Oxylipin Signaling: A Distinct Role for the Jasmonic Acid Precursor cis-(+)-12-Oxo-Phytodienoic Acid (cis-OPDA)

Dave, Anuja; Graham, Ian A.

doi:10.3389/fpls.2012.00042

Cited by 167 publications

(150 citation statements)

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“…A combination of genetics and feeding experiments has demonstrated that 12-OPDA interacts with ABA, inhibits seed germination, and increases ABA INSENSITIVE5 protein (Dave et al, 2011;Dave and Graham, 2012). These results, collectively, further highlight the importance of fine-tuning of jasmonate signatures in response to environmental and developmental signals and signify the stimulusdependent balance in levels of plant hormones and, by extension, their interactions.…”

Section: Discussionmentioning

confidence: 77%

Functional Convergence of Oxylipin and Abscisic Acid Pathways Controls Stomatal Closure in Response to Drought

et al. 2014

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Membranes are primary sites of perception of environmental stimuli. Polyunsaturated fatty acids are major structural constituents of membranes that also function as modulators of a multitude of signal transduction pathways evoked by environmental stimuli. Different stresses induce production of a distinct blend of oxygenated polyunsaturated fatty acids, "oxylipins." We employed three Arabidopsis (Arabidopsis thaliana) ecotypes to examine the oxylipin signature in response to specific stresses and determined that wounding and drought differentially alter oxylipin profiles, particularly the allene oxide synthase branch of the oxylipin pathway, responsible for production of jasmonic acid (JA) and its precursor 12-oxo-phytodienoic acid (12-OPDA). Specifically, wounding induced both 12-OPDA and JA levels, whereas drought induced only the precursor 12-OPDA. Levels of the classical stress phytohormone abscisic acid (ABA) were also mainly enhanced by drought and little by wounding. To explore the role of 12-OPDA in plant drought responses, we generated a range of transgenic lines and exploited the existing mutant plants that differ in their levels of stress-inducible 12-OPDA but display similar ABA levels. The plants producing higher 12-OPDA levels exhibited enhanced drought tolerance and reduced stomatal aperture. Furthermore, exogenously applied ABA and 12-OPDA, individually or combined, promote stomatal closure of ABA and allene oxide synthase biosynthetic mutants, albeit most effectively when combined. Using tomato (Solanum lycopersicum) and Brassica napus verified the potency of this combination in inducing stomatal closure in plants other than Arabidopsis. These data have identified drought as a stress signal that uncouples the conversion of 12-OPDA to JA and have revealed 12-OPDA as a drought-responsive regulator of stomatal closure functioning most effectively together with ABA.

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Section: Discussionmentioning

confidence: 77%

Functional Convergence of Oxylipin and Abscisic Acid Pathways Controls Stomatal Closure in Response to Drought

et al. 2014

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“…Given that cyclopentenones and cyclopentanones can have distinct signaling properties, we first investigated the potential for 10-OPEAmediated transcriptional regulation using the Affymetrix GeneChip maize genome array (7,12,16). Treatment with 10-OPEA after 90 min resulted in 55 genes with a twofold or greater change in probe intensity at 95% confidence.…”

Section: Resultsmentioning

confidence: 99%

Maize death acids, 9-lipoxygenase–derived cyclopente(a)nones, display activity as cytotoxic phytoalexins and transcriptional mediators

Christensen

Huffaker

Kaplan

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

145

125

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Plant damage promotes the interaction of lipoxygenases (LOXs) with fatty acids yielding 9-hydroperoxides, 13-hydroperoxides, and complex arrays of oxylipins. The action of 13-LOX on linolenic acid enables production of 12-oxo-phytodienoic acid (12-OPDA) and its downstream products, termed “jasmonates.” As signals, jasmonates have related yet distinct roles in the regulation of plant resistance against insect and pathogen attack. A similar pathway involving 9-LOX activity on linolenic and linoleic acid leads to the 12-OPDA positional isomer, 10-oxo-11-phytodienoic acid (10-OPDA) and 10-oxo-11-phytoenoic acid (10-OPEA), respectively; however, physiological roles for 9-LOX cyclopentenones have remained unclear. In developing maize (Zea mays) leaves, southern leaf blight (Cochliobolus heterostrophus) infection results in dying necrotic tissue and the localized accumulation of 10-OPEA, 10-OPDA, and a series of related 14- and 12-carbon metabolites, collectively termed “death acids.” 10-OPEA accumulation becomes wound inducible within fungal-infected tissues and at physiologically relevant concentrations acts as a phytoalexin by suppressing the growth of fungi and herbivores including Aspergillus flavus, Fusarium verticillioides, and Helicoverpa zea. Unlike previously established maize phytoalexins, 10-OPEA and 10-OPDA display significant phytotoxicity. Both 12-OPDA and 10-OPEA promote the transcription of defense genes encoding glutathione S transferases, cytochrome P450s, and pathogenesis-related proteins. In contrast, 10-OPEA only weakly promotes the accumulation of multiple protease inhibitor transcripts. Consistent with a role in dying tissue, 10-OPEA application promotes cysteine protease activation and cell death, which is inhibited by overexpression of the cysteine protease inhibitor maize cystatin-9. Unlike jasmonates, functions for 10-OPEA and associated death acids are consistent with specialized roles in local defense reactions.

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“…The first specific step in their biosynthesis is catalyzed by AOC that forms enantiopure cis(+)-OPDA, the first cyclic bioactive signaling molecule ( Fig. 1; Dave and Graham, 2012). In contrast to Arabidopsis, which has C 16 and C 18 fatty acid-derived pathways leading to the formation of cyclopentenones, P. patens has C 18 and C 20 fatty acid-derived pathways ( Fig.…”

Section: Discussionmentioning

confidence: 99%

“…In the absence of AOC, the epoxide is hydrolyzed into ketols and racemic 12-oxo-phytodienoic acid (OPDA). cis(+)-OPDA is the first cyclic and biologically active compound in that pathway (Dave and Graham, 2012). While the reactions leading from 18:3 (n-3) to cis(+)-OPDA occur in the plastid, all further enzymatic steps resulting in the formation of JA are localized in the peroxisomes (Wasternack, 2007).…”

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confidence: 99%

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Crystal Structures ofPhyscomitrella patensAOC1 and AOC2: Insights into the Enzyme Mechanism and Differences in Substrate Specificity

Neumann¹,

Brodhun²,

Sauer³

et al. 2012

Plant Physiology

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In plants, oxylipins regulate developmental processes and defense responses. The first specific step in the biosynthesis of the cyclopentanone class of oxylipins is catalyzed by allene oxide cyclase (AOC) that forms cis(+)-12-oxo-phytodienoic acid. The moss Physcomitrella patens has two AOCs (PpAOC1 and PpAOC2) with different substrate specificities for C 18 -and C 20 -derived substrates, respectively. To better understand AOC's catalytic mechanism and to elucidate the structural properties that explain the differences in substrate specificity, we solved and analyzed the crystal structures of 36 monomers of both apo and ligand complexes of PpAOC1 and PpAOC2. From these data, we propose the following intermediates in AOC catalysis: (1) a resting state of the apo enzyme with a closed conformation, (2) a first shallow binding mode, followed by (3) a tight binding of the substrate accompanied by conformational changes in the binding pocket, and (4) initiation of the catalytic cycle by opening of the epoxide ring. As expected, the substrate dihydro analog cis-12,13S-epoxy-9Z,15Z-octadecadienoic acid did not cyclize in the presence of PpAOC1; however, when bound to the enzyme, it underwent isomerization into the corresponding trans-epoxide. By comparing complex structures of the C 18 substrate analog with in silico modeling of the C 20 substrate analog bound to the enzyme allowed us to identify three major molecular determinants responsible for the different substrate specificities (i.e. larger active site diameter, an elongated cavity of PpAOC2, and two nonidentical residues at the entrance of the active site).

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Oxylipin Signaling: A Distinct Role for the Jasmonic Acid Precursor cis-(+)-12-Oxo-Phytodienoic Acid (cis-OPDA)

Cited by 167 publications

References 78 publications

Functional Convergence of Oxylipin and Abscisic Acid Pathways Controls Stomatal Closure in Response to Drought

Functional Convergence of Oxylipin and Abscisic Acid Pathways Controls Stomatal Closure in Response to Drought

Maize death acids, 9-lipoxygenase–derived cyclopente(a)nones, display activity as cytotoxic phytoalexins and transcriptional mediators

Crystal Structures ofPhyscomitrella patensAOC1 and AOC2: Insights into the Enzyme Mechanism and Differences in Substrate Specificity

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