Takeuchi, K.; Harimoto, S.; Che, Y.; Kumazawa, M.; Satoh, H.; Maekawa, S.; Miyake, C.; Ifuku, K.

Chilling stress induces photosystem I (PSI) photoinhibition in various plants, severely impairing their growth. However, the mechanisms suppressing chilling-induced PSI photoinhibition remain unclear. This study aimed to identify factors preventing PSI photoinhibition by comparing two cucumber cultivars with different susceptibilities to PSI photoinhibition and chilling stress tolerance. In the chilling-sensitive cultivar, partial degradation of the CF1-{gamma} subunit of chloroplast ATPase led to uncoupling of the thylakoid membrane. In addition, electron efflux from Fe-S clusters downstream of PSI was restricted under chilling stress, resulting in highly reduced Fe-S clusters. Notably, this PSI over-reduction in the chilling-sensitive cultivar was observed not only under chilling stress but also under fluctuating light conditions, limited CO2 conditions, and during the transition from darkness to light, suggesting that cyclic electron flow contributes to cultivar differences in PSI photoinhibition. Indeed, the chilling-tolerant cultivar exhibited higher activity of the chloroplast NADH dehydrogenase-like complex (NDH) and suppressed reactive oxygen species (ROS) accumulation during the early stages of chilling stress. In contrast, in the chilling-sensitive cultivar, destabilization of PSI-NDH supercomplex under chilling stress led to the loss of NDH activity, resulting in severe PSI over-reduction. This study provides evidence that NDH acts as a crucial electron sink to prevent PSI photoinhibition and provides new insights into the mechanisms underlying low-temperature stress tolerance.