A novelPGRL1paralog refined the control of photoprotection in grasses and facilitated cell specialisation in C₄photosynthesis

Abstract

One of the major events in plant history is the emergence of grasses (Poaceae), which colonised previously uninhabitable open land areas. Some grasses later evolved C4photosynthesis - operating between mesophyll and bundle sheath cells - becoming the most productive and resilient plants on Earth. We investigated whether a key regulator of photoprotection PGR5-LIKE PHOTOSYNTHETIC PHENOTYPE 1 (PGRL1), essential for survival of plants under fluctuating light, facilitated the adaptation of grasses to the open environments. We found that, in addition toPGRL1αpresent in all photosynthetic organisms, grasses evolved a new paralog,PGRL1β. AlphaFold3 modelling of predicted PGRL1 dimers suggests that the lumenal regions of PGRL1α monomers are linked by specific hydrogen bonds whereas lumenal regions of PGRL1β show primarily hydrophobic interactions. These differences likely result in distinct modes of regulation of photoprotection offered by the two paralogs which is supported by predominant expression ofPGRL1αin mesophyll cells andPGRL1βin bundle sheath cells of NADP-ME C4grasses maize, sorghum, andSetaria viridis. We propose that the mixed PGRL1α/β system enabled a better balancing between Photosystem I protection and Photosystem II activity depending on environmental conditions. Therefore, the emergence of PGRL1β contributed to the ecological dominance of grasses and the superior efficiency of NADP-ME C4photosynthesis.