Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis

•Three types of flexible mechanisms regulate photosynthetic light harvesting.•The orange carotenoid protein functions in cyanobacterial phycobilisomes.•LHCSR-dependent non-photochemical quenching evolved in algae.•PSBS-dependent non-photochemical quenching evolved in the green lineage.•Mosses represent a transitional state in regulation of light harvesting. All photosynthetic organisms need to regulate light harvesting for photoprotection. Three types of flexible non-photochemical quenching (NPQ) mechanisms have been characterized in oxygenic photosynthetic cyanobacteria, algae, and plants: OCP-, LHCSR-, and PSBS-dependent NPQ. OCP-dependent NPQ likely evolved first, to quench excess excitation in the phycobilisome (PB) antenna of cyanobacteria. During evolution of eukaryotic algae, PBs were lost in the green and secondary red plastid lineages, while three-helix light-harvesting complex (LHC) antenna proteins diversified, including LHCSR proteins that function in dissipating excess energy rather than light harvesting. PSBS, an independently evolved member of the LHC protein superfamily, seems to have appeared exclusively in the green lineage, acquired a function as a pH sensor that turns on NPQ, and eventually replaced LHCSR in vascular plants.