Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+ -permeable channels.
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.
Shabala
Sergey
S
School of Agricultural Sciences , University of Tasmania, Hobart, Tasmania 7001, Australia. sergey.shabala@utas.edu.au
Demidchik
Vadim
V
Shabala
Lana
L
Cuin
Tracey A
TA
Smith
Susan J
SJ
Miller
Anthony J
AJ
Davies
Julia M
JM
Newman
Ian A
IA
D017360:Arabidopsis / Q000166:cytology / Q000187:drug effects / Q000378:metabolism*; D002118:Calcium / Q000378:metabolism / Q000502:physiology*; D002462:Cell Membrane / Q000378:metabolism*; D003600:Cytosol / Q000378:metabolism; D004553:Electric Conductivity; D006706:Homeostasis; D009997:Osmotic Pressure; D018408:Patch-Clamp Techniques; D018515:Plant Leaves / Q000166:cytology / Q000187:drug effects / Q000378:metabolism; D018517:Plant Roots / Q000166:cytology / Q000187:drug effects / Q000378:metabolism; D011188:Potassium / Q000378:metabolism*; D026902:Potassium Channel Blockers / Q000494:pharmacology; D015221:Potassium Channels / Q000378:metabolism*; D011523:Protoplasts / Q000378:metabolism; D012964:Sodium / Q000378:metabolism; D012965:Sodium Chloride / Q000494:pharmacology*; D019789:Tetraethylammonium / Q000494:pharmacology
D026902:Potassium Channel Blockers; D015221:Potassium Channels; D012965:Sodium Chloride; D019789:Tetraethylammonium; D012964:Sodium; D011188:Potassium; D002118:Calcium