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
1O2 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.