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Published on June 23, 2006; 10.1104/pp.106.082388


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Received April 19, 2006
Returned for revision May 16, 2006
Accepted June 10, 2006

Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels

Sergey Shabala *, Vadim Demidchik , Lana Shabala , Tracey A. Cuin , Susan J. Smith , Anthony J. Miller , Julia M. Davies , and Ian A. Newman

School of Agricultural Sciences, University of Tasmania, Hobart, Tasmania 7001, Australia
Department of Biological Sciences, University of Essex, Wivenhoe Park, Essex, CO4 3SQ, United Kingdom
CPI Division, Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, United Kingdom
Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge, CB2 3EA, United Kingdom
School of Mathematics and Physics, University of Tasmania, Hobart, Tasmania 7001, Australia

* Corresponding author; email: Sergey.Shabala{at}utas.edu.au.

Calcium can ameliorate Na+ toxicity in plants by decreasing Na+ influx through non-selective cation channels (NSCC). Here, we show that elevated external [Ca2+] also inhibits Na+-induced K+ efflux through outwardly directed K+-permeable channels. MIFE and patch clamp techniques were used to characterise K+ fluxes from Arabidopsis root mature epidermis and leaf mesophyll under various Ca2+/Na+ ratios. NaCl-induced K+ efflux was not related to the osmotic component of the salt stress, it was inhibited by the K+ channel blocker TEA+, 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 depolarisation 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 a new 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.




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