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Metabolism and Enzymology

Stromal pH and Photosynthesis Are Affected by Electroneutral K⁺ and H⁺ Exchange through Chloroplast Envelope Ion Channels ¹

Horticulture Department, Cook College, Rutgers-The State University of New Jersey, New Brunswick, New Jersey 08903

Potassium movement across the limiting membrane of the chloroplast inner envelope is known to be linked to counterex-change of protons. For this reason, K⁺ efflux is known to facilitate stromal acidification and the resultant photosynthetic inhibition. However, the specific nature of the chloroplast envelope proteins that facilitate K⁺ fluxes, and the biophysical mechanism which links these cation currents to H⁺ counterflux, is not characterized. It was the objective of this work to elucidate the nature of the system regulating K⁺ flux linked to H⁺ counterflux across the chloroplast envelope. In the absence of external K⁺, exposure of spinach (Spinacia oleracea) chloroplasts to the K⁺ ionophore valinomycin was found to increase the rate of K⁺ efflux and H⁺ influx. These data were interpreted as suggesting that H⁺ counterexchange must be indirectly linked to movement of K⁺ across the envelope. Studies using the K⁺ channel blocker tetraethylammonium indicated that K⁺ likely moves, in a uniport fashion, into or out of the stroma through a monovalent cation channel in the envelope. Blockage of K⁺ efflux from the stroma by exposure to tetraethylammonium was found to restrict H⁺ influx, further substantiating an indirect linkage of these cation currents. Further studies comparing the effect of exogenous H⁺ ionophores and K⁺/H⁺ exchangers suggested that K⁺ uniport through this ion channel likely is the main endogenous pathway for K⁺ currents across the envelope. These experiments were also consistent with the presence of a proton channel in the envelope. Movement of H⁺ through this channel was speculated to be regulated and rate limited by an electroneutral requirement for K⁺ countercurrents through the separate K⁺ uniport pathway. K⁺ and H⁺ fluxes across the chloroplast envelope were envisioned to be interrelated via this mechanism. The significant effect of cation currents across the envelope, as mediated by these channels, on photosynthetic capacity of the isolated chloroplast was also demonstrated.

¹ New Jersey Agricultural Experiment Station, Publication No. 12149-10-91. This material is based upon work supported by the U.S. Department of Agriculture Competitive Research Grants Office under Award No. 90-37262-5586.

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