PSII photoinhibition as a protective strategy against PSI photoinhibition: Maintaining PSI in an oxidized state by suppressing PSII activity under environmental stress

Photosystem I (PSI) can be photoinhibited by excessive electron flow from Photosystem II (PSII), causing serious growth inhibition due to PSIs limited repair capacity. In contrast, PSII is more susceptible to photoinhibition under stress but has an efficient repair system. Consequently, PSII photoinhibition is considered a protective mechanism that mitigates PSI over-reduction. However, this photoprotective role under environmental stress remains unexplored in intact plants without using mutants or chemical treatments. To address this, we examined the relationship between PSII photoinhibition and susceptibility to PSI photoinhibition under two representative stresses that selectively induce PSI photoinhibition: chilling stress and fluctuating light, using A. thaliana and cucumber. Under chilling stress, A. thaliana exhibited marked PSII photoinhibition and maintained active PSI, whereas cucumber showed insufficient PSII downregulation and suffered PSI photoinhibition. In addition, when fluctuating light treatment was applied to plants with various Fv/Fm (the maximum quantum yield of PSII), plants with reduced Fv/Fm maintained oxidized PSI, and PSI photoinhibition progressed slowly. The susceptibility to PSI photoinhibition under fluctuating light strongly correlated with Fv/Fm, providing clear evidence that PSII photoinhibition protects PSI in vivo. Interestingly, even in plants where P700 remained oxidized during saturation pulses due to PSII photoinhibition, the iron-sulfur clusters (Fe-S clusters) remained reduced. However, the re-oxidation rate of reduced Fe-S clusters was enhanced in PSII-photoinhibited plants, suggesting that charge recombination to P700+ with reduced components on the acceptor side would suppress ROS generation downstream of PSI. This study clarifies how PSII photoinhibition suppresses PSI photoinhibition and prevents ROS-induced damage in wild-type plants under environmental stress.