High cyclic electron transfer via the PGR5 pathway in the absence of photosynthetic control

High PGR5-dependent cyclic electron transfer increases proton motive force but in the absence of ATP synthase regulation is insufficient to induce photosynthetic control. The light reactions of photosynthesis couple electron and proton transfers across the thylakoid membrane, generating NADPH, and proton motive force (pmf) that powers the endergonic synthesis of ATP by ATP synthase. ATP and NADPH are required for CO2 fixation into carbohydrates by the Calvin-Benson-Bassham cycle. The dominant Delta pH component of the pmf also plays a photoprotective role in regulating photosystem II light harvesting efficiency through nonphotochemical quenching (NPQ) and photosynthetic control via electron transfer from cytochrome b(6)f (cytb(6)f) to photosystem I. Delta pH can be adjusted by increasing the proton influx into the thylakoid lumen via upregulation of cyclic electron transfer (CET) or decreasing proton efflux via downregulation of ATP synthase conductivity (gH(+)). The interplay and relative contributions of these two elements of Delta pH control to photoprotection are not well understood. Here, we showed that an Arabidopsis (Arabidopsis thaliana) ATP synthase mutant hunger for oxygen in photosynthetic transfer reaction 2 (hope2) with 40% higher proton efflux has supercharged CET. Double crosses of hope2 with the CET-deficient proton gradient regulation 5 and ndh-like photosynthetic complex I lines revealed that PROTON GRADIENT REGULATION 5 (PGR5)-dependent CET is the major pathway contributing to higher proton influx. PGR5-dependent CET allowed hope2 to maintain wild-type levels of Delta pH, CO2 fixation and NPQ, however photosynthetic control remained absent and PSI was prone to photoinhibition. Therefore, high CET in the absence of ATP synthase regulation is insufficient for PSI photoprotection.

Automated summary

High PGR5-dependent cyclic electron transfer increases proton motive force, but without ATP synthase regulation, it cannot induce photosynthetic control. The light reactions of photosynthesis generate NADPH and ATP through electron and proton transfers, which are essential for CO2 fixation. The Delta pH component of proton motive force also plays a role in regulating photosystem II and photoprotection. Increasing proton influx via cyclic electron transfer or decreasing proton efflux via ATP synthase regulation can adjust Delta pH. However, high cyclic electron transfer in the absence of ATP synthase regulation is insufficient for photoprotection of photosystem I.