Jasmonate signaling: a conserved mechanism of hormone sensing

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The lipid-derived hormone jasmonate (JA) regulates diverse aspects of plant immunity and development. Among the central components of the JA signaling cascade are the E3 ubiquitin ligase SCFCOI1 and Jasmonate ZIM-domain (JAZ) proteins that repress transcription of JA-responsive genes. Recent studies provide evidence that amino acid-conjugated forms of JA initiate signal transduction upon formation of a coronatine-insensitive1 (COI1)–JA–JAZ ternary complex in which JAZs are ubiquitinated and subsequently degraded. Coronatine, a virulence factor produced by the plant pathogen Pseudomonas syringae, is a potent agonist of this hormone receptor system. Coronatine-induced targeting of JAZs to COI1 obstructs host immune responses to P. syrinage, providing a striking example of how pathogens exploit hormone signaling pathways in the host to promote disease. These findings, together with homology between COI1 and the auxin receptor, TIR1, extend the paradigm of F-box proteins as intracellular sensors of small molecules, and suggest a common evolutionary origin of the auxin and JA response pathways.

Introduction

The plant hormone jasmonate (JA) regulates diverse aspects of plant growth, development, and immunity. This lipid-derived signal and its bioactive derivatives (collectively referred to as JAs) play a critical role in controlling defense responses to an extraordinary range of biotic aggressors, most notably arthropod herbivores and necrotrophic pathogens [1, 2, 3]. Other processes that depend on JA signaling include responses to UV radiation and ozone and, depending on the plant species, male and female reproductive development [4]. In general, JA promotes defense and reproduction while inhibiting growth-related processes such as cell division and photosynthesis. These contrasting activities of JA imply a broader role for the hormone in regulating the balance between growth- and defense-related processes, thereby optimizing plant fitness in rapidly changing environments.

A combination of genetic, molecular, and biochemical analyses indicates that the core signal transduction chain linking JA synthesis to hormone-induced changes in gene expression consists of a quartet of interacting players: a JA signal, the SCF-type E3 ubiquitin ligase SCFCOI1, jasmonate ZIM-domain (JAZ) repressor proteins that are targeted by SCFCOI1 for degradation by the ubiquitin/26S proteasome pathway, and transcription factors (TFs) that positively regulate the expression of JA-responsive genes (Figure 1). Several major advances in the identification of these players, and the way in which they harmonize, have been reported in the past year. Here, we review this progress and highlight knowledge gaps that remain to be filled. Although we keep to the general theme of biotic interactions by discussing these topics in the context of plant immunity, a common mechanism of JA action likely accounts for most JA-signaled processes, including developmental responses. Readers are referred to several recent review articles for additional information on JA signaling and other aspects of JA biology [4, 5, 6, 7, 8, 9, 10, 11].

Section snippets

All that JAZ: orchestrating four-part harmony

A decade ago, identification of coronatine-insensitive1 (COI1) as an F-box protein led to the idea that negative regulators of JA signaling are subject to ubiquitin-dependent turnover in response to a JA signal [12, 13]. Subsequent biochemical and genetic studies showed that COI1 associates with other proteins of the SCF complex, including ASK1, RBX1, and CUL1, and that these components are important for JA-signaled responses [14, 15, 16]. A major breakthrough in understanding how COI1

A COI weapon of JAZ destruction

The switch between restrained and active states of JA-responsive gene expression is triggered by hormone-induced proteolysis of JAZs via the SCFCOI1/ubiquitin/26S proteasome pathway. This transition is initiated in response to biotic stress or other cues that result in JA accumulation (Figure 1). Two key pieces of experimental evidence support this view. First, JA stimulates turnover of JAZ-reporter fusion proteins in planta by a mechanism that requires COI1 and the 26S proteasome [17••, 18••].

Bioactive JAs: activation by conjugation

Newly synthesized jasmonic acid is subject to various enzymatic modifications that give rise to a plethora of JA derivatives [3, 6, 8]. An important challenge in the field of JA signal transduction is to identify the spectrum of JAs that directly promote COI1–JAZ interactions (Box 1). Cell-free and yeast-based assays showed that COI1 binding to certain JAZs is stimulated by jasmonoyl-isoleucine (JA-Ile) and structurally related JA-amino acid conjugates (e.g. JA-Val) [17••, 29•, 31••]. In light

The jasmonate receptor: here come those TIRs again

The emerging view of JA signaling (Figure 1) bears striking similarity to the mechanism of auxin action. It now appears that the functions of COI1, JAZ, and MYC2 in JA signaling are analogous to the core components of the auxin signaling pathway, namely the F-box protein TIR1 (and TIRl-like proteins), Aux/IAA repressor proteins, and auxin response factors, respectively. Sequence homology between COI1 and TIR1 implies a conserved role for these F-box proteins in signal transduction and,

Conclusions and future perspectives

Major strides toward elucidating the molecular mechanism of JA action have been reported in the past year. These advances include the discovery of JAZ proteins as substrates for SCFCOI1 and the identification of COI1 as a component of the JA perception machinery. This work extends the paradigm [50••] of F-box proteins as intracellular receptors for small molecules that regulate fundamental processes in plants. This new view of JA signal transduction frames several key questions that remain to

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank Ning Zheng for helpful comments on the manuscript, Ivo Feussner for sharing unpublished results, and Marlene Cameron for assistance in the preparation of figures. This work was supported by grants from the National Institutes of Health (R01GM57795) and the U.S. Department of Energy (DE-FG02-91ER20021).

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