The interplay between LHCSR and PSBS proteins provides photoprotection in Chlamydomonas reinhardtii pgr5 mutant under high light

Abstract

Cyclic electron transport (CET) is a vital alternative route that protects against photodamage and aids in energy production. This process depends on proton gradient regulation 5 (PGR5) and PGRL1-dependent pathways associated with CET. The exact roles of these proteins in photosystem I photochemistry under prolonged high light conditions are not fully understood. Continuous light adaptation hinges on two critical mechanisms: alterations in the proton motive force (pmf) and adjustments in the ratio of proteins activated by high light that dissipate excess light through non-photochemical quenching (NPQ). To explore this, we studied pgrl1 and pgr5 mutants to gauge their roles in balancing photochemistry and photoacclimation. These mutants showed inhibited growth, reduced photosynthetic efficiency, and a lowered pmf, leading to diminished non-photochemical energy quenching (qE) under high light. Prolonged high light exposure slowed down unregulated energy losses Y(NO), and relaxation helped regulate photosynthetic activity by increasing photoinhibitory quenching (qI), thus preventing further damage to the photosystem. The precise balance between the two pmf components, ΔpH and Δψ, is critical for controlling photochemistry and photoacclimation, yet remains elusive. In pgr5 reduced pmf led to an accumulation of cytochrome b₆f under high light, and a decrease in the ΔpH component and increased the Δψ component's role in photosynthetic acclimation. Notably, light-harvesting complex stress response protein 3 (LHCSR3) showed decreased expression in pgrl1, whereas pgr5 exhibited no expression of both LHCSR3 and LHCSR1 under high-light conditions. Moreover, continuous increase in PSBS protein accumulation in pgr5 suggests enhanced photoprotection in the absence of LHCSR3 under high light. The study provides significant insights into how CET regulates photoprotective proteins LHCSR and PSBS, influencing Chlamydomonas' survival strategies.