PSII Photoinhibition as a Protective Strategy: Maintaining an Oxidative State of PSI by Suppressing PSII Activity...

Photosystem I (PSI) can be photoinhibited by excessive electron flow from Photosystem II (PSII), causing serious growth inhibition due to PSI's limited repair capacity. In contrast, PSII is more prone to photoinhibition under environmental stress, but it can recover efficiently. 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 PSI protection under two representative stresses that selectively induce PSI photoinhibition: chilling stress and fluctuating light, using A. thaliana and cucumber plants. Under chilling stress, A. thaliana exhibited marked PSII photoinhibition and maintained active PSI, whereas cucumber showed insufficient PSII downregulation and suffered from 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 an 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. Interestingly, even in plants where P700 remained oxidized due to PSII photoinhibition, the Fe-S clusters remained reduced during saturation pulses. However, the re-oxidation of reduced Fe-S clusters was enhanced in PSII-photoinhibited plants, suggesting that charge recombination to P700⁺ with reduced components on the PSI acceptor side or accelerated processes downstream of ferredoxin would suppress ROS generation downstream of PSI. This study clarifies how PSII photoinhibition suppresses PSI photoinhibition and prevents ROS-induced damage under environmental stresses.