PGR5 is needed for redox-dependent regulation of ATP synthase both in chloroplasts and in cyanobacteria

Control of the proton motive force (pmf) via regulation of ATP synthase constitutes a key mechanism for photosynthetic organisms to maintain redox balance and induce photoprotective mechanisms under light fluctuations. Using time-resolved electrochromic shift measurements in various photosynthetic organisms, we found that ATP synthase is dynamically regulated during light fluctuations. While light-induced reduction of the CF1γ subunit is known to activate chloroplast ATP synthase, it did not account for the regulation in fluctuating light in Arabidopsis thaliana, suggesting alternative mechanisms. The PROTON GRADIENT REGULATION 5 (PGR5) protein is important for photoprotection in algal and plant chloroplasts. PGR5 has been proposed to facilitate cyclic electron transport around PSI (CET), but it also affects ATP synthase activity. The physiological role of cyanobacterial Pgr5 has remained elusive. We characterised a ∆pgr5 mutant of Synechocystis sp. PCC 6803 and investigated pmf dynamics in pgr5 mutants of Chlamydomonas reinhardtii, Arabidopsis, and the C4 grass Setaria viridis. While PGR5 was not required for CET in Synechocystis, it was needed for downregulating ATP synthase under high irradiance in all tested organisms via a thiol redox state dependent mechanism. As AtPGR5 interacted with AtCF1γ, PGR5 may have a conserved function as an inhibitor of ATP synthase.