PGR5-PGRL1-Dependent Cyclic Electron Transport Modulates Linear Electron Transport Rate in Arabidopsis thaliana

Abstract

Plants need tight regulation of photosynthetic electron transport for survival and growth under environmental and metabolic conditions. For this purpose, the linear electron transport (LET) pathway is supplemented by a number of alternative electron transfer pathways and valves. In Arabidopsis, cyclic electron transport (CET) around photosystem I (PSI), which recycles electrons from ferrodoxin to plastoquinone, is the most investigated alternative route. However, the interdependence of LET and CET and the relative importance of CET remain unclear, largely due to the difficulties in precise assessment of the contribution of CET in the presence of LET, which dominates electron flow under physiological conditions. We therefore generated Arabidopsis mutants with a minimal water-splitting activity, and thus a low rate of LET, by combining knockout mutations in PsbO1, PsbP2, PsbQ1, PsbQ2, and PsbR loci. The resulting Δ5 mutant is viable, although mature leaves contain only ∼ 20% of wild-type naturally less abundant PsbO2 protein. Δ5 plants compensate for the reduction in LET by increasing the rate of CET, and inducing a strong non-photochemical quenching (NPQ) response during dark-to-light transitions. To identify the molecular origin of such a high-capacity CET, we constructed three sextuple mutants lacking the qE component of NPQ (Δ5 npq4-1), NDH-mediated CET (Δ5 crr4-3), or PGR5-PGRL1-mediated CET (Δ5 pgr5). Their analysis revealed that PGR5-PGRL1-mediated CET plays a major role in ΔpH formation and induction of NPQ in C3 plants. Moreover, while pgr5 dies at the seedling stage under fluctuating light conditions, Δ5 pgr5 plants are able to survive, which underlines the importance of PGR5 in modulating the intersystem electron transfer.

A chloroplast thylakoid lumen protein is required for proper photosynthetic acclimation of plants under fluctuating light environments

“…S13 and S14 C-F). These data support published results demonstrating normal growth of npq1 and npq4 mutants under growth chamber fluctuating light conditions (46)(47)(48). In contrast, the PSII repair-defective mutants were smaller than wild type in the greenhouse, and all but one had significant reductions in PSII activity (Figs.…”

“…This regulatory complexity is illustrated when considering studies with NPQ-deficient npq1 and npq4 mutants. The observation that npq plants showed normal growth under greenhouse and growth chamber fluctuating light conditions (46)(47)(48) (Fig. 5C and SI Appendix, Figs.…”

PROTON GRADIENT REGULATION 5 supports linear electron flow to oxidize photosystem I

“…Furthermore, Fisher and Kramer () reported that Fd and NADPH‐dependent chlorophyll fluorescence rise is achieved by electron donation from Fd to PSII but not PQ‐pool, and the activity was quite small which cannot explain the drastic phenotype of pgr5 mutants. Therefore, it is doubtful whether chlorophyll fluorescence rise assesses the activity of Fd‐dependent CEF‐PSI, and the physiological relevance of PGR5/PGRL1‐dependent CEF is still under debate (Nandha et al , Suorsa et al , , Tikkanen et al , Mosebach et al ). The discordance of PGR5/PGRL1 function would be derived from the lack of direct assessment of Fd during photosynthesis.…”

Flavodiiron Protein Substitutes for Cyclic Electron Flow without Competing CO2 Assimilation in Rice

“…One pathway is mediated through the Fd-dependent PQ reduction, which is sensitive to antimycin A. Two proteins, PROTON GRADIENT REGULATION5 (PGR5; Munekage et al, 2002) and PGR5-like Photosynthetic Phenotype1 (PGRL1; DalCorso et al, 2008) are essential for the pathway to substantially function, although it remains obscure how these proteins are involved in this electron flow (Miyake, 2010;Kramer and Evans, 2011;Strand et al, 2016;Suorsa et al, 2016). The other pathway is mediated by chloroplast NADH dehydrogenase-like (NDH) complex (Yamamoto et al, 2011;Peltier et al, 2016).…”