile- type proteins (JAM1/bHLH017, JAM2/bHLH013, induced destruction. Whereas initial studies demonstrated that JAM3/bHLH003) that is closely related to the positively some JAZ members (e.g., JAZ1) are rapidly degraded acting MYC2 TF and its functional paralogs, MYC3, and 666 J Chem Ecol (2014) 40:657–675

MYC4 (Fonseca et al. 2014; Nakata et al. 2013; Sasaki- from studies showing that many plant-associated organisms Sekimoto et al. 2013;Songetal.2013). JAM proteins com- use effector-based strategies to create JA-SA imbalances that pete with MYC2 for binding to cis-acting G-box elements suppress one or the other branches of immunity (Table 2). within the promoters of JA-responsive genes. However, be- An important emerging paradigm in plant-herbivore inter- cause they lack the conserved activation domain found in actions is the ability of herbivores to activate the SA pathway MYC2/3/4, JAMs function as transcriptional repressors rather and thereby reduce the effectiveness of JATI as a basal defense than activators. JAM TFs also interact directly with JAZ (Hogenhout and Bos 2011; Walling 2008). For example, proteins, which may serve to increase the strength of tran- phloem feeding by silverleaf whitefly (Bemisia tabaci)results scriptional repression through recruitment of the co-repressors in increased expression of SA-related defense genes and con- NINJA and TOPLESS (Fonseca et al. 2014;Songetal.2013). comitant repression of JATI (Zarate et al. 2007; Zhang et al. Similar to other negative feedback loops, the expression of 2013). Similarly, insect egg-associated effectors trigger SA JAM1 is strongly upregulated by JA treatment and associated accumulation and JATI suppression in host tissues surround- stress responses (Fonseca et al. 2014; Nakata et al. 2013; ing the egg, thus favoring the survival of newly hatched larvae Sasaki-Sekimoto et al. 2013;Songetal.2013). (Bruessow et al. 2010; Reymond 2013). Secretion of SA into the locomotion mucus (slime trail) by some molluskan herbi- Other modes of negative regulation The multiple negative vores (Kästner et al. 2014), or excretion of SA into honeydew feedback loops described above likely act in concert to restrain by some aphid species (Schwartzberg and Tumlinson 2013), the amplitude and duration of JATI after the response is may reflect additional mechanisms to suppress JATI. The initiated. It should be noted, however, that the onset of JATI Coleopteran herbivore Leptinotarsa decemlineata (Colorado can be actively suppressed by other signals when the benefit potato beetle) employs an alternative but no less effective of growth outweighs the cost of defense. A compelling exam- strategy to hijack JATI; symbiotic bacteria in the oral secretion ple is repression of JATI during the shade avoidance response of the beetle activate SA-dependent responses and repress in which changes in light quality, as perceived by the photo- local and systemic JATI (Chung et al. 2013). That this phe- receptor phytochrome B, modulates the stability of MYC TFs nomenon also occurs in a root-feeding insect herbivore and JAZs to prioritize elongation growth over defense (Ballaré (Diabrotica virgifera, western corn rootworm) of maize sug- 2014; Cerrudo et al. 2012; Chico et al. 2014; Izaguirre et al. gests that host defense suppression by symbiotic bacteria may 2013;Morenoetal.2009). Recent studies have also provided be a general feeding strategy adopted by insect herbivores insight into the mechanisms by which JATI is suppressed by (Barr et al. 2010). the growth-related hormones gibberellic acid (Hou et al. 2010; Studies of the Arabidopsis-Pseudomonas syringae strain Yang et al. 2012b) and ethylene (Kim et al. 2014;Songetal. DC3000 (Pst DC3000) pathosystem have provided consider- 2014), as well as other negative regulators whose mode of able insight into how bacterial pathogens manipulate JATI- action is just beginning to be understood (Hu et al. 2013b). SATI antagonism to their own advantage. In this system, immunity to Pst DC3000 is mediated in large part by SATI. Interestingly, Pst DC3000 uses multiple effectors to activate JA responses through targeted destruction of JAZ proteins, Manipulation of JATI by Plant-associated Organisms which in turn suppresses SATI (Fig. 2). One well-studied effector is the polyketide coronatine (COR) that acts as a The efficacy of any given immune response is often reflected potent agonist of the COI1-JAZ co-receptor system (Bender by the extent to which host-associated pathogens and parasites et al. 1993;Katsiretal.2008b; Sheard et al. 2010). COR- evolved to evade that response. Consistent with its role in re- induced degradation of JAZ repressors strongly upregulates directing primary and secondary metabolism, perhaps it is not the expression of JA-responsive defense genes and surprising that plant pathogens and herbivores evolved strat- downregulates growth-related genes, and impairs multiple egies to manipulate (activate or suppress) JATI. Current views aspects of SATI (Attaran et al. 2014; Brooks et al. 2005; on this topic are influenced by the notion that JATI and SATI Melotto et al. 2006; Uppalapati et al. 2007;Zhaoetal.2003; are often mutually antagonistic (Caillaud et al. 2013;Kunkel Zheng et al. 2012). Suppression of SATI by COR is mediated and Brooks, 2002; Robert-Seilaniantz et al. 2011; Thaler et al. in part by NAC-type TFs that concomitantly repress the 2012). Studies performed with Arabidopsis, for example, expression of the key SA biosynthetic enzyme ICS1 and have led to the generalization that increased activity of the activate expression of a methyltransferase (BSMT1) that con- JA sector of immunity enhances the virulence of biotrophic verts SA to volatile MeSA (Attaran et al. 2009, 2014;Zheng pathogens that are sensitive to SATI, whereas expression of et al. 2012). That release of MeSA is observed in several other SATI favors the performance of insect herbivores and plant-enemy interactions (Dempsey et al. 2011)suggeststhat necrotropic pathogens that are more sensitive to JATI. Some disposal of SA through volatilization may be a general mech- of the strongest evidence for JATI-SATI antagonism comes anism to antagonize SATI by stresses that trigger JA signaling. J Chem Ecol (2014) 40:657–675 667

Pseudomonas syringae strains produce at least two type III With the exception of a few model plants, remarkably little secreted protein effectors that also promote degradation of is known about the identity of JA-regulated compounds that JAZ proteins to increase pathogenicity. HopZ1a is a putative provide resistance against specific attackers. It is currently acetyltransferase that modifies JAZ proteins to stimulate their unclear, for example, whether JA/COI1-mediated resistance degradation in a COI1-dependent manner (Jiang et al. 2013). of Arabidopsis, tomato, and maize to soil-borne Pythium HopX1 is a cysteine protease that destroys JAZs independent- (Table 1) involves similar or divergent defense chemistries. ly of COI1 (Gimenez-Ibanez et al. 2014). Interestingly, Major differences in specialized defense compounds between HopX1 is produced by a strain of P. syringae that does not these species, however, suggests that each plant may use the synthesize COR, indicating that distinct mechanisms to acti- core JA module to deploy different suites of chemical defense vate JA signaling through proteolytic destruction of JAZs against the same pathogen. Similarly, there is evidence that have arisen independently in the evolution of this pathogen tomato and Arabidopsis use highly distinct JA-regulated de- (Gimenez-Ibanez et al. 2014). These findings are consistent fense chemistries for protection against the generalist herbi- with results of large-scale protein-protein interaction screens vores Tetranychus urticae (two-spotted spider mite) and showing that JAZs are targets of effectors from both Trichoplusia ni (cabbage looper) (Herde and Howe 2014;Li P. syringae and the obligate biotrophic oomycete et al. 2002,2004; Zhurov et al. 2014). The modular architec- Hyaloperonospora arabidopsidis (Mukhtar et al. 2011). In ture of JATI thus appears to support the evolution, in different contrast to other biotrophic organisms, colonization of host host plants, of independent chemical solutions to the same tissues by some mutualistic ectomycorrhizal fungi is inhibited pathogen or herbivore, which may contribute to the diversity by JATI (Plett et al. 2014a). A recent study showed that the and sporadic distribution of secondary metabolites in higher ectomycorrhizal fungus Laccaria bicolor produces an effector plants (Fraenkel 1959). On the other hand, there are several (MiSSP7) that binds to and stabilizes a host JAZ protein to examples of similar defense compounds that evolved inde- repress JA responses that presumably inhibit establishment of pendently in diverse plant families (Berenbaum and Zangerl the symbiosis (Plett et al. 2014b). These collective studies 2008). Modern omics-based technologies offer tremendous highlight the COI1-JAZ co-receptor system as a central hub potential to better understand the evolution of constitutive of plant immunity and portend the discovery of additional and induced defense compounds by elucidating gene- effectors that target the core JA module. pathway-metabolite relationships in diverse groups of plants (Berenbaum and Zangerl 2008;Kliebenstein2012). Insight into the evolutionary forces that drive the diversity of chem- ical defenses also will benefit from a better understanding of Synthesis and Future Perspectives how these defense systems are matched by equally complex counter-defenses in plant attackers (Herde and Howe 2014). Recent research on many fronts has tremendously advanced It is becoming increasingly evident that the JA/COI1/JAZ/ our understanding of the mechanism of JA signaling and its TF module is a convergence point for direct crosstalk with relationship to induced plant immunity. These efforts have other signaling pathways that control growth and develop- coalesced around a simple model (Fig. 2) to explain how ment (Ballaré 2014; Erb et al. 2012;Huotetal.2014). It fluctuating levels of a small-molecule hormone (JA-Ile) exert appears that this crosstalk occurs primarily through direct transcriptional control over complex morphological and interaction between nuclear factors that regulate transcription, chemical defense traits. We suggest that the modular structure including the Mediator complex (Caillaud et al. 2013; Çevik of JATI allows the conserved core JA module to link different et al. 2012;Kiddetal.2011). Future research aimed at combinations of PRR-based recognition systems (inputs) and understanding changes in chromatin structure, epigenetic defense traits (outputs) to create new specificities of host modification, and cis-regulatory codes (Zou et al. 2011)that resistance. Indeed, there is good evidence that JATI is a direct TF-DNA interactions is expected to provide new insight significant driving force in shaping plant-animal associations into how transcriptional networks control complex JATI out- in natural environments (Kallenbach et al. 2012;Züstetal. puts, including transgenerational immunity (Rasmann et al. 2012). This conceptual framework provides a foundation for 2012). Various negative feedback loops act in concert to studies aimed at understanding the underlying mechanisms by restrain JATI outputs, but whether these control mechanisms which recognition-response systems give rise to phenotypic constitute an adaptive response to balance tradeoffs between plasticity, and for revealing how interactions between ge- JATI and growth, or perhaps other forms of immunity, re- nomes and environments have spawned highly diverse, idio- mains to be determined. Knowledge of how proteins in dif- syncratic defense traits in the plant kingdom. Meeting this ferent signaling pathways functionally interact to regulate challenge will require integrative approaches spanning the growth-defense antagonism has potential practical application ecosystem-to-gene continuum, as applied to experimental in the development of crop varieties that are both high yielding systems that offer both genomic and ecological resources. and stress tolerant. These efforts may be aided by 668 J Chem Ecol (2014) 40:657–675 mathematical models to predict how environmental inputs are technological tools available, exciting new discoveries may integrated within phytohormone networks to generate specific be just around the corner. physiological outcomes (Middleton et al. 2012). A significant gap in our understanding of JATI is how Acknowledgments We thank Marlene Cameron for assistance with recognition of danger signals at the cell surface activates JA figure graphics and the MSU Diagnostic Lab for diagnosis of Pythium- biosynthesis. By analogy to stress-responsive regulation of mediated root rot disease on jai1 tomato plants. This work was supported ethylene biosynthesis (Liu and Zhang 2004), identification in part by the National Institutes of Health (grant no. GM57795), the of direct targets of the relevant MAPK cascades may provide Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, Office of Science, US Department of Energy important clues. Attention also should be given to the hypoth- (grant no. DE–FG02–91ER20021), and a College of Natural Science esis that JA biosynthesis is controlled by calcium-dependent Dissertation Continuation Fellowship to M.C. signaling events that are coupled to PRR activation (Romeis and Herde 2014). Further analyses of how GLRs generate and/or propagate long-distance electrical signals that trigger systemic JA-Ile synthesis will undoubtedly yield important References new insights as well. A systems-level view of JA-Ile homeo- stasis, including pathways by which JA derivatives are Abe H, Shimoda T, Ohnishi J, Kugimiya S, Narusaka M, Seo S, Narusaka transported within and between cells, is ultimately needed to Y, Tsuda S, Kobayashi M (2009) Jasmonate-dependent plant de- understand how specific TFs are controlled by thresholds and fenses restricts thrips performance and preference. BMC Plant Biol 9:97 time-dependent signatures of the hormone. Finally, it should Abuqamar S, Chai MF, Luo H, Song F, Mengiste T (2008) Tomato be noted that although there is molecular evidence that plant protein kinase 1b mediates signaling of plant responses to resistance to insect herbivores is mediated by PRRs necrotrophic fungi and insect herbivory. Plant Cell 20:1964–1983 (Abuqamar et al. 2008;Princeetal.2014; Truitt et al. 2004; Acosta IF, Gasperini D, Chételat A, Stolz S, Santuari L, Farmer EE (2013) Role of NINJA in root jasmonate signaling. Proc Natl Yang et al. 2011), HAMP receptors remain to be identified in Acad Sci U S A 110:15473–15478 any plant. Agrawal AA (1999) Induced responses to herbivory in wild radish: One of the most exciting recent advances in the field of effects on several herbivores and plant fitness. Ecology 80:1713– induced plant immunity is evidence that the core JA module is 1723 Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, a common target of effectors from multiple plant-associated Tumlinson JH (1997) An elicitor of plant volatiles from beet army- microbes (Table 2). This finding is consistent with the idea worm oral secretion. Science 276:945–949 that different pathogens independently evolved virulence fac- Arimura GI, Maffei ME (2010) Calcium and secondary CPK signaling in tors that converge on common host targets within the PTI plants in response to herbivore attack. Biochem Bioph ResCommun 400:455–460 network (Jones and Dangl 2006; Mukhtar et al. 2011). Only Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez- time will tell whether the current list of COI1/JAZ-targeting GomezL,BollerT,AusubelFM,SheenJ(2002)MAP effectors is complete or, more likely, will continue to expand kinase signalling cascade in Arabidopsis innate immunity. as effector repertoires from diverse plant-associated microbes, Nature 415:977–983 Attaran E, Zeier TE, Griebel T, Zeier J (2009) Methyl salicylate produc- arthropods, and nematodes are systematically scrutinized tion and jasmonate signaling are not essential for systemic acquired (Boller and He 2009; Elzinga and Jander 2013; Hogenhout resistance in Arabidopsis. Plant Cell 21:954–971 and Bos 2011; Kandoth and Mitchum 2013). The strong Attaran E, Major IT, Cruz JA, Rosa BA, Koo AJ, Chen J, Kramer DM, He selection pressure imposed by JATI on arthropod herbivores SY, Howe GA (2014) Temporal dynamics of growth and photosyn- thesis suppression in response to jasmonate signaling. Plant and pathogens, together with evidence that many of these Physiol., in press. organisms actively suppress JA-based defenses, suggests the Baldwin IT (1998) Jasmonate-induced responses are costly but benefit existence of novel mechanisms by which plant-associated plants under attack in native populations. Proc Natl Acad Sci U S A organisms disrupt JATI. Interdisciplinary approaches aimed 95:8113–8118 at understanding how the JA module promotes broad- Baldwin IT, Callahan P (1993) Autotoxicity and chemical defense: nic- otine accumulation and carbon gain in solanaceous plants. spectrum immunity through the control of specialized metab- Oecologia 94:534–541 olism, and how this branch of immunity is subverted by plant Ballaré CL (2011) Jasmonate-induced defenses: a tale of intelligence, attackers, offers tremendous potential to help solve pressing collaborators and rascals. Trends Plant Sci 16:249–257 problems facing the world (Plant Science Research Summit Ballaré CL (2014) Light regulation of plant defense. Annu Rev Plant Biol 65:15.21–15.29 2013). From a biotechnological perspective, for example, Barr KL, Hearne LB, Briesacher S, Clark TL, Davis GE (2010) Microbial these efforts may inform synthetic approaches to harness symbionts in insects influence down-regulation of defense genes in specialized biochemical pathways for metabolic engineering maize. PLoS One 5:e11339 of new chemistries for a variety of plant-based products, Bender CL, Liyanage H, Palmer D, Ulrich M, Young S, Mitchell R (1993) Characterization of the genes controlling the biosynthesis including pigments, fragrances, flavors, pesticides, and phar- of the polyketide phytotoxin coronatine including conjugation be- maceuticals. Given the current pace of discovery and tween coronafacic and coronamic acid. Gene 133:31–38 J Chem Ecol (2014) 40:657–675 669

Berenbaum MR, Zangerl AR (2008) Facing the future of plant-insect Arabidopsis thaliana leaves: a role for lipoxygenase 6 in responses to interaction research: le retour à la “raison d’être”. Plant Physiol 146: long-distance wound signals. New Phytol 197:566–575 804–811 Chehab EW, Yao C, Henderson Z, Kim S, Braam J (2012) Arabidopsis Bergey DR, Howe GA, Ryan CA (1996) Polypeptide signaling for plant touch-induced morphogenesis is jasmonate mediated and protects defensive genes exhibits analogies to defense signaling in animals. against pests. Curr Biol 22:701–706 Proc Natl Acad Sci U S A 93:12053–12058 Chico JM, Chini A, Fonseca S, Solano R (2008) JAZ repressors Bhosale R, Jewell JB, Hollunder J, Koo AJK, Vuylsteke M, Michoel T, set the rhythm in jasmonate signaling. Curr Opin Plant Biol Hilson P, Goossens A, Howe GA, Browse J, Maere S (2013) 11:486–494 Predicting gene function from uncontrolled expression variation Chico JM, Fernández-Barbero G, Chini A, Fernández-Calvo P, Díez-Díaz among individual wild-type Arabidopsis plants. Plant Cell 25: M, Solano R (2014) Repression of jasmonate-dependent defenses 2865–2877 by shade involves differential regulation of protein stability of MYC Bidart-Bouzat MG, Kliebenstein D (2011) An ecological genomic ap- transcription factors and their JAZ repressors in Arabidopsis. Plant proach challenging the paradigm of differential plant responses to Cell, in press. specialist versus generalist insect. Oecologia 167:677–689 Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G (2006) The Boller T, Felix G (2009) A renaissance of elicitors: Perception of Arabidopsis receptor kinase FLS2 binds flg22 and determines the microbe-associated molecular patterns and danger signals by specificity of flagellin perception. Plant Cell 18:465–476 pattern-recognition receptors. Annu Rev Plant Biol 60:379–406 Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garcia- Boller T, He SY (2009) Innate immunity in plants: an arms race between Casado G, Lopez-Vidriero I, Lozano FM, Ponce MR, Micol JL, pattern recognition receptors in plants and effectors in microbial Solano R (2007) The JAZ family of repressors is the missing link in pathogens. Science 324:742–744 jasmonate signalling. Nature 448:666–673 Bonaventure G, Gfeller A, Proebsting WM, Hörtensteiner S, Chételat A, Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe Martinoia E, Farmer EE (2007) A gain-of-function allele of TPC1 interactions: shaping the evolution of the plant immune response. activates oxylipin biogenesis after leaf wounding in Arabidopsis. Cell 124:803–814 Plant J 49:889–898 Choi J, Tanaka K, Cao Y, Qi Y, Qiu J, Liang Y, Lee SY, Stacey G (2014) Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L, He P, Bush Identification of a plant receptor for extracellular ATP. Science 343: J, Cheng SH, Sheen J (2010) Differential innate immune signalling 290–294 via Ca2+ sensor protein kinases. Nature 464:418–422 Chung HS, Howe GA (2009) A critical role for the TIFY motif in Boughton AJ, Hoover K, Felton GW (2005) Methyl jasmonate applica- repression of jasmonate signaling by a stabilized splice variant of tion induces increased density of glandular trichomes on tomato, the JASMONATE ZIM-domain protein JAZ10 in Arabidopsis. Lycopersicon esculentum. J Chem Ecol 31:2211–2216 Plant Cell 21:131–145 Brooks DM, Bender CL, Kunkel BN (2005) The Pseudomonas syringae Chung HS, Koo AJK, Gao X, Jayanty S, Thines B, Jones AD, Howe GA phytotoxin coronatine promotes virulence by overcoming salicylic (2008) Regulation and function of Arabidopsis JASMONATE ZIM- acid-dependent defences in Arabidopsis thaliana. Mol Plant Pathol domain genes in response to wounding and herbivory. Plant Physiol 6:629–639 146:952–964 Browse J (2009) Jasmonate passes muster: a receptor and targets for the Chung HS, Niu Y, Browse J, Howe GA (2009) Top hits in contemporary defense hormone. Annu Rev Plant Biol 60:183–205 JAZ: An update on jasmonate signaling. Phytochemistry 70:1547– Browse J, Howe GA (2008) New weapons and a rapid response against 1559 insect attack. Plant Physiol 146:832–838 Chung HS, Cooke TF, Depew CL, Patel LC, Ogawa N, Kobayashi Y, Bruessow F, Gouhier-Darimont C, Buchala A, Métraux J-P, Reymond P Howe GA (2010) Alternative splicing expands the repertoire of (2010) Insect eggs suppress plant defence against chewing herbi- dominant JAZ repressors of jasmonate signaling. Plant J 63:613– vores. Plant J 62:876–885 622 Brutus A, Sicilia F, Macone A, Cervone F, Lorenzo G (2010) A domain Chung SH, Rosa C, Scully ED, Peiffer M, Tooker JF, Hoover K, Luthe swap approach reveals a role of the plant wall-associated kinase 1 DS, Felton GW (2013) Herbivore exploits orally secreted bacteria to (WAK1) as a receptor of oligogalacturonides. Proc Natl Acad Sci U suppress plant defenses. Proc Natl Acad Sci U S A 110:15728– S A 107:9452–9457 15733 Caillaud MC, Asai S, Rallapalli G, Piquerez S, Fabro G, Jones JDG De Geyter N, Gholami A, Goormachtig S, Goossens A (2012) (2013) A downy mildew effector attenuates salicylic acid-triggered Transcriptional machineries in jasmonate-elicited plant secondary immunity in Arabidopsis by interacting with the host mediator metabolism. Trends Plant Sci 17:349–359 complex. PLoS Biol 11:e1001732 De Lorenzo G, Brutus A, Savatin DV, Sicilia F, Cervone F (2011) Campos ML, de Almeida M, Rossi ML, Martinelli AP, Litholdo Junior Engineering plant resistance by constructing chimeric receptors that CG, Figueira A, Rampelotti-Ferreira FT, Vendramim JD, Benedito recognize damage-associated molecular patterns (DAMPs). Febs VA, Peres LEP (2009) Brassinosteroids interact negatively with Lett 585:1521–1528 jasmonates in the formation of anti-herbivory traits in tomato. J De Vleesschauwer D, Gheysen G, Höfte M (2013) Hormone defense Exp Bot 60:4347–4361 networking in rice: tales from a different world. Trends Plant Sci 18: Cerrudo I, Keller MM, Cargnel MD, Demkura PV, de Wit M, Patitucci 555–565 MS, Pierik R, Pieterse CMJ, Ballaré CL (2012) Low red/far-red De Vos M, Van Oosten VR, Van Poecke RMP, Van Pelt JA, Pozo MJ, ratios reduce Arabidopsis resistance to Botrytis cinerea and Mueller MJ, Buchala AJ, Métraux J-P, Van Loon LC, Dicke M, jasmonate responses via a COI1-JAZ10-dependent, salicylic acid- Pieterse CMJ (2005) Signal signature and transcriptome changes of independent mechanism. Plant Physiol 158:2042–2052 Arabidopsis during pathogen and insect attack. Mol Plant Microbe Çevik V, Kidd BN, Zhang P, Hill C, Kiddle S, Denby KJ, Holub EB, Inter 18:923–937 Cahill DM, Manners JM, Schenk PM, Bynon J, Kazan K (2012) Demianski AJ, Chung KW, Kunkel BN (2012) Analysis of Arabidopsis MEDIATOR25 acts as an integrative hub for the regulation of JAZ gene expression during Pseudomonas syringae pathogenesis. jasmonate-responsive gene expression in Arabidopsis. Plant Mol Plant Pathol 13:46–57 Physiol 160:541–555 Dempsey DA, Vlot AC, Wildermuth MC, Klessig DF (2011) Salicylic Chauvin A, Caldelari D, Wolfender JL, Farmer EE (2013) Four 13- acid biosynthesis and metabolism. The Arabidopsis book 9:e0156. lipoxygenases contribute to rapid jasmonate synthesis in wounded doi:10.1199/tab.0156 670 J Chem Ecol (2014) 40:657–675

Dicke M, Baldwin IT (2010) The evolutionary context for herbivore- synthesis and accumulation in Arabidopsis in response to wounding. induced plant volatiles: beyond the ‘cry for help.’. Trends Plant Sci J Biol Chem 283:16400–16407 15:167–175 Glazebrook J (2005) Contrasting mechanisms of defense against Doares SH, Syrovets T, Weiler EW, Ryan CA (1995) Oligogalacturonides biotrophic and necrotrophic pathogens. Annu Rev Phytopath 43: and chitosan activate plant defensive genes through the 205–227 octadecanoid pathway. Proc Natl Acad Sci U S A 92:4095–4098 Gog L, DeLucia EH, Berenbaum MR, Zangerl AR (2005) Autotoxic Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view effect of essential oils on photosynthesis in parsley, parsnip, and of plant-pathogen interactions. Nat Rev Genet 11:539–548 rough lemon. Chemoecology 15:115–119 Ellis C, Karafyllidis I, Turner JG (2002) Constitutive activation of Gonzales-Vigil E, Bianchetti CM, Phillips GN, Howe GA (2011) jasmonate signaling in an Arabidopsis mutant correlates with en- Adaptive evolution of threonine deaminase in plant defense against hanced resistance to Erysiphe cichoracearum, Pseudomonas insect herbivores. Proc Natl Acad Sci U S A 108:5897–5902 syringae,andMyzus persicae. Mol Plant Microbe Inter 15:1025– Gouhier-Darimont C, Schmiesing A, Bonnet C, Lassueur S, Reymond P 1030 (2013) Signalling of Arabidopsis thaliana response to Pieris Elzinga DA, Jander G (2013) The role of protein effectors in plant-aphid brassicae eggs shares similarities with PAMP-triggered immunity. interactions. Curr Opin Plant Biol 16:451–456 J Exp Bot 64:665–674 Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect- Grebner W, Stingl NE, Oenel A, Mueller MJ, Berger S (2013) specific plant reactions. Trends Plant Sci 17:250–259 Lipoxygensae6-dependent oxylipin synthesis in roots is required Falk KL, Kästner J, Bodenhausen N, Schramm K, Paetz C, Vassão DG, for abiotic and biotic stress resistance in Arabidopsis. Plant Reichelt M, von Knorre D, Bergelson J, Erb M, Gershenzon J, Physiol 161:2159–2170 Meldau S (2014) The role of glucosinolates and the jasmonic acid Green TR, Ryan CA (1972) Wound-induced proteinase inhibitor in plant pathway in resistance of Arabidopsis thaliana against molluskan leaves: A possible defense mechanism against insects. Science 175: herbivores. Mol Ecol 5:1188–1205 776–777 Farmer EE, Dubugnon L (2009) Detritivorous crustaceans become her- Grunewald W, Vanholme B, Pauwels L, Plovie E, Inze D, Gheysen G, bivores on jasmonate-deficient plants. Proc Natl Acad Sci U S A Goossens A (2009) Expression of the Arabidopsis jasmonate sig- 106:935–940 naling repressor JAZ1/TIFY10A is stimulated by auxin. EMBO Rep Farmer EE, Ryan CA (1990) Interplant communication: airborne methyl 10:923–928 jasmonate induces synthesis of proteinase inhibitors in plant leaves. Halitschke R, Schittko U, Pohnert G, Boland W, Baldwin IT (2001) Proc Natl Acad Sci U S A 87:7713–7716 Molecular interactions between the specialist herbivore Manduca Felle HH, Zimmermann MR (2007) Systemic signalling in barley sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana through action potentials. Planta 226:203–214 attenuata. III. Fatty acid-amino acid conjugates in herbivore oral Felton GW, Tumlinson (2008) Plant-insect dialogs: complex interactions secretions are necessary and sufficient for herbivore-specific plant at the plant-insec interface. Curr Opin Plant Biol 11:457–463 responses. Plant Physiol 125:711–717 Fernández-Calvo P, Chini A, Fernández-Barbero G, Chico JM, Gimenez- Heil M (2009) Damaged-self recognition in plant herbivore defence. Ibanez S, Geerinck J, Eeckhout D, Schweizer F, Godoy M, Franco- Trends Plant Sci 14:356–363 Zorrilla JM, Pauwels L, Witters E, Puga MI, Paz-Ares J, Goossens Heil M, Ibarra-Laclette E, Adame-Alvarez RM, Martinez O, Ramirez- A, Reymond P, De Jaeger G, Solano R (2011) The Arabidopsis Chaves E, Molina-Torres J, Herrera-Estrella L (2012) How plants bHLH transcription factors MYC3 and MYC4 are targets of JAZ sense wounds: Damaged-self recognition is based on plant-derived repressors and act additively with MYC2 in the activation of elicitors and induces octadecanoid signaling. PLoS One 7:e30537 jasmonate responses. Plant Cell 23:701–715 Heitz T, Widemann E, Lugan R, Miesch L, Ullmann P, Désaubry L, Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch Holder E, Grausem B, Kandel S, Miesch M, Werck-Reinchhart D, O, Wasternack C, Solano R (2009) (+)-7-iso-Jasmonoyl-L-isoleu- Pinot F (2012) Cytochromes P450 CYP94C1 and CYP94B3 cata- cine is the endogenous bioactive jasmonate. Nat Chem Biol 5:344– lyze two successive oxidation steps of plant hormone jasmonoyl- 350 isoleucine for catabolic turnover. J Biol Chem 287:6296–6306 Fonseca S, Fernández-Calvo P, Fernández GM, Diez-Diaz M, Gimenez- Herde M, Howe GA (2014) Host plant-specific remodeling of midgut Ibanez S, López-Vidriero I, Godoy M, Fernández-Barbero G, Van physiology in the generalist insect herbivore Trichoplusia ni. Insect Leene J, De Jaeger G, Franco-Zorrilla JM, Solano R (2014) Biochem Mol Biol 50C:58–67 bHLH003, bHLH013 and bHLH017 are new targets of JAZ repres- Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or sors negatively regulating JA responses. PLoS One 9:e86182 defend. Q Rev Biol 67:283–335 Fraenkel GS (1959) The raison d’être of secondary plant substances. Hogenhout SA, Bos JI (2011) Effector proteins that modulate plant– Science 129:1466–1470 insect interactions. Curr Opin Plant Biol 14:422–428 Fragoso V, Rothe E, Baldwin IT, Kim SG (2014) Root jasmonic acid Hou X, Lee LYC, Xia K, Yan Y, Yu H (2010) DELLAs modulate synthesis and perception regulate folivore-induced shoot metabo- jasmonate signaling via competitive binding to JAZs. Dev Cell 19: lites and increase Nicotiana attenuata resistance. New Phytol 202: 884–894 1335–1345 Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Fu ZQ, Dong X (2013) Systemic acquired resistance: Turning local Rev Plant Biol 59:41–66 infection into global defense. Annu Rev Plant Biol 64:839–863 Howe GA, Schilmiller AL (2002) Oxylipin metabolism in response to Gidda SK, Miersch O, Levitin A, Schmidt J, Wasternack C, Varin L stress. Curr Op Plant Biol 5:230–236 (2003) Biochemical and molecular characterization of a Howe GA, Lightner J, Browse J, Ryan CA (1996) An octadecanoid hydroxyjasmonate sulfotransferase from Arabidopsis thaliana.J pathway mutant (JL5) of tomato is compromised in signaling for Biol Chem 278:17895–17900 defense against insect attack. Plant Cell 8:2067–2077 Gimenez-Ibanez S, Boter M, Fernández-Barbero G, Chini A, Rathjen JP, Hu Y, Jiang L, Wang F, Yu D (2013a) Jasmonate regulates the inducer of Solano R (2014) The bacterial effector HopX1 targets JAZ tran- CBF expression–c-repeat binding factor/DRE binding factor1 cas- scriptional repressors to activate jasmonate signaling and promote cade and freezing tolerance in Arabidopsis. Plant Cell 25:2907– infection in Arabidopsis. PLoS Biol 12:e1001792 2924 Glauser G, Grata E, Dubugnon L, Mousavi SAR, Rudaz S, Wolfender JL, Hu P, Zhou W, Cheng Z, Fan M, Wang L, Xie D (2013b) JAV1 controls Farmer EE (2008) Spatial and temporal dynamics of jasmonate jasmonate-regulated plant defense. Mol Cell 50:504–515 J Chem Ecol (2014) 40:657–675 671

Hudgins JW, Christiansen E, Franceschi VR (2004) Induction of anatom- specifically secreted by a molluscan herbivore. PLoS One 9: ically based defense responses in stems of diverse conifers by e86500 methyl jasmonate: a phylogenetic perspective. Tree Physiol 24: Katagiri F, Tsuda K (2010) Understanding the plant immune system. Mol 251–264 Plant Microbe Interact 23:1531–1536 Huffaker A, Pearce G, Ryan CA (2006) An endogenous peptide signal in Katsir L, Chung HS, Koo AJK, Howe GA (2008a) Jasmonate signaling: a Arabidopsis activates components of the innate immune response. conserved mechanism of hormone sensing. Curr Opin Plant Biol 11: Proc Natl Acad Sci U S A 103:10098–10103 428–435 Huffaker A, Dafoe NJ, Schmelz EA (2011) ZmPep1, an ortholog of Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA (2008b) COI1 Arabidopsis elicitor peptide 1, regulates maize innate immunity is a critical component of a receptor for jasmonate and the bacterial and enhances disease resistance. Plant Physiol 155:1325–1338 virulence factor coronatine. Proc Natl Acad Sci U S A 105:7100– Huffaker A, Pearce G, Veyrat N, Erb M, Turlings TCJ, Sartor R, Shen Z, 7105 Briggs SP, Vaughan MM, Alborn HT, Teal PEA, Schmelz EA Kazan K, Manners JM (2008) Jasmonate signaling: toward an integrated (2013) Plant elicitor peptides are conserved signals regulating direct view. Plant Physiol 146:1459–1468 and indirect antiherbivore defense. Proc Natl Acad Sci U S A 110: Kazan K, Manners JM (2012) JAZ repressors and the orchestration of 5707–5712 phytohormone crosstalk. Trends Plant Sci 17:22–31 Huot B, Yao J, Montgomery BL, He SY (2014) Growth-defense tradeoffs Kazan K, Manners JM (2013) MYC2: The master in action. Mol Plant 6: in plants: a balancing act to optimize fitness. Mol Plant. doi:10.1093/ 686–673 mp/ssu049 Kessler A, Halitschke R, Baldwin IT (2004) Silencing the jasmonate Hyun Y, Choi S, Hwang HJ, Yu J, Nam S-J, Ko J, Park JY, Seo YS, Kim cascade: induced plant defenses and insect populations. Science EY, Ryu SB, Kim WT, Lee YH, Kang H, Lee I (2008) Cooperation 305:665–668 and functional diversification of two closely related galactolipase Kidd BN, Cahill DM, Manners JM, Schenk PM, Kazan K (2011) Diverse genes for jasmonate biosynthesis. Dev Cell 14:183–192 roles of the Mediator complex in plants. Semin Cell Dev Biol 22: Izaguirre MM, Mazza CA, Astigueta MS, Ciarla AM (2013) No time for 741–748 candy: passionfruit (Passiflora edulis) plants down-regulate Kim Y, Tsuda K, Igarashi D, Hillmer RA, Sakakibara H, Myers CL, damage-induced extra floral nectar production in response to light Katagiri F (2014) Mechanisms underlying robustness and tunability signals of competition. Oecologia 173:213–221 in a plant immune signaling network. Cell Host Microbe 15:84–94 Jeter CR, Tang W, Henaff E, Butterfield T, Roux SJ (2004) Evidence of a Kitaoka N, Matsubara T, Sato M, Takahashi K, Wakuta S, Kawaide H, novel cell signaling role for extracellular adenosine triphosphates Matsui H, Nabeta K, Matsuura H (2011) Arabidopsis CYP94B3 and diphosphates in Arabidopsis. Plant Cell 16:2652–2664 encodes jasmonyl-L-isoleucine 12-hydroxylase, a key enzyme in Jiang S, Yao J, Ma K-W, Zhou H, Song J, He SY, Ma W (2013) Bacterial the oxidative catabolism of jasmonate. Plant Cell Physiol 52:1757– effector activates jasmonate signaling by directly targeting JAZ 1765 transcriptional repressors. PLoS Pathog 9:e1003715 Kitaoka N, Kawaide H, Amano N, Matsubara T, Nabeta K, Takahashi K, Jones DGJ, Dangl JL (2006) The plant immune system. Nature 444:323– Matsuura H (2014) CYP94B3 activity against jasmonic acid amino 329 acid conjugates and the elucidation of 12-O-β-glucopyranosyl- Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S, Ntoukakis V, jasmonoyl-L-isoleucine as an additional metabolite. Jones JD, Shirasu K, Menke F, Jones A, Zipfel C (2014) Direct Phytochemistry 99:6–13 regulation of the NADPH oxidase RBOHD by the PRR-associated Kliebenstein DJ (2012) Plant defense compounds: systems approaches to kinase BIK1 during plant immunity. Mol Cell 54:43–55 metabolic analysis. Annu Rev Phytopathol 50:155–173 Kallenbach M, Bonaventure G, Gilardoni PA, Wissgott A, Baldwin IT Kombrink E (2012) Chemical and genetic exploration of jasmonate (2012) Empoasca leafhoppers attack wild tobacco plants in a biosynthesis and signaling paths. Planta 236:1351–1366 jasmonate-dependent manner and identify jasmonate mutants in Koo AJK, Howe GA (2009) The wound hormone jasmonate. natural populations. Proc Natl Acad Sci U S A 109:E1548–E1557 Phytochemistry 70:1571–1580 Kandoth PK, Mitchum MG (2013) War of the worms: how plants fight Koo AJK, Howe GA (2012) Catabolism and deactivation of the lipid- underground attacks. Curr Opin Plant Biol 16:457–463 derived hormone jasmonoyl-isoleucine. Frontiers Plant Sci 3:19 Kandoth PK, Ranf S, Pancholi SS, Jayanty S, Walla MD, Miller W, Howe Koo AJK, Chung HS, Kobayashi Y, Howe GA (2006) Identification of a GA, Lincoln DE, Stratmann JW (2007) Tomato MAPKs LeMPK1, peroxisomal acyl-activating enzyme involved in the biosynthesis of LeMPK2, and LeMPK3 function in the systemin-mediated defense jasmonic acid in Arabidopsis. J Biol Chem 281:33511–33520 response against herbivorous insects. Proc Natl Acad Sci U S A 104: Koo AJK, Gao X, Jones AD, Howe GA (2009) A rapid wound signal 12205–12210 activates the systemic synthesis of bioactive jasmonates in Kang JH, Wang L, Giri A, Baldwin IT (2006) Silencing threonine Arabidopsis. Plant J 59:974–986 deaminase and JAR4 in Nicotiana attenuata impairs jasmonic Koo AJK, Cooke TF, Howe GA (2011) Cytochrome P450 CYP94B3 acid-isoleucine-mediated defenses against Manduca sexta. Plant mediates catabolism and inactivation of the plant hormone Cell 18:3303–3320 jasmonoyl-L-isoleucine. Proc Natl Acad Sci U S A 108:9298–9303 Kang JH, Liu G, Shi F, Jones AD, Beaudry RM, Howe GA (2010a) The Krol E, Mentzel T, Chinchilla D, Boller T, Felix G, Kemmerling B, Postel tomato odorless-2 is defective in trichome-based production of S, Arents M, Jeworutzki E, Al-Rasheid KAS, Becker D, Hedrich R diverse specialized metabolites and broad-spectrum resistance to (2010) Perception of the Arabidopsis danger signal peptide 1 in- insect herbivores. Plant Physiol 154:262–272 volves the pattern recognition receptor AtPEPR1 and its close Kang JH, Shi F, Jones DA, Marks MD, Howe GA (2010b) Distortion of homologue AtPEPR2. J Biol Chem 285:13471–13479 trichome morphology by the hairless mutation of tomato affects the Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways leaf surface chemistry. J Exp Bot 61:1053–1064 in pathogen defense. Curr Opin Plant Biol 5:325–331 Kang JH, McRoberts J, Shi F, Moreno J, Jones D, Howe GA (2014) The Lee GI, Howe GA (2003) The tomato mutant spr1 is defective in flavanoid biosynthetic enzyme chalcone isomerase modulate terpe- systemin perception and the production of a systemic wound signal noid production in glandular trichomes of tomato. Plant Physiol 164: for defense gene expression. Plant J 33:567–576 1161–1174 Levy M, Wang Q, Kaspi R, Parrella MP, Abel S (2005) Arabidopsis Kästner J, von Knorre D, Himanshu H, Erb M, Baldwin IT, IQD1, a novel calmodulin–binding nuclear protein, stimulates glu- Meldau S (2014) Salicylic acid, a plant defense hormone, is cosinolate accumulation and plant defense. Plant J 43:79–96 672 J Chem Ecol (2014) 40:657–675

Li C, Williams M, Y-t L, Lee G-I, Howe GA (2002) Resistance of Mitsuhara I, Iwai T, Seo S, Yanagawa Y, Kawahigasi H, Hirose S, cultivated tomato to cell-content feeding herbivores is regulated by Ohkawa Y, Ohashi Y (2008) Characteristic expression of twelve the octadecanoid signaling pathway. Plant Physiol 130:494–503 rice PR1 family genes in response to pathogen infection, wounding, Li L, Zhao Y,McCaig BC, Wingerd BA, Wang J, Whalon ME, Pichersky and defense-related signal compounds. Mol Genet Genomics 279: E, Howe GA (2004) The tomato homolog of CORONATINE- 415–427 INSENSITIVE1 is required for the maternal control of seed matu- Mohan S, Ma PWK, Pechan T, Bassford ER, Williams WP, Luthe DS ration, jasmonate-signaled defense responses, and glandular tri- (2006) Degradation of the S. frugiperda peritrophic matrix by an chome development. Plant Cell 16:126–143 inducible maize cysteine protease. J Insect Physiol 52:21–28 Li L, Li M, Yu L, Zhou Z, Liang X, Liu Z, Cai G, Gao L, Zhang X, Wang Moreno JE, Tao Y, Chory J, Ballaré CL (2009) Ecological modulation of Y, Chen S, Zhou JM (2014) The FLS2-associated kinase BIK1 plant defenses via phytochrome control of jasmonate sensitivity. directly phosphorylates the NADPH oxidase RbohD to control plant Proc Natl Acad Sci U S A 106:4935–4940 immunity. Cell Host Microbe 15:329–338 MorenoJE,ShyuC,CamposML,PatelL,ChungHS,YaoJ,HeSY,Howe Liu Y, Zhang S (2004) Phosphorylation of 1-aminocyclopropane-1-car- GA (2013) Negative feedback control of jasmonate signaling by an boxylic acid synthase by MPK6, astress-responsive mitogen- alternative splice variant of JAZ10. Plant Physiol 162:1006–1017 activated protein kinase, induces ethylene biosynthesis in Mousavi SAR, Chauvin A, Pascaud F, Kellenberger S, Farmer EE (2013) Arabidopsis. Plant Cell 16:3386–3399 GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf Lotze MT, Zeh HJ, Rubartelli A, Sparvero LJ, Amoscato AA, Washburn wound signalling. Nature 500:422–426 NR, DeVera ME, Liang X, Tor M, Billiar T (2007) The grateful Mukhtar, European Union Effectoromics Consortium et al (2011) dead: damage-associated molecular patttern molecules and Independently evolved virulence effectors converge onto hubs in a reduction/oxidation regulate immunity. Immunol Rev 220:60–81 plant immune system network. Science 333:596–601 Maffei M, Bossi S, Spiteller D, Mithöfer A, Boland W (2004) Effects of Nahar K, Kyndt T, De Vleesschauwer D, Höfte M, Gheysen G (2011) feeding Spodoptera littoralis on lima bean leaves. I. Membrane The jasmonate pathway is a key player in systemically induced potentials, intracellular calcium variations, oral secretions, and re- defense against root knot nematodes in rice. Plant Physiol 157: gurgitate components. Plant Physiol 134:1752–1762 305–316 Maffei ME, Mithöfer A, Arimura G-I, Uchtenhagen H, Bossi S, Bertea Nakata M, Mitsuda N, Herde M, Koo AJK, Moreno JE, Suzuki K, Howe CM, Cucuzza LS, Novero M, Volpe V, Quadro S, Boland W (2006) GA, Ohme-Takagi M (2013) A bHLH-type transcription factor, Effects of feeding Spodoptera littoralis on lima bean leaves. III. ABA-inducible bhlh-type transcription factor/ja-associated myc2- Membrane depolarization and involvement of hydrogen peroxide. like1, acts as a repressor to negatively regulate jasmonate signaling Plant Physiol 140:1022–1035 in Arabidopsis. Plant Cell 25:1641–1656 Mafli A, Goudet J, Farmer EE (2012) Plants and tortoises: mutations in Navarro L, Zipfel C, Rowland O, Keller I, Robatzek S, Boller T, Jones the Arabidopsis jasmonate pathway increase feeding in a vertebrate JDG (2004) The transcriptional innate immune response to flg22. herbivore. Mol Ecol 21:2534–2541 Interplay and overlap with Avr gene-dependent defense responses Matzinger P (2002) The danger model: a renewed sense of self. Science and bacterial pathogenesis. Plant Physiol 135:1113–1128 296:301–305 Norman-Setterblad C, Vidal S, Palva ET (2000) Interacting signal path- McCloud ES, Baldwin IT (1997) Herbivory and caterpillar regurgitants ways control defense gene expression in Arabidopsis in response to amplify the wound-induced increases in jasmonic acid but not cell wall-degrading enzymes from Erwinia carotovora. Mol Plant nicotine in Nicotiana sylvestris. Planta 203:430–435 Microbe Inter 13:430–438 McConn M, Creelman RA, Bell E, Mullet JE, Browse J (1997) Jasmonate Orozco-Cárdenas ML, Narváez-Vásquez J, Ryan CA (2001) Hydrogen is essential for insect defense in Arabidopsis. Proc Natl Acad Sci U S peroxide acts as a second messenger for the induction of defense A 94:5473–5477 genes in tomato plants in response to wounding, systemin, and Meldau S, Erb M, Baldwin IT (2012) Defence and demand: mechanisms methyl jasmonate. Plant Cell 13:179–191 behind optimal defence patterns. Ann Bot 110:1503–1514 Paschold A, Bonaventure G, Kant MR, Baldwin IT (2008) Jasmonate Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant perception regulates jasmonate biosynthesis and JA-Ile metabolism: stomata function in innate immunity against bacterial invasion. Cell the case of COI1 in Nicotiana attenuata. Plant Cell Physiol 49: 126:969–980 1165–1175 Melotto M, Mecey C, Niu Y, Chung HS, Katsir L, Yao J, Zeng W, Thines Pauwels L, Goossens A (2011) The JAZ proteins: a crucial interface in B, Staswick P, Browse J, Howe GA, He SY (2008) A critical role of the jasmonate signaling cascade. Plant Cell 23:3089–3100 two positively charged amino acids in the Jas motif of Arabidopsis Pauwels L, Barbero GF, Geerinck J, Tilleman S, Grunewald W, Pérez JAZ proteins in mediating coronatine- and jasmonoyl isoleucine- AC, Chico JM, Bossche RV, Sewell J, Gil E, Garcia-Casado G, dependent interactions with the COI1 F-box protein. Plant J 55:979– Witters E, Inze D, Long JA, Jaeger GD, Solano R, Goossens A 988 (2010) NINJA connects the co-repressor TOPLESS to jasmonate Middleton AM, Úbeda-Tomás S, Griffiths J, Holman T, Hedden P, signalling. Nature 464:788–791 Thomas SG, Phillips AL, Holdsworth MJ, Bennett MJ, King JR, Pearce G, Strydom D, Johnson S, Ryan CA (1991) A polypeptide from Owen MR (2012) Mathematical modeling elucidates the role of tomato leaves induces wound-inducible proteinase inhibitor pro- transcriptional feedback in gibberellin signaling. Proc Natl Acad teins. Science 23:895–897 Sci U S A 109:7571–7576 Peiffer M, Tooker JF, Luthe DS, Felton GW (2009) Plants on early alert: Miersch O, Neumerkel J, Dippe M, Stenzel I, Wasternack C (2008) glandular trichomes as sensors for insect herbivores. New Phytol Hydroxylated jasmonates are commonly occuring metabolites of 184:644–656 jasmonic acid and contribute to a partial switch-off in jasmonate Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC (2009) signaling. New Phytol 177:114–127 Networking by small-molecule hormones in plant immunity. Nat Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl Chem Biol 5:308–316 JL, Mittler R (2009) The plant NADPH oxidase RBOHD mediates Plant Science Research Summit. (2013) Unleashing a decade of innova- rapid systemic signaling in response to diverse stimuli. Sci Signal 2: tion in plant science: A vision for 2015–2025. http://plantsummit. ra45 wordpress.com/ Mithöfer A, Boland W (2008) Recognition of herbivory-associated mo- Plett JM, Khachane A, Ouassou M, Sundberg B, Kohler A, Martin F lecular patterns. Plant Physiol 146:825–831 (2014a) Ethylene and jasmonic acid act as negative modulators J Chem Ecol (2014) 40:657–675 673

during mutualistic symbiosis between Laccaria bicolor and Populus Schmelz EA, LeClere S, Carroll MJ, Alborn HT, Teal PEA (2007) roots. New Phytol 202:270–286 Cowpea chloroplastic ATP synthase is the source of multiple plant Plett JM, Daguerre Y, Wittulsky S, Vayssières A, Deveau A, Melton SJ, defense elicitors during insect herbivory. Plant Physiol 144:793–805 Kohler A, Morrell-Flavey JL, Brun A, Veneault-Fourrey C, Martin F Schmelz EA, Kaplan F, Huffaker A, Dafoe NJ, Vaughan MM, Ni X, (2014b) Effector MiSSP7 of the mutualistic fungus Laccaria bicolor Rocca JR, Alborn HT, Teal PE (2011) Identity, regulation, and stabilizes the Populus JAZ6 protein and represses jasmonic acid activity of inducible diterpenoid phytoalexins in maize. Proc Natl (JA) responsive genes. Proc Natl Acad Sci U S A. doi:10.1073/ Acad Sci U S A 108:5455–5460 pnas.1322671111 Schmelz EA, Huffaker A, Sims JW, Christensen SA, Lu X, Okada K, Prince DC, Drurey C, Zipfel C, Hogenhout SA (2014) The leucine-rich Peters RJ (2014) Biosynthesis, elicitation and roles of monocot repeat receptor-like kinase brassinosteroid insensitive1-associated terpenoid phytoalexins. Plant J. doi:10.1111/tpj.12436 kinase1 and the cytochrome P450 phytoalexin deficient3 contribute Schwartzberg EG, Tumlinson JH (2013) Aphid honeydew alters plant to innate immunity to aphids in Arabidopsis. Plant Physiol 164: defence responses. Funct Ecol 28:386–394 2207–2019 Schweighofer A, Kazanaviciute V, Scheikl E, Teige M, Doczi R, Hirt H, Qi Z, Stephens NR, Spalding EP (2006) Calcium entry mediated by Schwanninger M, Kant M, Schuurink R, Mauch F, Buchala A, GLR3.3, an Arabidopsis glutamate receptor with a broad agonist Cardinale F, Meskiene I (2007) The PP2C-type phosphatase profile. Plant Physiol 142:963–971 AP2C1, which negatively regulates MPK4 and MPK6, modulates Qi T, Song S, Ren Q, Wu D, Huang H, Chen Y, Fan M, Peng W, Ren C, innate immunity, jasmonic acid, and ethylene levels in Arabidopsis. Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the Plant Cell 19:2213–2224 WD-Repeat/bHLH/MYB complexes to regulate jasmonate- Schweizer F, Fernández-Calvo P, Zander M, Diez-Diaz M, Fonseca S, mediated anthocyanin accumulation and trichome initiation in Glauser G, Lewsey MG, Ecker JR, Solano R, Reymond P (2013) Arabidopsis thaliana. Plant Cell 23:1795–1814 Arabidopsis basic helix-loop-helix transcription factors MYC2, Qi T, Huang H, Wu D, Yan J, Qi Y, Song S, Xie D (2014) Arabidopsis MYC3, and MYC4 regulate glucosinolate biosynthesis, insect per- DELLA and JAZ proteins bind the WD-repeat/bHLH/MYB com- formance, and feeding behavior. Plant Cell 25:3117–3132 plex to modulate gibberellin and jasmonate signaling synergy. Plant Seo S, Katou S, Seto H, Gomi K, Ohashi Y (2007) The mitogen- Cell Early Edition 26(3):1118–1133 activated protein kinases WIPK and SIPK regulate the levels Radhika V, Kost C, Mithöfer A, Boland W (2010) Regulation of of jasmonic and salicylic acids in wounded tobacco plants. extrafloral nectar secretion by jasmonates in lima bean is light Plant J 49:899–909 dependent. Proc Natl Acad Sci U S A 107:17228–17233 Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G, Hinds TR, Rasmann S, De Vos M, Casteel CL, Tian D, Halitschke R, Sun JY, Kobayashi Y, Hsu F-F, Sharon M, Browse J, He SY, Rizo J, Howe Agrawal AA, Felton GW, Jander G (2012) Herbivory in the previ- GA, Zheng N (2010) Jasmonate perception by inositol-phosphate- ous generation primes plants for enhanced insect resistance. Plant potentiated COI1-JAZ co-receptor. Nature 468:400–405 Physiol 158:854–863 Shyu C, Figueroa P, Depew CL, Cooke TF, Sheard LB, Moreno JE, Reymond P (2013) Perception, signaling and molecular basis of Katsir L, Zheng N, Browse J, Howe GA (2012) JAZ8 lacks a oviposition-mediated plant responses. Planta 238:247–258 canonical degron and has an EAR motif that mediates transcriptional Reymond P, Farmer EE (1998) Jasmonate and salicylate as global signals repression of jasmonate responses in Arabidopsis. Plant Cell 24: for defense gene expression. Curr Opin Plant Biol 1:404–411 536–550 Reymond P, Bodenhausen N, Van Poecke RMP, Krishnamurthy V, Dicke Silverman P, Seskar M, Kanter D, Schweizer P, Metraux JP, Raskin I M, Farmer EE (2004) A conserved transcript pattern in response to a (1995) Salicylic acid in rice (Biosynthesis, Conjugation, and specialist and a generalist herbivore. Plant Cell 16:3132–3147 Possible Role). Plant Physiol 108:633–639 Robert-Seilaniantz A, Grant M, Jones JDG (2011) Hormone crosstalk in Song CJ, Steinebrunner I, Wang X, Stout SC, Roux SJ (2006) plant disease and defense: more than just jasmonate-salicylate an- Extracellular ATP induces the accumulation of superoxide via tagonism. Annu Rev Phytopathol 49:317–343 NADPH oxidases in Arabidopsis. Plant Physiol 140:1222–1232 Romeis T, Herde M (2014) From local to global: CDPKs in systemic Song S, Qi T, Huang H, Ren Q, Wu D, Chang C, Peng W, Liu Y, Peng J, defense signaling upon microbial and herbivore attack. Curr Opin Xie D (2011) The jasmonate-ZIM domain proteins interact with the PlantBiol20:1–10 R2R3-MYB transcription factors MYB21 and MYB24 to affect Salvador-Recatalà V, Tjallingii WF, Farmer EE (2014) Real-time, in vivo jasmonate-regulated stamen development in Arabidopsis. Plant intracellular recordings of caterpillar-induced depolarization waves Cell 23:1000–1013 in sieve elements using aphid electrodes. New Phytol 203(2):674– Song S, Qi T, Fan M, Zhang X, Gao H, Huang H, Wu D, Guo H, Xie D 684 (2013) The bHLH subgroup IIId factors negatively regulate Sasaki-Sekimoto Y,Jikumaru Y,Obayashi T, Saito H, Masuda S, Kamiya jasmonate-mediated plant defense and development. PLoS Genet Y, Ohta H, Shirasu K (2013) Basic-Loop-Helix transcription factors 9:e1003653 JASMONATE-ASSOCIATED MYC2-LIKE1 (JAM1), JAM2, and Song S, Huang H, Gao H, Wang J, Wu D, Liu X, Yang S, Zhai Q, Li C, Qi JAM3 are negative regulators of jasmonate responses in T, Xie D (2014) Interaction between MYC2 and ETHYLENE Arabidopsis. Plant Phys 163:291–304 INSENSITIVE3 modulates antagonism between jasmonate and eth- Sato M, Tsuda K, Wang L, Coller J, Watanabe Y,Glazebrook J, Katagiri F ylene signaling in Arabidopsis. Plant Cell 26:263–279 (2010) Network modeling reveals prevalent negative regulatory Staswick PE (2008) JAZing up jasmonate signaling. Trends Plant Sci 13: relationships between signaling sectors in Arabidopsis immune 66–71 signaling. PLoS Pathog 6:e1001011 Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is Schaller A, Stintzi A (2009) Enzymes in jasmonate biosynthesis - activated by an enzyme that conjugates it to isoleucine in Structure, function, regulation. Phytochemistry 70:1532–1538 Arabidopsis. Plant Cell 16:2117–2127 Schilmiller AL, Howe GA (2005) Systemic signaling in the wound Staswick PE, Yuen GY, Lehman CC (1998) Jasmonate signaling mutants response. Curr Opin Plant Biol 8:369–377 of Arabidopsis are susceptible to soil fungus Pythium irregulare. Schmelz EA, Alborn HT, Banchio E, Tumlinson JH (2003) Quantitative Plant J 15:747–754 relationships between induced jasmonic acid levels and volatile Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin- emission in Zea mays during Spodoptera exigua herbivory. Planta dependent transcriptional repression during Arabidopsis embryo- 216:665–673 genesis. Science 319:1384–1386 674 J Chem Ecol (2014) 40:657–675

Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS, Han B, Zhu T, Zou G, Mining the plant-herbivore interface with a leafmining Drosophila Katagiri F (2003) Quantitative nature of Arabidopsis responses of Arabidopsis. Mol Ecol 20:995–1014 during compatible and incompatible interactions with the bacterial Widemann E, Miesch L, Lugan R, Holder E, Heinrich C, Aubert Y, pathogen Pseudomonas syringae. Plant Cell 15:317–330 Miesch M, Pinot F, Heitz T (2013) The amidohydrolases IAR3 Thaler JS, Stout MJ, Karban R, Duffey SS (2001) Jasmonate-mediated and ILL6 contribute to jasmonoyl-isoleucine hormone turnover induced plant resistance affects a community of herbivores. Ecol and generate 12-hydroxyjasmonic acid upon wounding in Entomol 26:312–324 Arabidopsis leaves. J Biol Chem 288:31701–31714 Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate Wildon DC, Thain JF, Minchin PEH, Gubb IR, Reilly AJ, Skipper YD, and salicylate signal crosstalk. Trends Plant Sci 17:260–270 Doherty HM, O’Donnell PJ, Bowles DJ (1992) Electrical signaling Thilmony R, Underwood W, He SY (2006) Genome-wide transcriptional and systemic proteinase-inhibitor induction in the wounded plant. analysis of the Arabidopsis thaliana interaction with the plant path- Nature 360:62–65 ogen Pseudomonas syringae pv. tomato DC3000 and the human Wise RP, Moscou MJ, Bogdanove AJ, Whitham SA (2007) Transcript pathogen Escherichia coli O157:H7. Plant J 46:34–53 profiling in host-pathogen interactions. Annu Rev Phytopathol 45: Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, 329–369 He SY, Howe GA, Browse J (2007) JAZ repressor proteins are Withers J, Yao J, Mecey C, Howe GA, Melotto M, He SY (2012) targets of the SCFCO11 complex during jasmonate signalling. Transcription factor-dependent nuclear localization of a transcrip- Nature 448:661–666 tional repressor in jasmonate hormone signaling. Proc Natl Acad Sci Thomma BP,Eggermont K, Penninckx IA, Mauch-Mani B, Vogelsang R, USA104:7483–7488 Cammue BP, Broekaert WF (1998) Separate jasmonate-dependent Woldemariam MG, Onkokesung N, Baldwin IT, Galis I (2012) and salicylate-dependent defense-response pathways in Arabidopsis Jasmonoyl- l-isoleucine hydrolase 1 (JIH1) regulates jasmonoyl- l- are essential for resistance to distinct microbial pathogens. Proc Natl isoleucine levels and attenuates plant defenses against herbivores. Acad Sci U S A 95:15107–15111 Plant J 72:758–767 Toda Y, Tanaka M, Ogawa D, Kurata K, Kurotani KI, Habu Y, Ando T, Wu J, Baldwin IT (2010) New insights into plant responses to the attack Sugimoto K, Mitsuda N, Katoh E, Abe K, Miyao A, Hirochika H, from insect herbivores. Annu Rev Genet 44:1–24 Hattori T, Takeda S (2013) RICE SALT SENSITIVE 3 forms a Wu J, Hettenhausen C, Meldau S, Baldwin IT (2007) Herbivory rapidly ternary complex with JAZ and Class-C bHLH factors and regulates activates MAPK signaling in attacked and unattacked leaf regions but jasmonate-induced gene expression and root cell elongation. Plant not between leaves of Nicotiana attenuata. Plant Cell 19:1096–1122 Cell 25:1709–1725 Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: an Traw MB, Bergelson J (2003) Interactive effects of jasmonic acid, Arabidopsis gene required for jasmonate-regulated defense and salicylic acid, and gibberellin on induction of trichomes in fertility. Science 280:1091–1094 Arabidopsis. Plant Physiol 133:1367–1375 Yamada S, Kano A, Tamaoki D, Miyamoto A, Shishido H, Miyoshi S, Truitt CL, Wei HX, Paré PW (2004) A plasma membrane protein from Taniguchi S, Akimitsu K, Gomi K (2012) Involvement of OsJAZ8 Zea mays binds with the herbivore elicitor volicitin. Plant Cell 16: in jasmonate-induced resistance to bacterial blight in rice. Plant Cell 523–532 Physiol 53:2060–2072 TsudaK,SatoM,GlazebrookJ,CohenJD,KatagiriF(2008)Interplay Yamaguchi Y, Pearce G, Ryan CA (2006) The cell surface leucine-rich between MAMP-triggered and SA-mediated defense responses. repeat receptor for AtPep1, an endogenous peptide elicitor in Plant J 53:763–775 Arabidopsis, is functional in transgenic tobacco cells. Proc Natl Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F (2009) Acad Sci U S A 103:10104–10109 Network properties of robust immunity in plants. PLoS Genet Yamaguchi Y,Huffaker A, Bryan AC, Tax FE, Ryan CA (2010) PEPR2 is 12:e1000772 a second receptor for the Pep1 and Pep2 peptides and contributes to Uppalapati SR, Ishiga Y, Wangdi T, Kunkel BN, Anand A, Mysore KS, defense responses in Arabidopsis. Plant Cell 22:508–522 Bender CL (2007) The phytotoxin coronatine contributes to patho- Yamane H (2013) Biosynthesis of phytoalexins and regulatory mecha- gen fitness and is required for suppression of salicylic acid accumu- nisms of it in rice. Biosci Biotechnol Biochem 77:1141–1148 lation in tomato inoculated with Pseudomonas syringae pv. tomato Yan Y, Stolz S, Chételat A, Reymond P, Pagni M, Dubugnon L, Farmer DC3000. Mol Plant Microbe Inter 20:955–965 EE (2007) A downstream mediator in the growth repression limb of van Loon LC, Rep M, Pieterse CM (2006) Significance of inducible the jasmonate pathway. Plant Cell 19:2470–2483 defense-related proteins in infected plants. Annu Rev Phytopathol Yan Y, Christensen S, Isakeit T, Engelberth J, Meeley R, Hayward A, 44:135–162 Emery RJN, Kolomiets MV (2012) Disruption of OPR7 and OPR8 Van Poecke RMP, Dicke M (2002) Induced parasitoid attraction by reveals the versatile function of jasmonic acid in maize development Arabidopsis thaliana: involvement of the octadecanoid and the and defense. Plant Cell 24:1420–1436 salicylic acid pathway. J Exp Bot 53:1793–1799 Yang DH, Hettenhausen C, Baldwin IT, Wu J (2011) BAK1 regulates the Vijayan P, Shockey J, Levesque CA, Cook RJ, Browse J (1998) A role for accumulation of jasmonic acid and the levels of trypsin proteinase jasmoante in pathogen defense of Arabidopsis. Proc Natl Acad Sci inhibitors in Nicotiana attenuata’s responses to herbivory. J Exp Bot USA95:7209–7214 62:641–652 Walling LL (2008) Avoiding effective defenses: strategies employed by Yang DH, Hettenhausen C, Baldwin IT, Wu J (2012a) Silencing phloem-feeding insects. Plant Physiol 146:859–866 Nicotiana attenuata calcium-dependent protein kinases, CDPK4 Wan J, Zhang XC, Neece D, Ramonell KM, Clough S, Kim SY, Stacey and CDPK5, strongly up-regulates wound-and herbivory-induced MG, Stacey G (2008) A LysM receptor-like kinase plays a critical jasmonic acid accumulations. Plant Phys 159:1591–1607 role in chitin signaling and fungal resistance in Arabidopsis. Plant Yang DL, Yao J, Mei C-S, Tong XH, Zeng LJ, Li Q, Xiao LT, Sun TP, Li Cell 20:471–781 J, Deng XW, Lee CM, Thomashow MF, Yang Y, Zuhua H, He SY Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, (2012b) Plant hormone jasmonate prioritizes defense over growth signal transduction and action in plant stress response, growth and by interfering with gibberellin signaling cascade. Proc Natl Acad Sci development. An update to the 2007 review in Annals of Botany. USA109:E1192–E1200 Ann Bot 111:1021–1058 Ye M, Luo SM, Xie JF, Li YF, Xu T, Liu Y, Song YY, Zhu-Salzman K, Whiteman NK, Groen SC, Chevasco D, Bear A, Beckwith N, Gregory Zeng RS (2012) Silencing COI1 in rice increases susceptibility to TR,DenouxC,MammarellaN,AusubelFM,PierceNE(2011) chewing insects and impairs inducible defense. PLoS One 7:e36214 J Chem Ecol (2014) 40:657–675 675

Yoshida Y, Sano R, Wada T, Takabayashi J, Okada K (2009) Jasmonic (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy acid control of GLABRA3 links inducible defense and trichome in Arabidopsis. Proc Natl Acad Sci U S A 108:12539–12544 patterning in Arabidopsis. Development 136:1039–1048 Zhurov V,Navarro M, Bruinsma KA, Arbona V,Santamaria ME, Cazaux Zarate SI, Kempema LA, Walling LL (2007) Silverleaf whitefly induces M, Wybouw N, Osborne EJ, Ens C, Rioja C, Vermeirssen V, Rubio- salicylic acid defenses and suppresses effectual jasmonic acid de- Somoza I, Krishna P, Diaz I, Schmid M, Gomez-Cardenas A, Peer fenses. Plant Physiol 143:866–875 YV, Grbic M, Clark RM, Leeuwen TV, Grbic V (2014) Reciprocal Zhang S, Klessig DF (2001) MAPK cascades in plant defense signaling. responses in the interaction between Arabidopsis and the cell- Trends Plant Sci 6:520–527 content-feeding chelicerate herbivore spider mite. Plant Physiol Zhang Y, Turner JG (2008) Wound-induced endogenous jasmonate stunt 164:384–399 plant growth by inhibiting mitosis. PLoS One 3:e3699 Zimmermann MR, Maischak H, Mithöfer A, Boland W, Felle HH (2009) Zhang PJ, Li WD, Huang F, Zhang JM, Xu FC, Lu YB (2013) Feeding by System potentials, a novel electrical long-distance apoplastic signal whiteflies suppresses downstream jasmonic acid signaling by in plants, induced by wounding. Plant Physiol 149:1593–1600 eliciting salicylic acid signaling. J Chem Ecol 39:612–619 Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, Boller T, Felix G Zhao Y, Thilmony R, Bender CL, Schaller A, He SY, Howe GA (2003) (2006) perception of the bacterial PAMP EF-Tu by the receptor EFR Virulence systems of Pseudomonas syringae pv. tomato promote restricts Agrobacterium-mediated transformation. Cell 125:749–760 bacterial speck disease in tomato by targeting the jasmonate signal- Zou C, Sun K, Mackaluso JD, Seddon AE, Jin R, Thomashow MF, Shiu ing pathway. Plant J 36:485–499 SH (2011) Cis-regulatory code of stress-responsive transcription in Zheng XY, Spivey NW, Zeng W, Liu PP, Fu ZQ, Klessig DF, He SY, Arabidopsis thaliana. Proc Natl Acad Sci U S A 108:14992–14997 Dong X (2012) Coronatine promotes Pseudomonas syringae viru- Zulak KG, Bohlmann J (2010) Terpenoid biosynthesis and special- lence in plants by activating a signaling cascade that inhibits ized vascular cells of conifer defense. J Integr Plant Biol 52: salicylic acid accumulation. Cell Host Microbe 11:587–596 86–97 Zhu Z, An F, Feng Y, Li P, Xue L, Mu A, Jiang Z, Kim JM, To TK, Li W, Züst T, Heichinger C, Grossniklaus U, Harrington R, Kliebenstein DJ, Zhang X, Yu Q, Dong Z, Chen WQ, Seki M, Zhou JM, Guo H Turnbull LA (2012) Natural enemies drive geographic variation in (2011) Derepression of ethylene-stabilized transcription factors plant defenses. Science 338:116–119