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Light intensities that limit electron flow induce rapid degradation of the photosystem II (PSII) reaction center D1 protein. The mechanism of this phenomenon is not known. We propose that at low excitation rates back electron flow and charge recombination between the QB •− or QA •− semiquinone acceptors and the oxidized S2,3 states of the PSII donor side may cause oxidative damage via generation of active oxygen species. Therefore, damage per photochemical event should increase with decreasing rates of PSII excitation. To test this hypothesis, the effect of the dark interval between single turnover flashes on the inactivation of water oxidation, charge separation and recombination, and the degradation of D1 protein were determined in spinach thylakoids. PSII inactivation per flash increases as the dark interval between the flashes increases, and a plateau is reached at dark intervals, allowing complete charge recombination of the QB •− /S2,3 or QA •− /S2 states (about 200 and 40 s, respectively). At these excitation rates: (i ) 0.7% and 0.4% of PSII is inactivated and 0.4% and 0.2% of the D1 protein is degraded per flash, respectively, and (ii ) the damage per flash is about 2 orders of magnitude higher than that induced by equal amount of energy delivered by excess continuous light. No PSII damage occurs if flashes are given in anaerobic conditions. These results demonstrate that charge recombination in active PSII is promoted by low rates of excitation and may account for a the high quantum efficiency of the rapid turnover of the D1 protein induced by limiting light.

Mechanism of photosystem II photoinactivation and D1 protein degradation at low light: The role of back electron flow