Coronatine inhibits stomatal closure through guard cell-specific inhibition of NADPH oxidase-dependent ROS production

Microbes trigger stomatal closure through microbe-associated molecular patterns (MAMPs). The bacterial pathogen Pseudomonas syringae pv. tomato (Pst) synthesizes the polyketide toxin coronatine, which inhibits stomatal closure by MAMPs and by the hormone abscisic acid (ABA). The mechanism by which c...

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Autores principales: Toum, L., Torres, P.S., Gallego, S.M., Benavídes, M.P., Vojnov, A.A., Gudesblat, G.E.
Formato: JOUR
Materias:
Abscisic acid
Arabidopsis thaliana
Coronatine
NADPH oxidase
Reactive oxygen species
Stomata
Acceso en línea:http://hdl.handle.net/20.500.12110/paper_1664462X_v7_nDECEMBER2016_p_Toum
Aporte de:
Biblioteca Digital - Facultad de Ciencias Exactas y Naturales (UBA) de Universidad de Buenos Aires
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spelling todo:paper_1664462X_v7_nDECEMBER2016_p_Toum2023-10-03T16:29:11Z Coronatine inhibits stomatal closure through guard cell-specific inhibition of NADPH oxidase-dependent ROS production Toum, L. Torres, P.S. Gallego, S.M. Benavídes, M.P. Vojnov, A.A. Gudesblat, G.E. Abscisic acid Arabidopsis thaliana Coronatine NADPH oxidase Reactive oxygen species Stomata Microbes trigger stomatal closure through microbe-associated molecular patterns (MAMPs). The bacterial pathogen Pseudomonas syringae pv. tomato (Pst) synthesizes the polyketide toxin coronatine, which inhibits stomatal closure by MAMPs and by the hormone abscisic acid (ABA). The mechanism by which coronatine, a jasmonic acid-isoleucine analog, achieves this effect is not completely clear. Reactive oxygen species (ROS) are essential second messengers in stomatal immunity, therefore we investigated the possible effect of coronatine on their production. We found that coronatine inhibits NADPH oxidase-dependent ROS production induced by ABA, and by the flagellin-derived peptide flg22. This toxin also inhibited NADPH oxidase-dependent stomatal closure induced by darkness, however, it failed to prevent stomatal closure by exogenously applied H2 O2 or by salicylic acid, which induces ROS production through peroxidases. Contrary to what was observed on stomata, coronatine did not affect the oxidative burst induced by flg22 in leaf disks. Additionally, we observed that in NADPH oxidase mutants atrbohd and atrbohd/f, as well as in guard cell ABA responsive but flg22 insensitive mutants mpk3, mpk6, npr1-3, and lecrk-VI.2-1, the inhibition of ABA stomatal responses by both coronatine and the NADPH oxidase inhibitor diphenylene iodonium was markedly reduced. Interestingly, coronatine still impaired ABA-induced ROS synthesis in mpk3, mpk6, npr1-3, and lecrk-VI.2-1, suggesting a possible feedback regulation of ROS on other guard cell ABA signaling elements in these mutants. Altogether our results show that inhibition of NADPH oxidase-dependent ROS synthesis in guard cells plays an important role during endophytic colonization by Pst through stomata. © 2016 Toum, Torres, Gallego, Benavídes, Vojnov and Gudesblat. Fil:Torres, P.S. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Fil:Vojnov, A.A. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Fil:Gudesblat, G.E. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. JOUR info:eu-repo/semantics/openAccess http://creativecommons.org/licenses/by/2.5/ar http://hdl.handle.net/20.500.12110/paper_1664462X_v7_nDECEMBER2016_p_Toum
institution Universidad de Buenos Aires
institution_str I-28
repository_str R-134
collection Biblioteca Digital - Facultad de Ciencias Exactas y Naturales (UBA)
topic Abscisic acid
Arabidopsis thaliana
Coronatine
NADPH oxidase
Reactive oxygen species
Stomata
spellingShingle Abscisic acid
Arabidopsis thaliana
Coronatine
NADPH oxidase
Reactive oxygen species
Stomata
Toum, L.
Torres, P.S.
Gallego, S.M.
Benavídes, M.P.
Vojnov, A.A.
Gudesblat, G.E.
Coronatine inhibits stomatal closure through guard cell-specific inhibition of NADPH oxidase-dependent ROS production
topic_facet Abscisic acid
Arabidopsis thaliana
Coronatine
NADPH oxidase
Reactive oxygen species
Stomata
description Microbes trigger stomatal closure through microbe-associated molecular patterns (MAMPs). The bacterial pathogen Pseudomonas syringae pv. tomato (Pst) synthesizes the polyketide toxin coronatine, which inhibits stomatal closure by MAMPs and by the hormone abscisic acid (ABA). The mechanism by which coronatine, a jasmonic acid-isoleucine analog, achieves this effect is not completely clear. Reactive oxygen species (ROS) are essential second messengers in stomatal immunity, therefore we investigated the possible effect of coronatine on their production. We found that coronatine inhibits NADPH oxidase-dependent ROS production induced by ABA, and by the flagellin-derived peptide flg22. This toxin also inhibited NADPH oxidase-dependent stomatal closure induced by darkness, however, it failed to prevent stomatal closure by exogenously applied H2 O2 or by salicylic acid, which induces ROS production through peroxidases. Contrary to what was observed on stomata, coronatine did not affect the oxidative burst induced by flg22 in leaf disks. Additionally, we observed that in NADPH oxidase mutants atrbohd and atrbohd/f, as well as in guard cell ABA responsive but flg22 insensitive mutants mpk3, mpk6, npr1-3, and lecrk-VI.2-1, the inhibition of ABA stomatal responses by both coronatine and the NADPH oxidase inhibitor diphenylene iodonium was markedly reduced. Interestingly, coronatine still impaired ABA-induced ROS synthesis in mpk3, mpk6, npr1-3, and lecrk-VI.2-1, suggesting a possible feedback regulation of ROS on other guard cell ABA signaling elements in these mutants. Altogether our results show that inhibition of NADPH oxidase-dependent ROS synthesis in guard cells plays an important role during endophytic colonization by Pst through stomata. © 2016 Toum, Torres, Gallego, Benavídes, Vojnov and Gudesblat.
format JOUR
author Toum, L.
Torres, P.S.
Gallego, S.M.
Benavídes, M.P.
Vojnov, A.A.
Gudesblat, G.E.
author_facet Toum, L.
Torres, P.S.
Gallego, S.M.
Benavídes, M.P.
Vojnov, A.A.
Gudesblat, G.E.
author_sort Toum, L.
title Coronatine inhibits stomatal closure through guard cell-specific inhibition of NADPH oxidase-dependent ROS production
title_short Coronatine inhibits stomatal closure through guard cell-specific inhibition of NADPH oxidase-dependent ROS production
title_full Coronatine inhibits stomatal closure through guard cell-specific inhibition of NADPH oxidase-dependent ROS production
title_fullStr Coronatine inhibits stomatal closure through guard cell-specific inhibition of NADPH oxidase-dependent ROS production
title_full_unstemmed Coronatine inhibits stomatal closure through guard cell-specific inhibition of NADPH oxidase-dependent ROS production
title_sort coronatine inhibits stomatal closure through guard cell-specific inhibition of nadph oxidase-dependent ros production
url http://hdl.handle.net/20.500.12110/paper_1664462X_v7_nDECEMBER2016_p_Toum
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AT benavidesmp coronatineinhibitsstomatalclosurethroughguardcellspecificinhibitionofnadphoxidasedependentrosproduction
AT vojnovaa coronatineinhibitsstomatalclosurethroughguardcellspecificinhibitionofnadphoxidasedependentrosproduction
AT gudesblatge coronatineinhibitsstomatalclosurethroughguardcellspecificinhibitionofnadphoxidasedependentrosproduction
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