Fast-activating channel controls cation fluxes across the native chloroplast envelope

A prerequisite for photosynthetic CO(2) fixation is the maintenance of alkaline pH in the stroma. This is achieved by H(+) pumping from the stroma to the cytosol, electrically balanced by an influx of cations through some unidentified non-selective envelope channels. In this study, the patch-clamp technique was applied to isolated Pisum sativum L. (pea) chloroplasts, and a fast-activating chloroplast cation (FACC) channel was discovered in the native envelope. This channel opens within a few milliseconds upon voltage steps to large positive or negative potentials. Remarkably, the single-channel conductance increased fivefold, from approximately 40 pS to approximately 200 pS (symmetric 250 mM KCl), upon a potential change from zero to +/- 200 mV. The FACC channel conducts all physiologically essential inorganic cations (K(+), Na(+), Ca(2+), Mg(2+)) with little preference. An increase of stromal pH from 7.3 to 8.0, mimicking dark-light transition, caused about a 2-fold decrease of the FACC channel activity within a physiologically relevant potential range. The FACC channel was completely and irreversibly blocked by Gd(3+). Based on the estimated transport capacity of the whole chloroplast population of FACC channels together with the envelope H(+)-ATPases, these channels can mediate electroneutral K(+)/H(+) exchange across the envelope, enabling stroma alkalinization, thereby allowing an optimal photosynthetic performance.