The protective role of chloroplast NADH dehydrogenase-like complex (NDH) against PSI photoinhibition under chilling stress.

Chilling stress induces photosystem I (PSI) photoinhibition in various plants, severely impairing their growth. However, the mechanisms suppressing chilling-induced PSI photoinhibition remain unclear. To identify factors preventing PSI photoinhibition, we compared two cucumber cultivars with different susceptibilities to PSI photoinhibition and chilling stress tolerance. Chilling stress caused uncoupling of thylakoid membrane in both cultivars, as previously reported. However, in the chilling-sensitive cultivar, electron efflux from ferredoxin (Fd) was more restricted under chilling stress, resulting in over-reduction of PSI. This over-reduction was observed not only under chilling stress but also under limited CO2 condition, suggesting that the lower alternative electron flow activity contributes to the cultivar difference in PSI photoinhibition. Indeed, the chilling-sensitive cultivar lost the activity of the chloroplast NADH dehydrogenase-like complex (NDH) due to destabilization of the PSI-NDH supercomplex under chilling stress, resulting in severe Fd over-reduction. By contrast, the chilling-tolerant cultivar maintained NDH activity and suppressed reactive oxygen species and PSI photoinhibition during chilling stress. This study provides evidence that NDH functions as a crucial electron sink to prevent PSI photoinhibition and provides new insights into the mechanisms underlying low-temperature stress tolerance.