Jasmonate signaling: a conserved mechanism of hormone sensing
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).
References (60)
Jasmonate: an oxylipin signal with many roles in plants
Vitam Horm
(2005)- et al.
Systemic signaling in the wound response
Curr Opin Plant Biol
(2005) JAZing up jasmonate signaling
Trends Plant Sci
(2008)Jasmonate perception: characterization of COI1 mutants provides the first clues
Trends Plant Sci
(1998)- et al.
Molecular players regulating the jasmonate signalling network
Curr Opin Plant Biol
(2005) - et al.
The GH3 family in plants: genome wide analysis in rice and evolutionary history based on EST analysis
Gene
(2006) - et al.
The Arabidopsis thaliana Jasmonate insensitive 1 gene is required for suppression of salicylic acid-dependent defenses during infection by Pseudomonas syringae
Mol Plant Microbe Interact
(2006) - et al.
Cooperation and functional diversification of two closely related galactolipase genes for jasmonate biosynthesis
Dev Cell
(2008) - et al.
Tissue-specific oxylipin signature of tomato flowers: allene oxide cyclase is highly expressed in distinct flower organs and vascular bundles
Plant J
(2000) - et al.
Plant immunity to insect herbivores
Annu Rev Plant Biol
(2008)
Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens
Annu Rev Phytopathol
Update on jasmonate signaling: new weapons and a rapid response against insect attack
Plant Physiol
Jasmonate signalling network in Arabidopsis thaliana: crucial regulatory nodes and new physiological scenarios
New Phytol
Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development
Ann Bot (Lond)
Biosynthesis and metabolism of jasmonates
J Plant Growth Regul
Jasmonate signaling pathway
Sci STKE
Jasmonate signaling: toward an integrated view
Plant Physiol
COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility
Science
The SCFCOI1 ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis
Plant Cell
COI1 links jasmonate signalling and fertility to the SCF ubiquitin–ligase complex in Arabidopsis
Plant J
JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling
Nature
The JAZ family of repressors is the missing link in jasmonate signalling
Nature
A downstream mediator in the growth repression limb of the jasmonate pathway
Plant Cell
The tify family previously known as ZIM
Trends Plant Sci
Arabidopsis ZIM, a plant-specific GATA factor, can function as a transcriptional activator
Biosci Biotechnol Biochem
PEAPOD regulates lamina size and curvature in Arabidopsis
Proc Natl Acad Sci U S A
Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling
Plant Cell
Jasmonate-insensitive1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis
Plant Cell
MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis
Plant Cell
The mitogen-activated protein kinase cascade MKK3-MPK6 is an important part of the jasmonate signal transduction pathway in Arabidopsis
Plant Cell
Cited by (293)
Interplay of phytohormone signaling with aluminum and drought-stress resistance mechanisms: An integrated perspective amidst climate change
2024, Environmental and Experimental BotanyCOI1 dependent jasmonic acid signalling positively modulates ROS scavenging system in transgenic hairy root culture of tomato
2024, Plant Physiology and BiochemistryDUF4057 containing express-protein negatively regulates the drought responses in rice
2023, Environmental and Experimental Botany