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ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS

Extracellular Ca²⁺ Ameliorates NaCl-Induced K⁺ Loss from Arabidopsis Root and Leaf Cells by Controlling Plasma Membrane K⁺-Permeable Channels¹

School of Agricultural Sciences (S.S., L.S., T.A.C.) and School of Mathematics and Physics (I.A.N.), University of Tasmania, Hobart, Tasmania 7001, Australia; Department of Biological Sciences, University of Essex, Essex CO4 3SQ, United Kingdom (V.D.); Crop Performance and Improvement Division, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, United Kingdom (S.J.S., A.J.M.); and Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom (J.M.D.)

Calcium can ameliorate Na⁺ toxicity in plants by decreasing Na⁺ influx through nonselective cation channels. Here, we show that elevated external [Ca²⁺] also inhibits Na⁺-induced K⁺ efflux through outwardly directed, K⁺-permeable channels. Noninvasive ion flux measuring and patch-clamp techniques were used to characterize K⁺ fluxes from Arabidopsis (Arabidopsis thaliana) root mature epidermis and leaf mesophyll under various Ca²⁺ to Na⁺ ratios. NaCl-induced K⁺ efflux was not related to the osmotic component of the salt stress, was inhibited by the K⁺ channel blocker TEA⁺, was not mediated by inwardly directed K⁺ channels (tested in the akt1 mutant), and resulted in a significant decrease in cytosolic K⁺ content. NaCl-induced K⁺ efflux was partially inhibited by 1 mM Ca²⁺ and fully prevented by 10 mM Ca²⁺. This ameliorative effect was at least partially attributed to a less dramatic NaCl-induced membrane depolarization under high Ca²⁺ conditions. Patch-clamp experiments (whole-cell mode) have demonstrated that two populations of Ca²⁺-sensitive K⁺ efflux channels exist in protoplasts isolated from the mature epidermis of Arabidopsis root and leaf mesophyll cells. The instantaneously activating K⁺ efflux channels showed weak voltage dependence and insensitivity to external and internal Na⁺. Another population of K⁺ efflux channels was slowly activating, steeply rectifying, and highly sensitive to Na⁺. K⁺ efflux channels in roots and leaves showed different Ca²⁺ and Na⁺ sensitivities, suggesting that these organs may employ different strategies to withstand salinity. Our results suggest an additional mechanism of Ca²⁺ action on salt toxicity in plants: the amelioration of K⁺ loss from the cell by regulating (both directly and indirectly) K⁺ efflux channels.

² These authors contributed equally to the paper.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Sergey Shabala (sergey.shabala{at}utas.edu.au).

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.106.082388.

^* Corresponding author; e-mail sergey.shabala{at}utas.edu.au; fax 613–6226–2642.

Received April 19, 2006; returned for revision June 6, 2006; accepted June 10, 2006.

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