First published online April 2, 2004; 10.1104/pp.103.032250
Plant Physiology 134:1536-1545 (2004)
© 2004 American Society of Plant Biologists
CELL BIOLOGY AND SIGNAL TRANSDUCTION
Cytoplasmic Alkalization Precedes Reactive Oxygen Species Production during Methyl Jasmonate- and Abscisic Acid-Induced Stomatal Closure1
Dontamala Suhita,
Agepati S. Raghavendra,
June M. Kwak and
Alain Vavasseur*
CEA/Cadarache-DSV-DEVM, Laboratoire des Echanges Membranaires et Signalisation, UMR 163 CNRS-CEA, Université de la Méditerranée, 13108 St Paul lez Durance cedex, France (D.S., A.V.); Department of Plant Sciences, School of Life Sciences, University of Hyderabad, Hyderabad 500046, India (D.S., A.S.R.); and Cell and Developmental Biology Section, Division of Biological Sciences, University of California San Diego, La Jolla, California 92093–0116 (J.M.K.)
Signaling events during abscisic acid (ABA) or methyl jasmonate (MJ)-induced stomatal closure were examined in Arabidopsis wild type, ABA-insensitive (ost1-2), and MJ-insensitive mutants (jar1-1) in order to examine a crosstalk between ABA and MJ signal transduction. Some of the experiments were performed on epidermal strips of Pisum sativum. Stomata of jar1-1 mutant plants are insensitive to MJ but are able to close in response to ABA. However, their sensitivity to ABA is less than that of wild-type plants. Reciprocally, the stomata of ost1-2 are insensitive to ABA but are able to close in response to MJ to a lesser extent compared to wild-type plants. Both MJ and ABA promote H2O2 production in wild-type guard cells, while exogenous application of diphenylene iodonium (DPI) chloride, an inhibitor of NAD(P)H oxidases, results in the suppression of ABA- and MJ-induced stomatal closure. ABA elevates H2O2 production in wild-type and jar1-1 guard cells but not in ost1-2, whereas MJ induces H2O2 production in both wild-type and ost1-2 guard cells, but not in jar1-1. MJ-induced stomatal closing is suppressed in the NAD(P)H oxidase double mutant atrbohD/F and in the outward potassium channel mutant gork1. Furthermore, MJ induces alkalization in guard cell cytosol, and MJ-induced stomatal closing is inhibited by butyrate. Analyses of the kinetics of cytosolic pH changes and reactive oxygen species (ROS) production show that the alkalization of cytoplasm precedes ROS production during the stomatal response to both ABA and MJ. Our results further indicate that JAR1, as OST1, functions upstream of ROS produced by NAD(P)H oxidases and that the cytoplasmic alkalization precedes ROS production during MJ or ABA signal transduction in guard cells.
1 This work was supported by grants from the Indo-French Centre for the Promotion of Advanced Research (grant no. 2203–1 to A.S.R. and A.V.) and the Council of Scientific and Industrial Research [grant no. 38(0949)/99/EMR–II to A.S.R.], both from New Delhi. J.M.K. was supported by a fellowship from the Human Frontier Science Program.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.032250.
* Corresponding author; email avavasseur{at}cea.fr; fax 33–4–42252364.
Received August 26, 2003;
returned for revision January 7, 2004;
accepted January 8, 2004.
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