First published online June 23, 2006; 10.1104/pp.106.082388
Plant Physiology 141:1653-1665 (2006)
© 2006 American Society of Plant Biologists
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
Sergey Shabala2,*,
Vadim Demidchik2,
Lana Shabala,
Tracey A. Cuin,
Susan J. Smith,
Anthony J. Miller,
Julia M. Davies and
Ian A. Newman
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.
1 This work was supported by Aus Industry (no. S00112661), Department of Education, Science and Training (no. CG040074), and University of Tasmania Institutional Research Grants Scheme (no. S0011864) grants to S.S.; an Australian Research Council grant (no. A00105708) to I.A.N.; and a Leverhulme Trust project grant (no. F/09 741/C) to J.M.D.
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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