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Plant Adaptation to Fluctuating Environment and Biomass Production Are Strongly Dependent on Guard Cell Potassium Channels

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Plant Adaptation to Fluctuating Environment and Biomass Production Are Strongly Dependent on Guard Cell Potassium Channels Plant adaptation to fluctuating environment and biomass production are strongly dependent on guard cell potassium channels Anne Lebaudy*, Alain Vavasseur†, Eric Hosy*, Ingo Dreyer*‡, Nathalie Leonhardt†, Jean-Baptiste Thibaud*, Anne-Alie´ nor Ve´ ry*, Thierry Simonneau§, and Herve´ Sentenac*¶ *Biochimie et Physiologie Mole´culaire des Plantes, Unite´Mixte de Recherche 5004, Centre National de la Recherche Scientifique/Institut National de la Recherche Agronomique (U.386)/Montpellier SupAgro/Universite´Montpellier 2, 1 Place Viala, 34060 Montpellier Cedex 1, France; †Laboratoire des Echanges Membranaires et Signalisation, Unite´Mixte de Recherche 6191, Centre National de la Recherche Scientifique/Commissariat a`l’Energie Atomique/Universite´ Aix-Marseille, 13108 St. Paul lez Durance Cedex, France; and §Laboratoire d’Ecophysiologie des Plantes sous Stress Environnementaux, Unite´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) At least four genes encoding plasma membrane inward K؉ chan- plant physiology by engineering an Arabidopsis mutant totally nels (Kin channels) are expressed in Arabidopsis guard cells. A deprived of this activity. double mutant plant was engineered by disruption of a major Kin channel gene and expression of a dominant negative channel Results construct. Using the patch-clamp technique revealed that this Genetic Engineering of an Arabidopsis Mutant Deprived of GCKin mutant was totally deprived of guard cell Kin channel (GCKin) Activity. In a first step, we screened candidate mutant lines in activity, providing a model to investigate the roles of this activity which expression of inward Kϩ channels is affected, by looking in the plant. GCKin activity was found to be an essential effector of for altered transpiration as the most probable phenotype. At stomatal opening triggered by membrane hyperpolarization and least four inward Kϩ channel genes, KAT1, KAT2, AKT1, and thereby of blue light-induced stomatal opening at dawn. It im- AKT2, all belonging to the Shaker family, are expressed in guard proved stomatal reactivity to external or internal signals (light, CO2 cells, the first two at higher levels than the others (11, 12). PLANT BIOLOGY availability, and evaporative demand). It protected stomatal func- Disruption of KAT1 was known to barely affect leaf transpiration tion against detrimental effects of Na؉ when plants were grown (11). To assess the role of KAT2, we isolated a T-DNA mutant in the presence of physiological concentrations of this cation, plant in which expression of this gene was totally abolished probably by enabling guard cells to selectively and rapidly take up [supporting information (SI) Fig. S1]. When compared with WT K؉ instead of Na؉ during stomatal opening, thereby preventing plants, this knockout mutant, named kat2-1, displayed neither deleterious effects of Na؉ on stomatal closure. It was also shown difference in transpiration rate (Fig. S2) nor any apparent to be a key component of the mechanisms that underlie the phenotype (data not shown). Alternatively, we developed a circadian rhythm of stomatal opening, which is known to gate dominant negative strategy based on the fact that Shaker chan- stomatal responses to extracellular and intracellular signals. Fi- nels are homotetrameric or heterotetrameric proteins, formed nally, in a meteorological scenario with higher light intensity from subunits encoded by one or several Shaker genes (13–16). during the first hours of the photophase, GCKin activity was found WT plants were transformed with a dominant negative (dom- to allow a strong increase (35%) in plant biomass production. Thus, neg) kat2 construct (15) under control of the KAT2 promoter. a large diversity of approaches indicates that GCKin activity plays The resulting transgenic plants, named domneg-1 (T3 generation, pleiotropic roles that crucially contribute to plant adaptation to homozygous for the domneg transgene), did not display any fluctuating and stressing natural environments. defect in transpiration (Fig. S2) or any apparent phenotype (data not shown). Interestingly, a transpiration phenotype appeared Arabidopsis ͉ circadian rhythm ͉ inward Shaker ͉ stomata ͉ when the kat2 domneg construct was introduced in the kat2-1 transpirational water loss knockout background. The resulting double mutant (T3 gener- ation, homozygous for both mutations) displayed decreased he leaf epidermis is covered with a waxy cuticle that prevents transpirational water loss during the light period when compared with WT plants (Fig. S2; see also below). It did not display any Twater loss but also impedes diffusion of atmospheric CO2 ϩ toward the inner photosynthetic tissues. Gas exchanges mainly phenotype in terms of leaf K contents or stomatal densities occur through microscopic pores in the epidermis, named stomata. (data not shown). Back-crossing this double mutant with the WT By controlling stomatal aperture, the plant copes with the conflict- plant indicated that the transpiration phenotype was linked to the simultaneous presence of both mutations and not to the locus ing needs of allowing CO2 entry for photosynthesis and of prevent- ing excessive water loss (1). An increase or decrease in turgor of the of insertion of the domneg construct (data not shown). guard cells lining the pore opens or closes the stoma, respectively. Patch-clamp experiments were then performed to determine Kϩ and accompanying anions (malate and chloride) are among the major solutes involved in this osmotically driven process (2–6). ϩ ϩ Author contributions: A.L., A.V., E.H., I.D., N.L., J.-B.T., A.-A.V., T.S., and H.S. designed Changes in guard cell K content involve K channel activity 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., ϩ (7, 8) encoded by Shaker K channel genes (9). A single Shaker J.-B.T., A.-A.V., T.S., and H.S. analyzed data; and A.L. and H.S. wrote the paper. gene in Arabidopsis, GORK, encodes the guard cell membrane The authors declare no conflict of interest. outward conductance, and disruption of this gene results in This article is a PNAS Direct Submission. impaired stomatal closure in response to darkness or abscisic ‡Present address: Universita¨t Potsdam, Institut fu¨r Biochemie und Biologie, Karl- ϩ acid (ABA) (10). Regarding the inward K conductance, Ara- Liebknecht-Strasse, D-14476 Potsdam-Golm, Germany. bidopsis guard cells express at least four genes coding for Shaker ¶To whom correspondence should be addressed. E-mail: [email protected]. ␣-subunits involved in formation of inward channels (11). Here This article contains supporting information online at www.pnas.org/cgi/content/full/ ϩ we assess the importance of the guard cell membrane inward K 0709732105/DCSupplemental. channel (GCKin) activity in stomatal movements and whole- © 2008 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0709732105 PNAS ͉ April 1, 2008 ͉ vol. 105 ͉ no. 13 ͉ 5271–5276 Downloaded by guest on September 29, 2021 A WT kat2-1 A fusicoccin ± Cs+ B white light C red or blue light - Cs+ + Cs+ blue red 3 WT WT WT kincless kincless kincless -200 mV 2 -200 mV 1 domneg-1 Stomatal aperture (µm) aperture Stomatal 0 400 pA 250 ms 0 1234 0 1234 0 123 kincless Time (h) Time (h) Time (h) ϩ -200 mV Fig. 2. Disruption of inward K channel activity affects stomatal opening. Epidermal strips were peeled from WT (filled symbols) or kincless (open symbols) plants at the end of the dark period. Stomatal opening was induced (t ϭ 0) by fusicoccin (10 ␮M) in the presence or absence of Csϩ (30 mM) (A)or by switching on white light (B) or blue or red light (C). Kϩ concentration in the I tot (pA) Ϯ Ͼ B 400 bath solution: 10 mM (A)or30mM(B and C). Data are means SE. n 100 Ͼ Ͼ Vm (mV) in A, n 150 in B, and n 200 in C. 001-002- 051 evidence for total absence of GCKin activity. (ii) Stomatal opening was strongly dependent on GCKin activity when it was -400 triggered by fusicoccin or blue light, two treatments that have WT [9] kincless [8] been extensively characterized as leading to membrane hyper- domneg-1 [7] polarization. (iii) On the contrary, stomatal opening was poorly kat2-1 [7] -800 dependent on GCKin activity when it was triggered by red light. Fig. 1. Absence of inward Kϩ channel activity in guard cells of the kincless The mechanisms of red light-induced stomatal opening are still mutant. (A) Representative macroscopic current traces recorded with the unclear, and conflicting data have been reported on the actual patch-clamp technique in guard cell protoplasts from WT (Upper Left), kat2-1 contribution of Hϩ-ATPase activation and membrane hyperpo- (knockout mutant disrupted in the KAT2 gene) (Upper Right), domneg-1 larization to the process (18). (expressing a dominant negative kat2 construct in WT background) (Lower Right), or kincless (expressing the same domneg construct in the kat2-1 GCK Activity Underlies Stomatal Responsiveness to Changes in Light, background) (Lower Left) plants. In all recordings, the holding potential was in Ϫ100 mV; voltage steps were applied to potentials ranging between Ϫ100 Air Humidity, and CO2 Availability in Intact Plants. Consequences of and ϩ120 mV in 20-mV increments (top traces for each genotype) or between the absence of GCKin activity on leaf transpiration were then Ϫ100 and Ϫ260 mV in increments of Ϫ20 mV (bottom traces for each geno- investigated by using a setup that continuously monitors tran- type). (B) Comparison of current–voltage relationships from the different spirational water loss in an intact plant. Consistent with the genotypes. Total current (I tot, sampled at time marked by symbols over the above results, absence of GCK activity affected the increase in Ϯ in recordings in A) is plotted against membrane potential.
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