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

A prerequisite for photosynthetic CO₂ 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 ∼40 pS to ∼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⁺, Ca²⁺, Mg²⁺) 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 Gd³⁺. 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.