First published online November 21, 2002; 10.1104/pp.012187
Plant Physiol, December 2002, Vol. 130, pp. 2152-2163
Convergence of Calcium Signaling Pathways of Pathogenic Elicitors
and Abscisic Acid in Arabidopsis Guard Cells1,2
Birgit
Klüsener,34
Jared J.
Young,3
Yoshiyuki
Murata,5
Gethyn J.
Allen,
Izumi C.
Mori,
Veronique
Hugouvieux,6 and
Julian
I.
Schroeder
Cell and Developmental Biology Section, Division of Biology, and
Center for Molecular Genetics, University of California, San Diego, La
Jolla, California 92093-0116
A variety of stimuli, such as abscisic acid (ABA), reactive
oxygen species (ROS), and elicitors of plant defense reactions, have
been shown to induce stomatal closure. Our study addresses commonalities in the signaling pathways that these stimuli trigger. A
recent report showed that both ABA and ROS stimulate an
NADPH-dependent, hyperpolarization-activated Ca2+ influx
current in Arabidopsis guard cells termed "ICa" (Z.M. Pei, Y. Murata, G. Benning, S. Thomine, B. Klüsener, G.J. Allen, E. Grill, J.I. Schroeder, Nature [2002] 406: 731-734). We found that
yeast (Saccharomyces cerevisiae) elicitor and chitosan,
both elicitors of plant defense responses, also activate this current and activation requires cytosolic NAD(P)H. These elicitors also induced
elevations in the concentration of free cytosolic calcium ([Ca2+]cyt) and stomatal closure in guard
cells. ABA and ROS elicited [Ca2+]cyt
oscillations in guard cells only when extracellular Ca2+
was present. In a 5 mM KCl extracellular buffer, 45% of
guard cells exhibited spontaneous [Ca2+]cyt
oscillations that differed in their kinetic properties from ABA-induced
Ca2+ increases. These spontaneous
[Ca2+]cyt oscillations also required the
availability of extracellular Ca2+ and depended on the
extracellular potassium concentration. Interestingly, when ABA was
applied to spontaneously oscillating cells, ABA caused cessation of
[Ca2+]cyt elevations in 62 of 101 cells,
revealing a new mode of ABA signaling. These data show that fungal
elicitors activate a shared branch with ABA in the stress signal
transduction pathway in guard cells that activates plasma membrane
ICa channels and support a requirement for
extracellular Ca2+ for elicitor and ABA signaling, as well
as for cellular [Ca2+]cyt oscillation maintenance.
1
This work was supported by the National
Institutes of Health (grant no. GM 60396 to J.I.S. and training grant
no. 3T32GM07240-25S1 to J.J.Y.), by the Department of Energy (grant
no. 94ER2018-07 to J.I.S.), by the National Science Foundation (grant
no. MCB 0077791 to J.I.S.), by the Alexander von Humboldt Foundation
(Feodor-Lynen fellowship to B.K.), and in part by the Ministry of
Education, Science, Sports and Culture of Japan (fellowship to
Y.M.).
2
This paper is dedicated to the memory of Gethyn Allen.
3
These authors contributed equally to the paper.
4
Present address: Lehrstuhl für
Pflanzenphysiologie, Ruhr-Universität Bochum, D-44780 Bochum, Germany.
5
Present address: Department of Agriculture, Okayama
University, Okayama 700, Japan.
6
Present address: Laboratoire de Physiologie Cellulaire
Végétale, Département Réponse et Dynamique
Cellulaires, CEA Grenoble, 38054 Grenoble cedex 9, France.
© 2002 American Society of Plant Biologists
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