Báo cáo khoa học: Plant oxylipins: COI1/JAZs/MYC2 as the core jasmonic acid-signalling module pptx

MINIREVIEW Plant oxylipins: COI1/JAZs/MYC2 as the core jasmonic acid-signalling module Andrea Chini, Marta Boter and Roberto Solano Departamento de Gene ´ tica Molecular de Plantas, Centro Nacional de Biotecnologı ´ a-CSIC, Madrid, Spain Introduction Plants are sessile organisms that need to adapt to their constantly changing environment. The specific plant response to a particular stimulus, crucial for its survival and fitness, is mediated by a complex hormonal network. Jasmonates (JAs) are essential signalling molecules modulating the plant response to biotic and abiotic stresses as well as several growth and developmental traits [1–4]. In general, JAs help to modulate the com- petitive allocation of plant energy to defence or growth, the two major processes determining plant fitness. Dissection of the jasmonic acid (JA) pathway has been predominantly carried out using genetic studies. The Arabidopsis coi1 mutant was originally identified as insensitive to coronatine (COR), a bacterial com- pound structurally related to JAs [5,6]. coi1 plants are defective in all JA-dependent responses tested, demon- strating the central role of COI1 in the JA-signalling pathway [7]. COI1 encodes an F-box protein. Proteins containing an F-box domain are components of the Skp ⁄ Cullin ⁄ F-box (SCF)-type E3 ubiquitine ligase complexes conferring substrate specificity. Mutations in additional components or regulators of SCF com- plexes such as AXR1, CUL1, RBX and JAI4 ⁄ SGT1b also show JA insensitivity, further supporting the importance of protein degradation in activating the JA pathway (Table 1) [8–12]. Keywords arabidopsis; COI1; hormone response; Jas domain; jasmonate signalling; JAZ repressors; MYC2; transcription factors; ZIM domain Correspondence R. Solano, Departamento de Gene ´ tica Molecular de Plantas, Centro Nacional de Biotecnologı ´ a-CSIC, Campus Universidad Auto ´ noma, 28049 Madrid, Spain Fax: +34 91 585 4506 Tel: +34 91 585 5429 E-mail: rsolano@cnb.csic.es (Received 7 November 2008, revised 3 February 2009, accepted 20 February 2009) doi:10.1111/j.1742-4658.2009.07194.x Jasmonic acid (JA) and its derivates, collectively known as jasmonates (JAs), are essential signalling molecules that coordinate the plant response to biotic and abiotic challenges, in addition to several developmental pro- cesses. The COI1 F-box and additional SCF modulators have long been known to have a crucial role in the JA-signalling pathway. Downstream JA-dependent transcriptional re-programming is regulated by a cascade of transcription factors and MYC2 plays a major role. Recently, JAZ family proteins have been identified as COI1 targets and repressors of MYC2, defining the ‘missing link’ in JA signalling. JA–Ile has been proposed to be the active form of the hormone, and COI1 is an essential component of the receptor complex. These recent discoveries have defined the core JA-signal- ling pathway as the module COI1 ⁄ JAZs ⁄ MYC2. Abbreviations ARF, auxin response factor; bHLH, basic helix-loop-helix; COR, coronatine; ERF, ethylene response factor; GA, gibberellin; IAA, indole-3- acetic acid; JA, jasmonic acid; Me-JA, methyl ester of JA; OPDA, 12-oxophytodienoic acid; PIF, phytochrome interacting factor; SCF, Skip ⁄ Cullin ⁄ F-box; TF, transcription factor. 4682 FEBS Journal 276 (2009) 4682–4692 ª 2009 The Authors Journal compilation ª 2009 FEBS Parallel genetic screens for JA-insensitive mutants identified jin1, carrying a mutation in the MYC2 gene, another key component of the JA-signalling pathway [10,13,14]. MYC2 encodes a basic helix-loop-helix (bHLH) transcription factor (TF) that recognizes the G-box and G-box variants in the promoter of its target genes and regulates different branches of the JA path- way [10,14–18]. MYC2 induces JA-mediated responses such as wounding, inhibition of root growth, JA bio- synthesis, oxidative stress adaptation and anthocyanin biosynthesis. In addition, MYC2 represses other JA-mediated responses such as tryptophan metabolism and defences against necrotrophic pathogens [10,14,17]. However, ethylene-response-factor 1 (ERF1) and other ERFs, such as ORA59, integrate JA and ethylene signals, and regulate some of the MYC2- modulated responses in an opposite fashion [10,19,20]. More recently, several independent groups have identified the JAZ family of repressors in Arabidopsis by genetic screens and microarray analyses [16,21,22]. JAZ proteins are direct targets of COI1 that are degraded by the 26S proteasome in response to the hormone. Furthermore, JAZ proteins also directly interact with MYC2 repressing its activity, and there- fore function as repressors of the JA pathway [16,23]. Discovery of the JAZ family led to the identification of the first core signalling module in the JA pathway: COI1–JAZs–MYC2 [3,16], which is the focus of this minireview. Moreover, the similarities between JA and other hormone-signalling pathways such as those of auxins, gibberellins or ethylene are also discussed. These similarities suggest a common strategy to trans- duce hormonal signals in plants, based on the regula- tion of protein stability by the ubiquitin–proteasome pathway. JA perception and the nature of the active hormone Despite multiple biochemical and genetic efforts, the molecular details of hormone perception have been utterly shielded until recently. COI1 is essential for all known JA-dependent responses and, intriguingly, the closest COI1 homologues among the  700 Arabidop- sis F-box proteins are the auxin receptors TIR1 ⁄ AFBs [24–26]. The critical role of COI1 in all JA responses and the acknowledged similarity between the JA and auxin pathways suggest that COI1 might be the long- sought JA receptor [16,27,28]. The identification of the JA receptor is intimately correlated to the nature of the ligand molecules. The JA biosynthetic pathway ends with the production of JA and the methyl ester of JA (Me-JA), long consid- ered the bioactive molecules [4,29–31]. Characteriza- tion of the JA-insensitive jar1 mutant identified JAR1 as an enzyme catalysing the conjugation of JA to amino acids (preferentially Ile) [32–35]. Although jar1 mutants are defective in some JA responses, these defects are complemented by external application of JA–Ile, revealing the biological relevance of this natu- Table 1. SCF and COP9 Arabidopsis mutants impaired in JA signalling. Mutant Gene Major phenotype Refs coi1 At2g39940, F-box component of the SCF E3 ubiquitine ligase complexes Reduced root growth inhibition and anthocyanin accumulation by JA and coronatine. Male sterile [5,7] axr1 At1g05180, RUB-activating enzyme E1 Reduced root growth inhibition by JA. Reduced expression of VSP, Thi1.2 and PDF1.2 upon JA treatment [12,94] eta3 ⁄ jai4 At4g11260 ⁄ SGT1b modulator of the SCF complex Reduced root growth inhibition by JA [9,10] fus6 ⁄ CSN1-11 At3g61140 ⁄ CSN1, subunit 1 of the COP9 complex involved in protein deneddylation Reduced root growth inhibition by JA. Reduced expression of PDF1.2 upon JA treatment [95] cul1 ⁄ axr6 At4g02570 ⁄ CULLIN1, cullin protein of the SCF complex Reduced root growth inhibition by JA [11,96] AtRBX1 RNAi At5g20570 ⁄ RBXA, ring-box 1-like protein Reduced root growth inhibition by JA. Reduced expression of VSP and AOS upon JA treatment [12,97] CSN5 RNAi At1g22820 ⁄ CSN5A, subunit of the COP9 complex involved in protein deneddylation Reduced root growth inhibition by JA. Reduced expression of VSP upon JA treatment [97] A. Chini et al. COI1/JAZs/MYC2: the core JA-signalling module FEBS Journal 276 (2009) 4682–4692 ª 2009 The Authors Journal compilation ª 2009 FEBS 4683 rally occurring JA derivative and suggesting that JA is not active per se [4,33–38]. Recent reports have shown that JA–Ile directly induces the interaction between COI1 and several JAZ proteins at physiological concentrations, whereas none of the tested precursors or intermediates, such as 12- oxophytodienoic acid (OPDA), Me-JA or JA, can promote the interaction [21,23,39] (S. Fonseca et al., unpublished results). Taken together, these results con- firm that JA–Ile has all the essential characteristics of a bioactive molecule. Direct JA–Ile and COR induction of the COI1 ⁄ JAZs interaction provides a framework to identify the JA receptor. The binding of radiolabelled COR by tomato cellular extracts requires COI1 [39]. Thus, extracts from null coi1 mutants failed to recover any radiolabelled COR. Similarly, a point mutation (L418F) in the COI1 region corresponding to the auxin-binding pocket of TIR1 decreases the recovery of radiolabelled COR [39]. In addition, JA–Ile and COR are recognized by the same receptor, because JA–Ile can compete with radiolabelled COR for bind- ing to the extract [39]. More recently, immunoprecipi- tated COI1 has been proved to interact with different JAZ proteins in a hormone-dependent manner, indi- cating that either COI1, or a protein co-purifying with COI1, is the COR ⁄ JA–Ile receptor (S. Fonseca et al., manuscript submitted). As expected for a hor- monal receptor, the COI1 ⁄ JAZs interaction is dose dependent, reversible and very quick. Moreover, the expression of COI1 and JAZ proteins in yeast is suffi- cient for hormone-dependent yeast responsiveness and growth [21,23] (S. Fonseca et al., unpublished results). In summary, several independent lines of evidence strongly support that COI1 or the COI1 ⁄ JAZ com- plex is the COR and JA–Ile receptor. However, direct binding between COI1 and the hormone has not been reported and the structural resolution of the COI1– hormone–JAZ complex is crucial to reveal the molec- ular details of the hormone perception. In addition to Ile, JAR1 can conjugate JA to other amino acids (Val, Leu, Ala, Phe, Met, Thr, Trp and Gln), although less efficiently [33]. Similar to JA–Ile, JA–Val, JA–Leu and JA–Ala are also naturally occur- ring molecules able to directly induce a COI1 ⁄ JAZ interaction in tomato cell extract and whose external application triggers specific JA-dependent plant responses [21,33,39]. In contrast to the bioactive JA– Ile, however, JA–Val, JA–Leu and JA–Ala fail to induce JA-dependent root growth inhibition in the Arabidopsis jar1 mutant, demonstrating that, at least in Arabidopsis, these JA–amino acid conjugates are not active as such, but require a functional JAR1 to acti- vate JA-dependent responses [33] (S. Fonseca et al., unpublished results). Therefore, in Arabidopsis, JA–Ile is the only bioactive JA identified to date and JAR1 is essential for producing this hormone. Of note, several jar1 alleles and knockout lines show a residual JA–Ile presence suggesting partial redundancy in the JAR1 function, as already shown in tobacco [33,34,40]. Despite its importance, JA–Ile is the first, but proba- bly not the only, bioactive JA. For example, Arabidop- sis opr3 mutants, unable to convert OPDA into JA, are deficient in several JA-regulated responses such as growth inhibition and fertility, but not in activating defence responses [41]. OPDA also induces the expres- sion of several JA-responsive genes, as well as a specific sub-set of JA-independent genes, confirming the ability of OPDA to trigger plant responses distinct to JA [42,43]. In addition, JA–Ile treatment of JAR4 ⁄ 6-silenced tobacco plants, deficient in JA–Ile produc- tion, is able to re-establish the natural resistance response to Manduca sexta. However, application of JA–Ile fails to restore the defence response in LOX3- silenced plants, lacking JA–Ile and other oxylipins [40]. These data suggest that other oxylipins, in addition to JA–Ile, are responsible for triggering JA-mediated defence responses and, therefore, the existence of addi- tional bioactive JAs can be expected. JAZ repressors: the JA-pathway hub JAZ proteins represent the molecular connection between COI1 and MYC2; the three proteins defining the core JA-signalling module. In Arabidopsis, the JAZ protein family consists of 12 members sharing two conserved motifs, ZIM and Jas. Loss of the Jas motif in JAI3 ⁄ JAZ3 (the jai3-1 mutant) causes dominant JA insensitivity, indicating the relevance of this motif for the regulation of this protein function [16]. Consis- tently, constitutive expression of truncated forms of JAZ1, JAZ3 and JAZ10 lacking the Jas motif also generates JA-insensitive plants [16,21,22]. In vivo deg- radation studies have shown that at least three JAZ proteins, JAZ1, JAZ3 and JAZ6, are degraded by the 26S proteasome in a COI1-dependent manner upon JA treatment. Yeast two-hybrid and pull-down assays showed that, in the presence of the hormone, COI1 physically interacts with JAZ1, JAZ3 and JAZ9 via their Jas motif in a dose-dependent manner, and that two positively charged amino acids within this motif are essential for the interaction [21,23,39] (S. Fonseca et al., manuscript submitted). Truncated JAZ deriva- tives (lacking the Jas motif) consistently lose this hor- mone-dependent binding to COI1 and are resistant to JA-induced degradation [16,21,23,39]. Therefore, deg- COI1/JAZs/MYC2: the core JA-signalling module A. Chini et al. 4684 FEBS Journal 276 (2009) 4682–4692 ª 2009 The Authors Journal compilation ª 2009 FEBS radation of JAZ proteins is essential to de-repress the JA pathway. Continuous repression of their TF targets by these degradation-resistant JAZ derivatives has been proposed to explain the mechanism by which they promote dominant JA insensitivity [21,23]. However, this explanation is unlikely because the Jas motif is also required for the interaction with MYC2 [16,23] (S. Fonseca et al., unpublished results). In contrast to COI1, the interaction of JAZ proteins with MYC2 does not depend on the presence of the hormone [16,23,39]. Therefore, both COI1 and MYC2 proteins seem to compete for interaction with the Jas motif, and the presence of the hormone determines the out- come of this competition [16]. Thus, under basal con- ditions, the Jas domain of JAZ proteins interacts with MYC2 and other transcription factors to repress the JA response. Increases in JA–Ile after stress would promote COI1 binding to the Jas domain of JAZ proteins, their consequent degradation and the release of MYC2 and other transcription factors involved in JA-induced gene expression [16]. Constitutive expression of the truncated version of JAZ3 prevents JA-dependent degradation of other JAZ proteins such as JAZ1 and JAZ9, suggesting a possible alternative explanation for the dominant JA- insensitive phenotype promoted by truncated JAZs. The mutant JAZ3 protein (retaining the ZIM domain but lacking the Jas motif) was proposed to partially inactivate COI1, therefore preventing the degradation of additional JAZ proteins that continue to repress their TF targets [16]. Crystal structure analyses of COI–JAZ complexes, identification of new JAZ targets and characterization of the ZIM domain function will help to clarify this issue. Consistent with the interaction between JAZ3 and MYC2, microarray experiments have shown that genes containing MYC2 DNA-binding sites (the G- and T ⁄ G-boxes) in their promoters and positively regulated by MYC2 are deregulated in jai3-1 mutants [16]. Therefore, the genetic and molecular data, together with transcriptional profiling, pinpointed JAZ proteins as the long-postulated repressors targeted for protea- some-degradation by SCF COI1 to activate the JA-regu- lated responses. To date, only MYC2 has been identified as a target of JAZ repressors. However, MYC2 does not regulate all JA-dependent responses, and therefore, JAZ proteins are expected to target additional TFs. MYC2 belongs to the large family of bHLH transcription factors (> 160 in Arabidopsis) involved in many different processes, from stress responses to development [44,45]. MYC2 constitutes a master switch regulating abscisic acid and JA ⁄ ethylene responses, as well as blue-light-dependent photomorphogenesis [10,17,46,47]. It is tempting to speculate that other bHLHs, structurally related to MYC2, may also be targeted by JAZ proteins to fine- tune specific downstream responses. In the recent years, additional TFs belonging to different families such as ERF (ERF1, ORA59, AtERF1, AtERF2, and AtERF4), MYB (MYB21 and MYB24) and WRKY (WRKY70, WRKY18) have also been involved in JA signalling [19,20,48–51]. Thus, these TFs and their clos- est homologues represent the best candidates for JAZ targets to date [17]. However, some of these TFs may be indirectly modulated by MYC2 via a secondary regulatory cascade, such as the case of the NAC transcription factors ANAC019 and ANAC055, whose expression is induced by JA in a MYC2-dependent manner [52]. JAZ family: redundancy and specificity Functional redundancy among JAZ family members has been inferred from the lack of JA-related pheno- types in individual knockout jaz mutants, with the exception of JAZ10 [21,22]. Supporting this redun- dancy, all the COI1-interacting JAZ proteins also inter- act with MYC2 (i.e. JAZ1, JAZ3 and JAZ9) [16,23]. Moreover, phylogenetic analyses of the JAZ gene fam- ily, the number and position of their introns, as well as their presence in duplicated chromosome segments, show the existence of well-defined JAZ clades [16,21,53]. Therefore, although the implication of the JAZ family in regulation of the JA pathway is clear, double or multiple mutants are required to demonstrate the involvement of individual JAZ genes in this path- way, and to clarify their regulation of particular JA responses. Despite their likely redundant function, some speci- ficity in the role of individual JAZ proteins can be expected. In fact, different JAs, precursors or mimetics induce specific, as well as overlapping, responses in plants [41–43,54–58]. A mechanistic explanation for these specific responses in particular tissues may be based on the promotion of specific COI1 ⁄ JAZ com- plexes by different bioactive JAs, combined with the fact that different JAZ proteins may target specific TFs, and with the tissue specificity of JAZs and⁄ or their TF targets. Thus, specific JAZ degradation in response to a particular jasmonate would determine the activation of a specific module (COI1 ⁄ JAZ ⁄ TF) and subsequent tissue-specific JA responses [16,21]. Although data supporting this hypothesis are scarce, examples can be found in the closely related auxin pathway. Thus, the SCF-mediated degradation of A. Chini et al. COI1/JAZs/MYC2: the core JA-signalling module FEBS Journal 276 (2009) 4682–4692 ª 2009 The Authors Journal compilation ª 2009 FEBS 4685 different Aux ⁄ indole-3-acetic acid (IAA) repressors in response to specific auxins exhibits different kinet- ics [59,60]. Moreover, specificity in the TF targets of Aux ⁄ IAA genes has also been reported [61–64]. Finally, tissue-specific expression of different Aux ⁄ IAA and ⁄ or their TF targets has been described [62,65,66]. Similar to the case of the auxin pathway, JAZ profiling analyses show very diverse tissue- and stage- specific expressions (Fig. 1) [67]. Interestingly, similar spatial and temporal regulation is also emerging for the production and accumulation of JA and its deri- vates. Recent metabolite profiling of Arabidopsis plants showed very dynamic spatial and temporal changes in the synthesis of JA and its hydroxylated derivates in response to wounding [68]. In addition, a comprehen- sive ‘jasmonate ⁄ oxylipin signature’ analysis, measuring JA, its precursors and derivates in several plant species, confirmed their differential accumulation in specific organs and stages [57,69]. Oxylipin inactivation by hydroxylation and sulfonation may also contribute to the establishment of these dynamic spatial and temporal patterns of jasmonate activity [68]. Moreover, an elegant genetic approach has also confirmed this temporal regulatory mechanism by identifying the DGL gene, a homologue of DAD1, encoding a chloro- plastic lipase [70,71]. Both enzymes catalyse the pro- duction of linolenic acid, the first, critical step in JA biosynthesis. Although DAD1 and DGL share partial functional redundancy, their differential induction kinetics and organ-specific expression (DAD1 in flow- ers, DGL in leaves) provides them with independent, temporally and spatially separated roles [70]. The tis- sue- and stage-specific expression of JAZ genes and their TF targets, combined with the spatially and temporally regulated biosynthesis of bioactive JAs may generate an extraordinary rich signalling repertoire able to modulate very different JA responses despite the likely partial JAZ redundancy. The characterization of lines knocked-out in com- plete JAZ clades, combined with a precise study of JAZ expression patterns and the comprehensive analy- ses of COI1 interaction with all JAZs in the presence of different bioactive JAs, is required to elucidate indi- vidual JAZ function. Evolutionary success of SCF function Recent advances in hormone signalling have uncovered a common strategy in which SCF protein degradation complexes are central for the transmission of hormonal signals in plants (Fig. 2). In the case of auxins, IAA and related molecules serve as ‘molecular glue’ bring- ing together the F-box protein TIR1 ⁄ AFB and the JAZ1 Stage III Stage II Dry seed Dry seed Dry seed Dry seed Stage I Stage III Stage II Stage I Stage III Stage II Stage I Stage III Stage II Stage I JAZ3 JAZ9 JAZ10 Fig. 1. Tissue-specific expression of repre- sentative JAZ genes. The expression of JAZ1, JAZ3, JAZ9 and JAZ10 genes is rep- resented as in the Bio-Array Resource (BAR) database (http://bbc.botany.utoronto.ca/) [67]. The gene expression in root cells types, flowers and the whole plant show significant tissue-specific differences. COI1/JAZs/MYC2: the core JA-signalling module A. Chini et al. 4686 FEBS Journal 276 (2009) 4682–4692 ª 2009 The Authors Journal compilation ª 2009 FEBS Aux ⁄ IAA proteins, resulting in the degradation of Aux ⁄ IAA repressors, which in turn activate the auxin response by de-repression of auxin response factor (ARF) transcriptional activators [24,26,72]. Similarly, JA–Ile may also serve as ‘molecular glue’ to promote the interaction between COI1 and the JAZ proteins, resulting in JAZ degradation and the consequent de-repression of JA transcriptional activators such as MYC2. Both Aux ⁄ IAA and JAZ are rapidly induced by auxins and JA, respectively, and their induction depends on their respective transcriptional activator targets (ARFs and MYC2, respectively) providing a negative regulatory loop that allows to switch off the response [16,21,73]. Gibberellin (GA) signalling may also fit into this common strategy, although some variations are evi- dent. Unlike the F-boxes, TIR1 and COI1, the GA receptor, GID1, has similarity with a hormone-sensi- tive lipase [74]. GA binding to GID1 is required for the interaction of the receptor with DELLA proteins, transcriptional repressors of GA responses [75–79]. In turn, GID1–DELLA interaction promotes the recogni- tion of DELLA by the F-box SLY1 resulting in the degradation of DELLA repressors and the de-repres- sion of transcriptional activators of GA-responsive genes like PIF3 and PIF4 [80–82], which belong to the bHLH family, like MYC2. Interestingly, recent findings have shown that a constitutively active domi- nant-negative DELLA mutation, gai, enhances the induction of JA-responsive genes, whereas a quadruple DELLA knockout mutant, which lacks four of the five Arabidopsis DELLA proteins, was partially insensitive to JA [83]. This finding points to a possible role for DELLA proteins in GA ⁄ JA signalling cross-talk, although the molecular bases remain unknown. Auxin signalling Auxins SCF SCF TIR1 TIR1 Aux/IAA Aux/IAA ARFs ARFs Auxin responsive genes 26S proteasome Aux/IAA Aux/IAA JA signalling AB MYC2 MYC2 JA responsive genes Other TFs? 26S proteasome SCF SCF COI1 COI1 J A Z J A Z ? JA-Ile JAZ JAZ Ethylene signalling EIN3 EIN3 Ethylene responsive genes 26S proteasome Ethylene SCF SCF EBF EBF EIN3 EIN3 PIFs PIFs GA responsive genes 26S proteasome GA signalling GA SCF SCF SLY1 SLY1 DELLA DELLA GID1 GID1 DELLA DELLA CD Fig. 2. SCF-dependent proteasome degra- dation represents a common strategy in plant hormone signalling. (A) In an un- induced situation, the JAZ proteins repress MYC2 and additional unknown transcription factors. Upon JA–Ile perception, JAZ repres- sors are targeted for proteasome degrada- tion by SCF COI1 , therefore liberating MYC2 and activating the JA responses. (B) In the same way, Aux ⁄ IAA inhibits the ARF tran- scriptional modulators in the absence of auxin. Increased auxin concentrations pro- mote SCF TIR1 -mediated degradation of Aux ⁄ IAAs, which in turn de-repress ARF transcription factors and auxin responses. (C) Similarly, at basal GA levels, the DELLA repressors block phytochrome interacting factors (PIFs) and additional transcription factors. Following hormone perception, GID1 mediates the recognition and degrada- tion of the DELLA repressors by SCF SLY1 , therefore activating PIF transcriptional mod- ulators and downstream GA responses. (D) The ethylene pathway is the most diver- gent situation because, in the absence of the hormone, the transcriptional activator EIN3 is constitutively degraded in a SCF EBF1 ⁄ 2 -dependent manner. Upon ethyl- ene perception, EIN3 is stabilized, thus activating ethylene responses. These models were adapted from Chico et al. [3]. A. Chini et al. COI1/JAZs/MYC2: the core JA-signalling module FEBS Journal 276 (2009) 4682–4692 ª 2009 The Authors Journal compilation ª 2009 FEBS 4687 A central role for SCF-mediated degradation in eth- ylene signalling is also well documented [84,85]. The ethylene pathway represents the most divergent situa- tion because a transcriptional activator, EIN3, is constitutively degraded in a proteasome-dependent manner by direct interaction with two F-box proteins, EBF1 and EBF2 [86,87]. Upon ethylene perception, EIN3 is stabilized, thus activating ethylene responses. More recently, identification of the novel plant branching hormones, strigolactones, has been reported [88,89]. Interestingly, one of the key proteins regulating the branching process is again an F-box, MAX2, which has been proposed to mediate the degradation of a repressor in response to the branching hormone [90–92]. If this is the case, the strigolactone pathway may be very similar to that of auxins, JA and GAs, providing further evidence of the extraordinary success of the ubiquitin ⁄ proteasome pathway as a strategic mechanism in plant hormone sensing and signalling. Evolutionarily, auxin, JA, GA and ethylene percep- tion and signalling pathways would constitute subtle turns in a unique and highly conserved plant strategy [3,84,90,93]. This mechanism may provide potential nodes of interaction between different signalling mole- cules explaining the extraordinary plasticity intrinsi- cally associated with these pathways. On/off model and future perspectives The discovery and characterization of the JAZ proteins describes the first complete JA-signalling module (COI ⁄ JAZ ⁄ MYC2) that helps us understand how JA responses are turned on and off (Fig. 2). Upon hor- monal perception, JAZ repressors are targeted by SCF COI1 for degradation, de-repressing MYC2 and probably additional TFs. These transcriptional modu- lators activate downstream JA-mediated responses as well as the expression of most JAZ genes, therefore re-establishing the MYC2 ⁄ JAZ repressor complexes [16]. This simple negative feedback loop represents an efficient regulatory mechanism providing an appropri- ate response to JA and its subsequent autoregulated deactivation (Fig. 2). Although the discovery of JAZ repressors has paved the way for understanding the core module responsible for JA signalling, new questions arise that need to be addressed if we are to fully understand the fine-tuning of this core module. As described above, the nature of the active plant hormone is essential to fully appreciate the details of JA perception. JA–Ile is the only bioac- tive JA identified to date, although the existence of additional bioactive molecules may be expected. The specific COI1 ⁄ JAZ interaction provides the molecular tools with which to test the direct activity of several JAs. An additional layer of regulation in JA signalling may be the intracellular transport of the hormone. JAZ repressors, and probably COI1, are nuclear pro- teins and the COI1-dependent degradation of JAZ proteins triggered by the hormone also occurs in the nucleus. However, it remains unknown whether the active molecules diffuse or are actively transferred into the nucleus. Finally, the tissue and temporal specificity of JAZ genes expression, in combination with their likely repression of different TFs, may account for the acti- vation of specific JA responses. Further analyses of the mechanisms by which JA-signalling modules are temporally and spatially distributed will result in a comprehensive understanding of the complexity of JA-mediated plant responses. Acknowledgements We thank J.M. Chico and S. Fonseca for critical reading of the manuscript. Work in RS’s lab is supported by funding from the Ministerio de Educacio ´ n y Ciencia of Spain, the Comunidad de Madrid and European Com- mission. AC was supported by the Juan de la Cierva Programme and an EMBO Long-term Fellowship. Note added in proof Very recently, two manuscripts have reported that the ZIM domain acts as a protein–protein interaction domain mediating homo- and heteromeric interactions between JAZ proteins (Chung & Howe, 2009 [98,99]). Chung & Howe also propose that JAZ splice variants serve to attenuate signal output in the presence of JA via protein–protein interaction through the ZIM domain. These findings provide new clues to under- stand the dominant JA insensitivity conferred by the JAZDJas proteins. References 1 Balbi V & Devoto A (2008) Jasmonate signalling network in Arabidopsis thaliana: crucial regulatory nodes and new physiological scenarios. New Phytol 177, 301–318. 2 Browse J & Howe GA (2008) New weapons and a rapid response against insect attack. 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MINIREVIEW Plant oxylipins: COI1/JAZs/MYC2 as the core jasmonic acid-signalling module Andrea Chini, Marta Boter and Roberto. function as repressors of the JA pathway [16,23]. Discovery of the JAZ family led to the identification of the first core signalling module in the JA pathway: COI1–JAZs–MYC2