Widespread adaptive evolution in the photosystems of angiosperms provides new insight into the evolution of photosystem II repair

Oxygenic photosynthesis generates the initial energy source which fuels nearly all life on earth. At the heart of the process are the photosystems, pigment binding multi-protein complexes that catalyse the first step of photochemical conversion of light energy into chemical energy. Here, we investigate the molecular evolution at single residue resolution of the plastid-encoded subunits of the photosystems across 773 angiosperm species. We show that despite an extremely high level of conservation, 7% of residues in the photosystems, spanning all photosystem subunits, exhibit hallmarks of adaptive evolution. Through in silico modelling of these adaptive substitutions we uncover the impact of these changes on the properties of the photosystems, focussing on their effects on co-factor binding and the formation of inter-subunit interfaces. We further reveal that evolution has repeatedly destabilised the interaction photosystem II and its D1 subunit, thereby reducing the energetic barrier for D1 turn-over and photosystem repair. Together, these results provide new insight into the trajectory of photosystem evolution during the radiation of the angiosperms.