The PSI-NDH supercomplex prevents chilling-induced PSI photoinhibition

Chilling stress induces photosystem I (PSI) photoinhibition in cucumber (Cucumis sativus L.). This process is associated with insufficient activity of the chloroplast NADH dehydrogenase-like complex (NDH). However, whether the importance of NDH can be generalized to other species and how NDH function is impaired remain unclear. We first examined whether NDH is essential for PSI protection under chilling stress using an NDH-deficient rice (Oryza sativa L.) mutant. The NDH-deficient rice exhibited pronounced PSI photoinhibition under chilling stress. By contrast, rice expressing flavodiiron protein (FLV), which functions as an alternative electron acceptor downstream of PSI, did not exhibit PSI photoinhibition under chilling stress, demonstrating that the electron sink capacity of NDH is important for PSI protection under chilling stress. Furthermore, in cucumber, chilling stress destabilizes the PSI-NDH supercomplex, leading to NDH monomerization and a consequent loss of NDH activity. This NDH monomerization is likely attributable to chilling-induced damage to the light-harvesting complex Lhca, which mediates the association between PSI and NDH. Together, these results indicate that NDH protects PSI from photoinhibition under chilling stress, and that chilling-induced destabilization of the PSI-NDH supercomplex represents a key molecular mechanism underlying PSI over-reduction and photoinhibition in cucumber.