Cyclic electron flow around photosystem I (CEF) is critical for balancing the photosynthetic energy budget of the chloroplast, by generating ATP without net production of NADPH. We demonstrate that the chloroplast NADPH dehydrogenase complex (NDH), a homolog to respiratory Complex I, pumps approximately two protons from the chloroplast stroma to the lumen per electron transferred from ferredoxin to plastoquinone, effectively increasing the efficiency of ATP production via CEF by two-fold compared to CEF pathways involving non-proton-pumping plastoquinone reductases. By virtue of this proton-pumping stoichiometry, we hypothesise that NDH not only efficiently contributes to ATP production, but operates near thermodynamic reversibility, with potentially important consequences for remediating mismatches in the thylakoid energy budget.
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