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

In higher plants, light drives the linear photosynthetic electron transport reaction from H₂ O to electron sinks, which is called the linear electron flow (LEF). LEF activity should be regulated depending on electron sinks; otherwise excess electrons accumulate in the thylakoid membranes and stimulate reactive oxygen species (ROS) production in photosystem I (PSI), which causes oxidative damage to PSI. To prevent ROS production in PSI, PSI should be oxidized during photosynthesis, and PROTON GRADIENT REGULATION 5 (PGR5) and PGR like 1 (PGRL1) are important for this oxidation. PGR5 and PGRL1 are recognized as a component of ferredoxin-dependent cyclic electron flow around PSI (Fd-CEF-PSI), however there is no direct evidence for the significant operation of Fd-CEF-PSI during photosynthesis in wild-type (WT) plants. Thus, electron distribution by PGR5 and PGRL1 between Fd-CEF-PSI and LEF is still elusive. Here, we show direct evidence that Fd-CEF-PSI activity is minor during steady-state photosynthesis by measuring the Fd redox state in vivo in Arabidopsis thaliana. We found that Fd oxidation rate is determined by LEF activity during steady-state photosynthesis in WT. On the other hand, pgr5 and pgrl1 showed lower electron transport efficiency from PSI to electron sinks through Fd during steady-state photosynthesis. These results demonstrate that electrons are exclusively consumed in electron sinks through Fd, and the phenotypes of pgr5 and pgrl1 are likely caused by the disturbance of the LEF between PSI and electron sinks. We suggest that PGR5 and PGRL1 modulate the LEF according to electron sink activities around PSI.