Loss of PSAE redirects PGRL1 to photosystem I and enhances PGR5-dependent cyclic electron transfer in Arabidopsis

Electrons energised by light energy at photosystem I (PSI) primarily enter the linear photosynthetic electron transfer (LET) or cyclic electron transfer (CET) pathway. The balance between LET and CET activity is a crucial factor in the regulation of photosynthesis, since CET increases the stoichiometry of proton to electron transfer. The additional transmembrane proton gradient ({Delta}pH) triggers feedback control of light harvesting and electron transfer photoprotection via non-photochemical quenching (NPQ) and photosynthetic control (PCON), maintaining the balance between the output of the light reactions and the downstream metabolism. Previously, it was found that Arabidopsis mutants lacking the stromal-facing membrane-extrinsic PSAE subunit of PSI (psae1-3) show enhanced CET activity, decreased LET and lower PSI oxidation in excess light. Here we show that high CET activity in psae1-3 primarily depends on the Proton Gradient Regulation 5 (PGR5)-dependent CET pathway rather than the NDH-dependent pathway. High CET is abolished in the psae1-3 pgr5CAS double mutant. In the psae1-3 ndho double mutant the elevated proton flux and CET are largely maintained; however, CO2 fixation and growth are significantly worsened, indicating that NDH still makes a physiologically meaningful contribution in the psae1-3 background. Biochemical analysis revealed that PGRL1 is redistributed from its normal mixed membrane distribution to become predominantly PSI-associated in psae1-3, providing a physical basis for the enhanced PGR5-dependent CET. These results underscore the primary importance of the PGR5-dependent CET pathway for optimal photosynthesis and CO2 fixation in Arabidopsis and establish the organisation of the PSI acceptor side as a key regulatory determinant of the CET/LET balance.