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Jasmonate-Triggered Plant Immunity 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.<H. Kang G. A. Howe (*) these protective chemical shields and associated morphologi- Department of Energy-Plant Research Laboratory, Michigan State cal structures may be constitutive or inducible. It is thought University, East Lansing, MI 48824, USA e-mail: [email protected] that natural selection, at least in some plant species, favored the evolution of induced defenses because they have lower G. A. Howe resource allocation costs than constitutive resistance traits Department of Biochemistry and Molecular Biology, Michigan State (Baldwin 1998; Herms and Mattson 1992; Thaler et al. University, East Lansing, MI 48824, USA 2012). A key feature of many induced defense traits is their Present Address: expression in tissues distal to the site of infection or attack. J.-H. Kang The combined effect of local and systemic defense responses Department of Plant Science, Plant Genomics and Breeding Institute, provides broad-spectrum resistance against biotic attack, and and Research Institute for Agriculture and Life Sciences, College of Agricultural Sciences, Seoul National University, 599 Gwanak-ro constitutes a form of induced immunity (Fu and Dong 2013; Gwank-gu, Seoul 151-921, Republic of Korea Howe and Jander 2008;JonesandDangl2006). 658 J Chem Ecol (2014) 40:657–675 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
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