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

Abstract

The regulation of proton motive force (pmf) via ATP synthase activity is a critical mechanism by which photosynthetic organisms maintain redox homeostasis and activate photoprotective responses under fluctuating light conditions. Here, we used time-resolved electrochromic shift (ECS) measurements to investigate pmf dynamics across a range of photosynthetic organisms. Our results reveal that ATP synthase is dynamically regulated during light fluctuations, but in Arabidopsis thaliana could this regulation could not be explained by the known light-induced reduction of the CF{square}{gamma} subunit, suggesting alternative control mechanisms. The PROTON GRADIENT REGULATION 5 (PGR5) protein, previously proposed to facilitate cyclic electron transport (CET), also has a potential role in ATP synthase regulation. The physiological role of cyanobacterial Pgr5 has remained elusive. We characterised a {Delta}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. Furthermore, interaction between AtPGR5 and AtCF{square}{gamma} suggests that PGR5 functions as a conserved inhibitor of ATP synthase under high light, contributing to pmf retention and photoprotection. HighlightPGR5 is involved in regulation of ATP synthase in fluctuating light conditions across photosynthetic organisms in a manner that depends on the thiol redox state of the chloroplast or cell.