The rise and fall of the photoinhibition-related energy dissipation qI

Abstract

AbstractPhotosynthesis converts sunlight into chemical energy, sustaining the vast majority of the biosphere. Photosystem II (PSII), the oxygen-forming enzyme that initiates photosynthesis, is however particularly prone to light-induced damage in a process known as photoinhibition, which limits the productivity of both aquatic and land photosynthesis. Photoinhibition is associated with an energy dissipation process of unknown origin, termed qI. Here, we present a detailed biophysical and biochemical in vivo study of qI in model green alga Chlamydomonas reinhardtii. Time-resolved fluorescence measurements demonstrate the origin of qI, and indicate the PSII reaction centre as the site of the quencher. Oxygen-dependence of quenching site formation, but not photoinhibition itself, is shown, suggesting that two types of PSII damage – donor and acceptor-side impairment – can be separated. We then demonstrate that the quenching loss takes place in the absence of PSII repair, and is mediated by the degradation of photoinhibited PSII cores by the FtsH protease. Finally, we integrate data ranging from picoseconds to hours in the context of structure-function excitation energy-transferring membrane patches, revealing the extent of PSII heterogeneity from the onset of photoinhibition until the breakdown of damaged PSII.Graphical AbstractHighlightsUpon photoinhibition, oxygen sensitization results in an irreversible formation of quenching (qI) and inactivation of Photosystem IIqI takes place in the PSII reaction centrePhotoinhibition-induced D1 cleavage is much slower than qI formationFtsH metalloprotease is required to degrade quenching PSII reaction centresA multiscale energy transfer model describes heterogeneity of PSII during photoinhibition