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Zostera marina, a fully submerged marine angiosperm with a unique evolutionary history associated with its terrestrial origin, has distinct photochemical characteristics caused by its oxygen-evolving complex (OEC) being prone to deactivation in visible light. Based on the present phylogenetic analysis, the chloroplast NADPH dehydrogenase-like (NDH) complex was found to be completed in of Z. marina, unlike other marine plants, suggesting its crucial role. Thus, the responses of electron transport to irradiation were investigated through multiple chlorophyll fluorescence techniques and Western blot analysis. Moreover, the respective contribution of the two photosystem I cyclic electron flow (PSI-CEF) pathways to the generation of trans-thylakoid proton gradient (∆pH) was also examined using inhibitors. The contributions of the two PSI-CEF pathways to ∆pH were similar; furthermore, there was a trade-off between the two pathways under excess irradiation: the PGR5/L1-dependent PSI-CEF decreased gradually following its activation during the initial illumination, while NDH-dependent PSI-CEF was activated gradually with exposure duration. OEC inactivation was continuously under excess irradiation, which exhibits a positive linear correlation with the activation of NDH-dependent PSI-CEF. We suggest that PGR5/L1-dependent PSI-CEF was preferentially activated to handle the excess electron caused by the operation of OEC during the initial illumination. Subsequently, the increasing OEC inactivation with exposure duration resulted in a deficit of electrons. Limited electrons from PSI might preferentially synthesize NADPH, which could support the function of NDH-dependent PSI-CEF to generate ∆pH and ATP via reducing ferredoxin, thereby maintaining OEC stability.