PGR5 is required for efficient Q cycle in the cytochrome b6f complex during cyclic electron flow

Proton Gradient Regulation 5 (PGR5) is involved in the control of photosynthetic electron transfer but its mechanistic role is not yet clear. Several models have been proposed to explain phenotypes such as a diminished steady state proton motive force (pmf) and increased photodamage of photosystem I (PSI). Playing a regulatory role in cyclic electron flow (CEF) around PSI, PGR5 contributes indirectly to PSI protection by enhancing photosynthetic control, which is a pH-dependent downregulation of electron transfer at the cytochrome b6f complex (b6f). Here, we re-evaluated the role of PGR5 in the green alga Chlamydomonas reinhardtii and conclude that pgr5 possesses a dysfunctional b6f. Our data indicate that the b6f low-potential chain redox activity likely operated in two distinct modes - via the canonical Q cycle during linear electron flow and via an alternative Q cycle during CEF, attributing a ferredoxin-plastoquinone reductase activity to the b6f. The latter mode allowed efficient oxidation of the low-potential chain in the WT b6f. A switch between the two Q cycle modes was dependent of PGR5 and relied on unknown stromal electron carrier(s), which were a general requirement for b6f activity. In CEF-favouring conditions the electron transfer bottleneck in pgr5 was the b6f and insufficient flexibility in the low-potential chain redox tuning might account for the mutant pmf phenotype and the secondary consequences. Models of our findings are discussed.