Plant adaptation to fluctuating environment and biomass production are strongly dependent on guard cell potassium channels

doi:10.1073/pnas.0709732105

Plant adaptation to fluctuating environment and biomass production are strongly dependent on guard cell potassium channels

*Biochimie et Physiologie Moléculaire des Plantes, Unité Mixte de Recherche 5004, Centre National de la Recherche Scientifique/Institut National de la Recherche Agronomique (U.386)/Montpellier SupAgro/Université Montpellier 2, 1 Place Viala, 34060 Montpellier Cedex 1, France;
^†Laboratoire des Echanges Membranaires et Signalisation, Unité Mixte de Recherche 6191, Centre National de la Recherche Scientifique/Commissariat à l'Energie Atomique/Université Aix-Marseille, 13108 St. Paul lez Durance Cedex, France; and
^§Laboratoire d'Ecophysiologie des Plantes sous Stress Environnementaux, Unité Mixte de Recherche 759, Institut National de la Recherche Agronomique/Montpellier SupAgro, 1 Place Viala, 34060 Montpellier Cedex 1, France

Edited by Maarten J. Chrispeels, University of California at San Diego, La Jolla, CA, and approved February 8, 2008 (received for review October 12, 2007)

Abstract

At least four genes encoding plasma membrane inward K⁺ channels (K_in channels) are expressed in Arabidopsis guard cells. A double mutant plant was engineered by disruption of a major K_in channel gene and expression of a dominant negative channel construct. Using the patch-clamp technique revealed that this mutant was totally deprived of guard cell K_in channel (GCK_in) activity, providing a model to investigate the roles of this activity in the plant. GCK_in activity was found to be an essential effector of stomatal opening triggered by membrane hyperpolarization and thereby of blue light-induced stomatal opening at dawn. It improved stomatal reactivity to external or internal signals (light, CO₂ availability, and evaporative demand). It protected stomatal function against detrimental effects of Na⁺ when plants were grown in the presence of physiological concentrations of this cation, probably by enabling guard cells to selectively and rapidly take up K⁺ instead of Na⁺ during stomatal opening, thereby preventing deleterious effects of Na⁺ on stomatal closure. It was also shown to be a key component of the mechanisms that underlie the circadian rhythm of stomatal opening, which is known to gate stomatal responses to extracellular and intracellular signals. Finally, in a meteorological scenario with higher light intensity during the first hours of the photophase, GCK_in activity was found to allow a strong increase (35%) in plant biomass production. Thus, a large diversity of approaches indicates that GCK_in activity plays pleiotropic roles that crucially contribute to plant adaptation to fluctuating and stressing natural environments.

Footnotes

^¶To whom correspondence should be addressed. E-mail: sentenac{at}supagro.inra.fr
Author contributions: A.L., A.V., E.H., I.D., N.L., J.-B.T., A.-A.V., T.S., and H.S. designed research; A.L., A.V., E.H., I.D., N.L., and A.-A.V. performed research; A.L., A.V., E.H., I.D., N.L., J.-B.T., A.-A.V., T.S., and H.S. analyzed data; and A.L. and H.S. wrote the paper.
↵ ^‡Present address: Universität Potsdam, Institut für Biochemie und Biologie, Karl-Liebknecht-Strasse, D-14476 Potsdam-Golm, Germany.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/cgi/content/full/0709732105/DCSupplemental.