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As an alternative electron sink, chlororespiration, comprising the NAD(P)H dehydrogenase complex and plastid terminal plastoquinone oxidase, may play a significant role in sustaining the redox equilibrium between stroma and thylakoid membrane. This study identified a distinct role for chlororespiration in the marine angiosperm Zostera marina, whose oxygen-evolving complex (OEC) is prone to photo-inactivation as a result of its inherent susceptibility to excess irradiation. The strong connectivity between OEC peripheral proteins and key chlororespiratory enzymes, as demonstrated in the interaction network of differentially expressed genes, suggested that the recovery of photo-inactivated OEC was connected with chlororespiration. Chlorophyll fluorescence, transcriptome and Western blot data verified a new physiological role for chlororespiration to function as photoprotection and generate a proton gradient across the thylakoid membrane for the recovery of photo-inactivated OEC. Chlororespiration was only activated in darkness following excess irradiation exposure, which might be related to electron deficiency in the electron transport chain because of the continuous impairment of the OEC. The activation of chlororespiration in Z. marina was prone to proactivity, which was also supported by the further activation of the oxidative pentose-phosphate pathway synthesizing NADPH to meet the demand of chlororespiration during darkness. This phenomenon is distinct from the common assumption that chlororespiration is prone to consuming redundant reducing power during the short transition phase from light to dark.

Chlororespiration Serves as Photoprotection for the Photo-Inactivated Oxygen-Evolving Complex in Zostera marina, a Marine Angiosperm