Jasmonate and related signalling compounds have a crucial role in both host immunity and development in plants, but the molecular details of the signalling mechanism are poorly understood. Here we identify members of the jasmonate ZIM-domain (JAZ) protein family as key regulators of jasmonate signalling. JAZ1 protein acts to repress transcription of jasmonate-responsive genes. Jasmonate treatment causes JAZ1 degradation and this degradation is dependent on activities of the SCF(COI1) ubiquitin ligase and the 26S proteasome. Furthermore, the jasmonoyl-isoleucine (JA-Ile) conjugate, but not other jasmonate-derivatives such as jasmonate, 12-oxo-phytodienoic acid, or methyl-jasmonate, promotes physical interaction between COI1 and JAZ1 proteins in the absence of other plant proteins. Our results suggest a model in which jasmonate ligands promote the binding of the SCF(COI1) ubiquitin ligase to and subsequent degradation of the JAZ1 repressor protein, and implicate the SCF(COI1)-JAZ1 protein complex as a site of perception of the plant hormone JA-Ile.
Jasmonates (JAs) are a family of plant hormones that regulate plant growth, development, and responses to stress. The F-box protein CORONATINE-INSENSITIVE 1 (COI1) mediates JA signaling by promoting hormone-dependent ubiquitination and degradation of transcriptional repressor JAZ proteins. Despite its importance, the mechanism of JA perception remains unclear. Here we present structural and pharmacological data to show that the true JA receptor is a complex of both COI1 and JAZ. COI1 contains an open pocket that recognizes the bioactive hormone, (3R,7S)-jasmonoyl-L-isoleucine (JA-Ile), with high specificity. High-affinity hormone binding requires a bipartite JAZ degron sequence consisting of a conserved α-helix for COI1 docking and a loop region to trap the hormone in its binding pocket. In addition, we identify a third critical component of the JA co-receptor complex, inositol pentakisphosphate, which interacts with both COI1 and JAZ adjacent to the ligand. Our results unravel the mechanism of JA perception and highlight the ability of F-box proteins to evolve as multi-component signaling hubs.
Jasmonic acid (JA) and its precursor 12-oxophytodienoic acid (OPDA) act as plant growth regulators and mediate responses to environmental cues. To investigate the role of these oxylipins in anther and pollen development, we characterized a T-DNA-tagged, male-sterile mutant of Arabidopsis, opr3. The opr3 mutant plants are sterile but can be rendered fertile by exogenous JA but not by OPDA. Cloning of the mutant locus indicates that it encodes an isozyme of 12-oxophytodienoate reductase, designated OPR3. All of the defects in opr3 are alleviated by transformation of the mutant with an OPR3 cDNA. Our results indicate that JA and not OPDA is the signaling molecule that induces and coordinates the elongation of the anther filament, the opening of the stomium at anthesis, and the production of viable pollen. Just as importantly, our data demonstrate that OPR3 is the only isoform of OPR capable of reducing the correct stereoisomer of OPDA to produce JA required for male gametophyte development.
The oxylipin jasmonate (JA) regulates many aspects of growth, development, and environmental responses in plants, particularly defense responses against herbivores and necrotrophic pathogens. Mutants of Arabidopsis helped researchers define the biochemical pathway for synthesis of jasmonoyl-isoleucine (JA-Ile), the active form of JA hormone, and demonstrated that JA is required for plant survival of insect and pathogen attacks and for plant fertility. Transcriptional profiling led to the discovery of the JASMONATE ZIM-DOMAIN (JAZ) proteins, which are repressors of JA signaling. JA-Ile relieves repression by promoting binding of the JAZ proteins to the F-box protein CORONATINE INSENSITIVE1 (COI1) and their subsequent degradation by the ubiquitination/26S-proteasome pathway. Although we now have a much better understanding of the molecular mechanism of JA action, many questions remain. Experimental answers to these questions will expand our knowledge of oxylipin signaling in plants and animals and will also provide new tools for efforts to improve crop protection and reproductive performance.
The Arabidopsis opr3 mutant is defective in the isoform of 12-oxophytodienoate (OPDA) reductase required for jasmonic acid (JA) biosynthesis. Oxylipin signatures of wounded opr3 leaves revealed the absence of detectable 3R,7S-JA as well as altered levels of its cyclopentenone precursors OPDA and dinor OPDA. In contrast to JA-insensitive coi1 plants and to the fad3 fad7 fad8 mutant lacking the fatty acid precursors of JA synthesis, opr3 plants exhibited strong resistance to the dipteran Bradysia impatiens and the fungus Alternaria brassicicola. Analysis of transcript profiles in opr3 showed the wound induction of genes previously known to be JA-dependent, suggesting that cyclopentenones could fulfill some JA roles in vivo. Treating opr3 plants with exogenous OPDA powerfully up-regulated several genes and disclosed two distinct downstream signal pathways, one through COI1, the other via an electrophile effect of the cyclopentenones. We conclude that the jasmonate family cyclopentenone OPDA (most likely together with dinor OPDA) regulates gene expression in concert with JA to fine-tune the expression of defense genes. More generally, resistance to insect and fungal attack can be observed in the absence of JA.OPDA reductase ͉ opr3 ͉ Arabidopsis ͉ insect A major objective in plant biology is to develop an integrated understanding of how plants survive in their environment and reproduce. Although it has become clear in the last decade that jasmonic acid (JA) is a key regulator in the development, physiology, and defense of plants, the complexity of the signaling network in which JA evolves is just emerging (1). JA is involved in carbon partitioning (2), in mechanotransduction (3), and the ability of plants to synthesize and perceive JA is absolutely essential for the correct development and release of pollen in Arabidopsis (4-7). Highlighting the regulatory importance of JA, a JA-responsive transcription factor, ORCA3, first found in Catharanthus, provides an important link between primary and secondary metabolism (8). There is also strong evidence supporting a central role of JA in plant defense. Exogenous JA powerfully regulates the expression of many defense genes in plants, and its in vivo production and perception seem to be of vital importance in mounting successful defense against insect attackers (9-11). Together with ethylene, JA also plays a crucial role in defense against necrotrophic fungi (12-14) and in induced systemic resistance in response to nonpathogenic rhizobacteria (15). Broader roles of JA in plant stress responses are likely; it is known that the JA biosynthesis pathway is important in gene activation subsequent to UV damage in plants (16), and JA has been implicated in some responses to water stress (17).The biosynthesis of JA occurs through the octadecanoid pathway (18,19) and is initiated by the addition of molecular oxygen to linolenic acid (18:3) to form 13-hydroperoxylinolenic acid (13-HPOTrE). This fatty acid hydroperoxide is then dehydrated by allene oxide synthase (AOS) and cyclized by ...
Polyunsaturated fatty acids (PUFAs) are essential membrane components in higher eukaryotes and are the precursors of many lipid-derived signaling molecules. Here, pathways for PUFA synthesis are described that do not require desaturation and elongation of saturated fatty acids. These pathways are catalyzed by polyketide synthases (PKSs) that are distinct from previously recognized PKSs in both structure and mechanism. Generation of cis double bonds probably involves position-specific isomerases; such enzymes might be useful in the production of new families of antibiotics. It is likely that PUFA synthesis in cold marine ecosystems is accomplished in part by these PKS enzymes.
The signaling pathways that allow plants to mount defenses against chewing insects are known to be complex. To investigate the role of jasmonate in wound signaling in Arabidopsis and to test whether parallel or redundant pathways exist for insect defense, we have studied a mutant (fad3-2 fad7-2 fad8) that is deficient in the jasmonate precursor linolenic acid. Mutant plants contained negligible levels of jasmonate and showed extremely high mortality (Ϸ80%) from attack by larvae of a common saprophagous fungal gnat, Bradysia impatiens (Diptera: Sciaridae), even though neighboring wild-type plants were largely unaffected. Application of exogenous methyl jasmonate substantially protected the mutant plants and reduced mortality to Ϸ12%. These experiments precisely define the role of jasmonate as being essential for the induction of biologically effective defense in this plant-insect interaction. The transcripts of three wound-responsive genes were shown not to be induced by wounding of mutant plants but the same transcripts could be induced by application of methyl jasmonate. By contrast, measurements of transcript levels for a gene encoding glutathione S-transferase demonstrated that wound induction of this gene is independent of jasmonate synthesis. These results indicate that the mutant will be a good genetic model for testing the practical effectiveness of candidate defense genes.
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