Photoinhibition is the popular topic in plant photosynthesis. However, restricted to experimental systems of in vitro membranes, knowledge of photosystem II (PSII) donor-side photoinhibition remains limited. Here, we report the first in vivo study of the mechanism in the marine higher plant Zostera marina. Preferential oxygen-evolving complex photoinactivation decreased the light-harvesting capacity and enhanced photosystem I cyclic electron flow (CEF). Non-photochemical quenching was inefficient and alternative electron flows, e.g. chlororespiration, Mehler reaction, malic acid synthesis, and photorespiration, remained unactivated, thereby reducing the unnecessary consumption of limited electron resources and maintaining a well carbon assimilation level. At variance with the PSII acceptor-side photoinhibition, the PSII photodamage of Z. marina was not attributed to 1 O 2 but was associated with the long-lived P680 + resulted from the photoinactivated OEC. Furthermore, we provided the novel insights into the PSII donor-side photoinhibition that rare PSII-CEF and ascorbate assumed photoprotective roles in Z. marina, which could donate electrons to the PSII reaction center to prevent the oxidative damage by P680 +. This study addressed an important knowledge gap in PSII donor-side photoinhibition, providing a novel understanding of photosynthetic regulation mechanism responding to light stress.
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