K+ currents through SV-type vacuolar channels are sensitive to elevated luminal sodium levels.
Non-selective slow vacuolar (SV) channels mediate uptake of K+ and Na+ into vacuolar compartment. Under salt stress plant cells accumulate Na+ in the vacuole and release vacuolar K+ into the cytoplasm. It is, however, unclear how plants mediate transport of K+ from the vacuole without concomitant efflux of toxic Na+. Here we show by patch-clamp studies on isolated Arabidopsis thaliana cell culture vacuoles that SV channels do not mediate Na+ release from the vacuole as luminal Na+ blocks this channel. Gating of the SV channel is dependent on the K+ gradient across the vacuolar membrane. Under symmetrical K+ concentrations on both sides of the vacuolar membrane, SV channels mediate potassium uptake. When cytoplasmic K+ decreases, SV channels allow K+ release from the vacuole. In contrast to potassium, Na+ can be taken up by SV channels, but not released even in the presence of a 150-fold gradient (lumen to cytoplasm). Accumulation of Na+ in the vacuole shifts the activation potential of SV channels to more positive voltages and prevents gradient-driven efflux of K+. Similar to sodium, under physiological conditions, vacuolar Ca2+ is not released from vacuoles via SV channels. We suggest that a major Arabidopsis SV channel is equipped with a positively charged intrinsic gate located at the luminal side, which prevents release of Na+ and Ca2+, but permits efflux of K+. This property of the SV channel guarantees that K+ can shuttle across the vacuolar membrane while maintaining Na+ and Ca2+ stored in this organelle.
Ivashikina
Natalya
N
Department of Molecular Plant Physiology and Biophysics, Julius-von-Sachs Institute of Biosciences, Biocentre, Würzburg University, Julius-von-Sachs-Platz 2, 97082 Würzburg, Germany.
Hedrich
Rainer
R
D017360:Arabidopsis / Q000502:physiology*; D002118:Calcium / Q000502:physiology; D018929:Cell Culture Techniques; D015640:Ion Channel Gating / Q000502:physiology*; D008564:Membrane Potentials / Q000502:physiology; D015221:Potassium Channels / Q000502:physiology*; D012964:Sodium / Q000502:physiology*; D014617:Vacuoles / Q000502:physiology*
D015221:Potassium Channels; D012964:Sodium; D002118:Calcium