Chlororespiration induces non-photochemical quenching of chlorophyll fluorescence during darkness in lichen chlorobionts

Abstract

Lichens and their algal partners are desiccation-tolerant organisms and as such survive after the complete loss of water. This trait is the consequence of several physiological, biochemical and structural features, including specific mechanisms dissipating excess light to avoid photooxidative stress. The maximum quantum yield of photosystem II (PSII; Fv/Fm) is widely used as a sensitive indicator of photosynthetic performance and is calculated after complete relaxation in darkness of the fluorescence quenching associated with active light energy dissipation mechanisms. Unexpectedly, we observed that lichens and isolated chlorobionts (chlorophyte symbionts in lichen) maintained in darkness for several hours showed a strong decrease in the ratio Fv/Fm, which was reversible after re-illumination. We analyzed this dark-induced Fv/Fm decay in the chlorobiont Asterochloris erici through steady-state and fast-induction kinetics of chlorophyll a fluorescence and simultaneous P700 oxidation measurements. We found that the gradual decay of Fv/Fm in darkness was caused by reversible dark-induced inactivation of some PSII reaction centers that was accompanied by a decrease in the flux of electrons to PSI. Darkness induced the plastoquinone-reductase activity associated with chlororespiration and the phosphorylation of light harvesting complex (LHC). We propose that upon phosphorylation the LHC detaches from PSII, resulting in a decrease of exciton-trapping by PSII reaction centers and, consequently, an increased dissipation of light energy. This mechanism probably serves an ecophysiological function in lichens to prevent the damage at dawn or under strong fluctuating light conditions when lichens are in a hydrated state.