Update on Jasmonate Signaling Jasmonate Signaling: Toward an Integrated View

Oxylipins are biologically active signaling molecules derived from oxygenated polyunsaturated fatty acids and are found ubiquitously in most living organisms. In mammals, the eicosanoids, which include prostaglandins, are one of the best-studied groups of biologically important oxylipins. In addition to their essential roles in numerous other physiological functions, eicosanoids function as signaling molecules in vertebrate and invertebrate animals and in eukaryotic microbes (Stanley, 2006). The discovery of prostaglandins and related biologically active substances was recognized by the award of a Nobel Prize in Physiology or Medicine in 1982. Shortly after this, the pioneering work published in Plant Physiology by Vick and Zimmerman (1984) provided one of the first insights into the biosynthesis of jasmonate (JA), an oxylipin signaling molecule in plants. Indeed, of the various oxylipins synthesized enzymatically through the oxylipin (also known as octadecanoid) pathway, the plant hormones JAs (e.g. jasmonic acid and its methyl ester, MeJA) are often considered to be the structural and, in some cases, functional analogues of prostaglandins in animals. JAs are potent regulators of genes involved in cell growth and biotic and abiotic stress responses. Over the last decade or so, the JA signaling pathway has been studied extensively in dicot plant species, such as Arabidopsis (Arabidopsis thaliana), tomato (Solanum lycopersicum), and tobacco (Nicotiana tabacum), and to a somewhat limited extent in monocot plants, such as barley (Hordeum vulgare) and rice (Oryza sativa). Although much remains to be learnt, both forward and reverse genetic studies, particularly in Arabidopsis, have greatly expanded our understanding of the potential roles of JAs in plants. The biosynthesis of JAs has recently been reviewed (Wasternack, 2007), and a general overview is shown in Figure 1. Following synthesis, JAs are perceived by as yet unknown receptor proteins, and this presumably activates a signal transduction pathway that culminates in the transcriptional activation or repression of a large number of JA-responsive genes. JAs inhibit root elongation, and this property has been extensively exploited for the identification of JA signaling mutants. One of the first JA signaling mutants identified was the Arabidopsis coronatine insensitive1 (coi1) mutant. Root elongation of coi1 mutant seedlings showed reduced sensitivity to JAs but also to coronatine (COR), a functional JA homolog and toxin produced by the bacterial pathogen Pseudomonas syringae (Feys et al., 1994). The coi1 mutant displays defects in many, if not all, JA-dependent functions, such as fertility, secondary metabolite biosynthesis, pest and pathogen resistance, and wound responses. The COI1 locus encodes an F-box protein, and because F-box proteins are integral parts of multi-protein complexes involved in protein ubiquitination, it was speculated that COI1 is required for removal of repressors of the JA signaling pathway (Xie et al., 1998). However, until very recently, the nature of the COI1-targeted repressors has remained elusive. Similarly, two other JA signaling loci, JAR1 (JASMONATE RESISTANT1) and JIN1 (JASMONATE INSENSITIVE1), were identified from analyses of the Arabidopsis jar1 and jin1 mutants, which also show reduced sensitivity to exogenous JAs. JAR1 encodes a JA amino acid synthetase involved in conjugating jasmonic acid to Ile (Staswick and Tiryaki, 2004). JIN1 (also known as MYC2) encodes a basic helix-loop-helix-type transcription factor involved in the transcriptional regulation of JA-responsive gene expression (Lorenzo et al., 2004). Despite extensive characterizations of individual mutants, the exact nature of the functional relationships among these three major players (i.e. COI1, JAR1, and JIN1/MYC2) of JA signaling has long been enigmatic. Importantly, the recent cloning of the JAI3 (JASMONATE INSENSITIVE3) locus (Chini et al., 2007) has filled a significant gap in our overall understanding of the JA signaling pathway by mechanistically linking the functions of COI1, JAR1, and JIN1, as well as revealing the nature of the longsought repressors of JA signaling. Our aim in this Update article is to briefly review these recent findings that have added fresh insights into our understanding of how JA signals are transmitted within the cell. Our particular focus will be on the roles of a recently discovered class of repressors whose destruction through a COI1-mediated ubiquitination pathway is required for the transcriptional activation of the JA-dependent gene expression. In addition, the emerging roles of the transcriptional regulator JIN1/MYC2 that acts immediately downstream * Corresponding author; e-mail [email protected]. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Kemal Kazan ([email protected]). www.plantphysiol.org/cgi/doi/10.1104/pp.107.115717