New Weapons and a Rapid Response against Insect Attack

Abstract

Jasmonates (JAs) comprise a class of related oxylipin signaling molecules that have overlapping roles in regulating both stress responses and development in plants. Stress responses that depend on JA signaling include not only defense against insects but also defense against microbial pathogens, as well as responses to UV radiation, ozone, and other abiotic stresses (Glazebrook, 2005; Wasternack, 2007; Balbi and Devoto, 2008; Howe and Jander, 2008). In healthy, nonstressed plant tissue, JAs are involved in carbon partitioning, mechanotransduction, senescence, and reproductive development (Browse, 2005). The JA-dependent responses are associated with large-scale reprogramming of gene expression; hundreds of downstream JA-regulated and JA-coregulated genes have been identified (Reymond et al., 2000; Schenk et al., 2000; Devoto et al., 2005; Mandaokar et al., 2006). Biosynthesis and metabolism of JA. The octadecanoid pathway converts 18:3 to (+)-7-iso-JA, which epimerizes to the more stable (−)-JA isomer. It is generally assumed that (+)-7-iso-JA is the biologically relevant and more active form of the hormone. JA is metabolized to a wide range of derivatives (see text for details). For example, JA carboxyl methyltransferase (JMT in the image) converts JA to the volatile compound MeJA. Conjugation of JA to Ile by JAR1 produces JA-Ile, which promotes COI1 interaction with the JAZ1 repressor protein. Other enzymes, presumably related to JAR1, catalyze the formation of other JA-amino acid conjugates (JACs in the image). Coronatine (in red) is a phytotoxin produced by virulent strains of Pseudomonas syringae. The toxin functions as a JA mimic and is structurally related to JA-Ile. The ability of methyl-JA (MeJA) to induce anti-insect proteinase inhibitors (PIs) in tomato (Solanum lycopersicum) was first reported in 1990 (Farmer and Ryan, 1990); articles describing the induction of some pathogen-defense genes followed (Glazebrook, 2005). The critical requirement for JA to induce defense against insects was established through investigations of JA synthesis mutants in tomato (Howe et al., 1996; Li et al., 2005) and Arabidopsis (McConn et al., 1997). Similarly, mutant analysis was central to establishing the importance of JA in defense against pathogens—particularly necrotrophic fungi and oomycetes (Vijayan et al., 1998; Glazebrook, 2005)—and to the recognition that JA is essential during the final stages of flower development in Arabidopsis (McConn and Browse, 1996) and tomato (Li et al., 2004). In this Update, we will focus on the role of JAs in plant defense against arthropod herbivores, but the other processes controlled by the hormone will be discussed to the extent that they have provided new insight into the molecular mechanism of JA signaling. JA is synthesized from membrane-derived 18:3 via the octadecanoid pathway (Browse, 2005; Schaller et al., 2005; Wasternack, 2007; Fig. 1). Newly synthesized JA, also known as (+)-7-iso-JA, epimerizes to the more stable (−)-JA isomer in which the side chains on the cyclopentane ring are in the thermodynamically more stable trans-configuration. JA is subject to various enzymatic transformations to generate a suite of derivatives that differ in their biological activities (Fig. 1). Among the major routes of JA metabolism are: (1) methylation of C-1 to yield volatile MeJA, which was originally identified as a fragrant component of jasmine flowers; (2) decarboxylation of C-1 to form another volatile compound, cis-jasmone; (3) hydroxylation at C-12 (or C-11) yielding tuberonic acid and related derivatives that can be modified further by sulfation or glycosylation; (4) reduction of C-6 to yield cucurbic acid, which may also be esterified to sugar residues; and (5) amide-linked conjugation of the carboxyl group to Ile and other amino acids, yielding jasmonoyl-l-Ile (JA-Ile) and other jasmonoyl-amino acid conjugates, respectively (Fig. 1). An important question in JA research concerns the biological function of the many chemical derivatives of the hormone. Here, we define bioactive JAs as compounds that bind to a receptor to evoke a physiological response. Nonbioactive JAs are either precursors or deactivated forms of active JAs. For example, hydroxylation of JA was recently implicated as a mechanism to deactivate the JA signaling pathway (Miersch et al., 2007). Although JA (i.e. jasmonic acid) and MeJA are generally considered to be bioactive, receptors that bind JA/MeJA have not been identified. Analysis of jar1 mutants that fail to convert JA to JA-Ile indicates that JA-Ile is a primary signal for at least some defense responses to pathogens and insects (Staswick et al., 1998; Staswick and Tiryaki, 2004; Kang et al., 2006). At present, JA-Ile is the only derivative known to be active at the molecular level (see below). The JA pathway constitutes a highly conserved mechanism for promoting plant defense responses to many, if not most, arthropod herbivores (Howe and Jander, 2008