An Abscisic Acid-Independent Oxylipin Pathway Controls Stomatal Closure and Immune Defense in Arabidopsis

Montillet, Jean‐Luc; Leonhardt, Nathalie; Mondy, Samuel; Tranchimand, Sylvain; Rumeau, Dominique; Boudsocq, Marie; García, Ana Victoria Torres; Douki, Thierry; Bigeard, Jean; Laurière, Christiane; Chevalier, Anne; Castresana, Carmen; Hirt, Heribert

doi:10.1371/journal.pbio.1001513

Cited by 232 publications

(253 citation statements)

References 74 publications

(98 reference statements)

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“…By contrast, our findings consistently show that under no circumstances are equal concentrations of ABA and MeJA similarly potent in stomatal closure. The ability of MeJA to induce stomatal closure remains controversial, because in support of our data, a recent report showed that MeJA at concentrations up to 100 mM is ineffective in reducing stomatal aperture (Montillet et al, 2013). Furthermore, dose response curve studies show that maximum reduction of stomatal aperture is achieved by 12-OPDA at approximately 5-fold-lower concentrations than that of MeJA (Fig.…”

Section: External Application Of 12-opda Promotes Stomatal Closuresupporting

confidence: 75%

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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: External Application Of 12-opda Promotes Stomatal Closuresupporting

confidence: 75%

“…Asterisk denotes significant difference in aperture under a given treatment (P , 0.0001). 12-OPDA in reducing stomata aperture is also reported as a functional innate immunity mechanism to ward plants against pathogens (Montillet et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2014

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“…9-HOT and 9-KOT induce ROS or act as reactive electrophile species to trigger transcriptional reprogramming or to modify macromolecules covalently (Vellosillo et al, 2007;Mueller et al, 2008;López et al, 2011;Vicente et al, 2012;Farmer and Mueller, 2013;Montillet et al, 2013). Plant responses to these oxylipins are under mitochondrial retrograde control, as 9-HOT causes mitochondrial aggregation and loss of mitochondrial membrane potential and NOXY2 (and the 9-LOX signaling NOXY genes DYNAMIN-RELATED PROTEIN3A/NOXY15 and FRIENDLY MITOCHONDRIA/NOXY38) encodes a mitochondrial protein (Vellosillo et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

“…Genetic studies in Arabidopsis (Arabidopsis thaliana) showed a 9-LOX function in activating local defense and stomata closure against virulent Pseudomonas spp. (Hwang and Hwang, 2010;López et al, 2011;Montillet et al, 2013) as well as 9-LOX and a-DOX pathway cooperation in triggering systemic resistance (Vicente et al, 2012). There is also evidence of a role in activating systemic defense for C9 oxylipins formed by nonenzymatic free radical reactions (Jung et al, 2009;Wang et al, 2014;Wittek et al, 2014).…”

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confidence: 99%

9-Lipoxygenase-derived oxylipins activate brassinosteroid signaling to promote cell wall-based defense and limit pathogen infection

et al. 2015

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The oxylipins, a large family of oxygenated lipid derivatives, regulate plant development and immunity. Two members of the 9-lipoxygenase (9-LOX) oxylipin pathway, 9-hydroxyoctadecatrienoic acid and 9-ketooctadecatrienoic acid, control root development and plant defense. Studies in Arabidopsis (Arabidopsis thaliana) using a series of 9-hydroxyoctadecatrienoic acidand 9-ketooctadecatrienoic acid-insensitive nonresponding to oxylipins (noxy) mutants showed the importance of the cell wall as a 9-LOX-induced defense component and the participation of NOXY proteins in signaling cell wall damage. Here, we examined 9-LOX signaling using the mutants lox1lox5, which lacks 9-LOX activity, and noxy2-2, which shows oxylipin insensitivity and mitochondrial dysfunction. Mutants in brassinosteroids (BRs), a class of plant hormones necessary for normal plant growth and the control of cell wall integrity, were also analyzed. Several lines of evidence indicated that 9-LOX-derived oxylipins induce BR synthesis and signaling to activate cell wall-based responses such as callose deposition and that constitutive activation of BR signaling in bri1-EMS-suppressor 1-D (bes1-D) plants enhances this response. We found that constitutive BR signaling in bes1-D and brassinolide-resistant 1-1D (bzr1-1D) mutants conferred resistance to Pseudomonas syringae. bes1-D and bzr1-1D showed increased resistance to Golovinomyces cichoracearum, an obligate biotrophic fungus that penetrates the cell wall for successful infection, whereas susceptibility was enhanced in lox1lox5 and noxy2-2. Our results indicate a sequential action of 9-LOX and BR signaling in activating cell wall-based defense, and this response prevents pathogen infection. These results show interaction between the 9-LOX and BR pathways and help to clarify their role in modulating plant defense.

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“…Stomatal aperture was measured on epidermal peels excised from the abaxial side of leaves of 3-to 4-week-old plants, essentially as described by Montillet et al (2013). In all cases, two epidermal peels from two independent plants of the indicated genotype were first incubated for 30 min in darkness at ambient air in a bathing solution containing 30 mM KCl, 1 mM CaCl 2 , and 10 mM MES/Tris pH6.0, prior to exposure to the indicated treatment.…”

Section: Measurements Of Stomatal Aperturementioning

confidence: 99%

Aquaporins Contribute to ABA-Triggered Stomatal Closure through OST1-Mediated Phosphorylation

et al. 2015

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International audienceStomatal movements in response to environmental stimuli critically control the plant water status. Although these movements are governed by osmotically driven changes in guard cell volume, the role of membrane water channels (aquaporins) has remained hypothetical. Assays in epidermal peels showed that knockout Arabidopsis thaliana plants lacking the Plasma membrane Intrinsic Protein 2;1 (PIP2;1) aquaporin have a defect in stomatal closure, specifically in response to abscisic acid (ABA). ABA induced a 2-fold increase in osmotic water permeability (Pf) of guard cell protoplasts and an accumulation of reactive oxygen species in guard cells, which were both abrogated in pip2;1 plants. Open stomata 1 (OST1)/Snf1-related protein kinase 2.6 (SnRK2.6), a protein kinase involved in guard cell ABA signaling, was able to phosphorylate a cytosolic PIP2;1 peptide at Ser-121. OST1 enhanced PIP2;1 water transport activity when coexpressed in Xenopus laevis oocytes. Upon expression in pip2;1 plants, a phosphomimetic form (Ser121Asp) but not a phosphodeficient form (Ser121Ala) of PIP2;1 constitutively enhanced the Pf of guard cell protoplasts while suppressing its ABA-dependent activation and was able to restore ABA-dependent stomatal closure in pip2;1. This work supports a model whereby ABA-triggered stomatal closure requires an increase in guard cell permeability to water and possibly hydrogen peroxide, through OST1-dependent phosphorylation of PIP2;1 at Ser-121

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An Abscisic Acid-Independent Oxylipin Pathway Controls Stomatal Closure and Immune Defense in Arabidopsis

Abstract: In Arabidopsis the stomatal defense response, a feature of the innate immunity in plants, involves oxylipin-mediated mechanisms that are independent of the phytohormone abscisic acid.

Cited by 232 publications

References 74 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

9-Lipoxygenase-derived oxylipins activate brassinosteroid signaling to promote cell wall-based defense and limit pathogen infection

Aquaporins Contribute to ABA-Triggered Stomatal Closure through OST1-Mediated Phosphorylation

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