Multiple inward channels provide flexibility in Na+/K+ discrimination at the plasma membrane of barley suspension culture cells

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Abstract
Ion transport across the plasma membrane of suspension-culture cells derived from immature barley embryos has been studied in low (15 mM KCl) and high (additional 150 mM NaCl) salt conditions to understand how plants discriminate between K+ and Na+ during ion uptake. In both media about 50% of the cells exhibited resting potentials more negative than any of the passive diffusion potentials. In whole-cell patch clamp experiments membrane hyperpolarization activated large inward currents. Whilst the instantaneous current components did not discriminate between K+ and Na+, the time-dependent current, Iin, was selective for K+ over Na+. Further analysis of Iin revealed the following properties: double exponential current activation (time-constants 0.03 s and 0.3 s, half activation potential − 171 mV); no inactivation; complete block by Ba2+ (30 mM in 100 mM KCl) and part block by TEA+ (maximum 50% with 20 mM); dependence on millimolar concentrations of cytoplasmic ATP; no block by external or cytoplasmic Na+. The selectivity sequences K+ ≫ Rb+ > NH+4 > Na+ ≫ Cl− and K+ ≫ NH+4 > Na+ > Rb+ were determined from measurements of reversal potentials and relative steady-state currents respectively. PNa:PK was 0.07 ± 0.02 (from reversal potentials) and INa:IK was 0.17 + 0.05 (from relative currents). A high variance among the observed permeability ratios suggested that several channels with different ion-selectivities contributed to the time-dependent whole-cell currents. In single channel experiments, several inward channels with distinct properties were found. The major channels were (i) a voltage-gated, K+-selective channel (12 pS), (ii) an ATP-activated non-selective cation channel (7 pS) and (iii) an inward-rectifying anion-channel (150 pS, all unitary conductances given for 100 mM KCI). No significant differences were found in whole-cell currents or single-channel characteristics between cells that had been adapted to a high-salt growth-medium (150 mM NaCl) and non-adapted cells. The idea that differential regulation of plasma membrane ion channels gives rise to a physiological flexibility, allowing the cells to control Na+ uptake under varying external conditions, is discussed.

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