Supercharged PGR5-dependent cyclic electron transfer compensates for mis-regulated chloroplast ATP synthase

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 (CBBC). The dominant ΔpH component of the pmf also plays a photoprotective role in regulating photosystem II (PSII) light harvesting efficiency, through non-photochemical quenching (NPQ), and cytochrome b6f (cytb6f) to photosystem I (PSI) electron transfer, via photosynthetic control. ΔpH 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 ΔpH control to photoprotection are not well understood. Here, we show that an Arabidopsis ATP synthase mutant (hope2) with 40% higher proton efflux, has supercharged CET. Double crosses of hope2 with the CET-deficient pgr5 and ndho lines reveal that PGR5-dependent CET is the major pathway contributing to higher proton influx. PGR5-dependent CET allows hope2 to maintain wild-type levels of ΔpH, CO2 fixation and NPQ, however photosynthetic control remains absent, and PSI is acceptor-side limited. Therefore, high CET in the absence of ATP synthase regulation is insufficient for PSI photoprotection.