Restricting electron flow at cytochrome b6f when downstream electron acceptors are severely limited

Abstract

Photosynthetic organisms frequently experience abiotic stress that restricts their growth and development. Under such circumstances, most absorbed solar energy cannot be used for CO2 fixation and can cause the photoproduction of reactive oxygen species (ROS) that can damage the photosynthetic reaction centers of photosystem I and II (PSI and PSII), resulting in a decline in primary productivity. This work describes a biological ‘switch’ in the green alga Chlamydomonas reinhardtii that reversibly restricts photosynthetic electron transport (PET) at the cytochrome b6f (Cyt b6f) complex when the capacity for accepting electrons downstream of PSI is severely limited. We specifically show this restriction in STARCHLESS6 (sta6) mutant cells, which cannot synthesize starch when they are limited for nitrogen (growth inhibition) and subjected to a dark-to-light transition. This restriction represents a form of photosynthetic control that causes diminished electron flow to PSI and thereby prevents PSI photodamage but does not appear to rely on a ΔpH. Furthermore, when electron flow is restricted, the plastid alternative oxidase (PTOX) becomes active, functioning as an electron valve that dissipates some excitation energy absorbed by PSII and allows the formation of a proton motive force (PMF) that would drive some ATP production [potentially sustaining PSII repair and non-photochemical quenching (NPQ)]. The restriction at the Cyt b6f complex can be gradually relieved with continued illumination. This study provides insights into how photosynthetic electron transport responds to a marked reduction in availability of downstream electron acceptors and the protective mechanisms involved.

A congestion downstream of PSI causes the over-reduction of the electron transport chain inpgr5independent of membrane energization

“…However, because no parallel assessment of changes in NADPH levels was done, it is not possible to conclude on the primary limiting factor for photosynthetic electron transport and metabolism from these data. Recently, in C. reinhardtii , a severe restriction in starch biosynthesis was shown to cause an acceptor side limitation of PSI and result in over-reduction of the entire electron transport chain, from the PSII acceptor side to restricted light-induced oxidation of cytochrome f (Saroussi et al, 2023). These defects closely resemble those in pgr5 , demonstrating that also a defect in the reactions of primary chloroplast metabolism might be causal for the defects observed in pgr5 .…”