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

Oxygenic photosynthesis generates the initial energy source that fuels nearly all life on Earth. At the heart of the process are the photosystems, which are pigment binding multiprotein complexes that catalyze the first step of photochemical conversion of light energy into chemical energy. Here, we investigate the molecular evolution of the plastid-encoded photosystem subunits at single-residue resolution 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 modeling of these adaptive substitutions, we uncover the impact of these changes on the predicted properties of the photosystems, focusing on their effects on cofactor binding and intersubunit interface formation. By analyzing these cohorts of changes, we reveal that evolution has repeatedly altered the interaction between Photosystem II and its D1 subunit in a manner that is predicted to reduce the energetic barrier for D1 turnover and photosystem repair. Together, these results provide insight into the trajectory of photosystem adaptation during angiosperm evolution.