A novel PGRL1 paralog refined the control of photoprotection in grasses and facilitated cell specialisation in C4 photosynthesis

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 C4 photosynthesis--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 to PGRL1 present in all photosynthetic organisms, grasses evolved a new paralog, PGRL1{beta}. AlphaFold3 modelling of predicted PGRL1 dimers suggests that the lumenal regions of PGRL1 monomers are linked by specific hydrogen bonds whereas PGRL1{beta}s lumenal regions 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 of PGRL1 in mesophyll cells and PGRL1{beta} in bundle sheath cells of NADP-ME C4 grasses maize, sorghum, and Setaria viridis. We propose that the mixed PGRL1/{beta} system enabled a better balancing between Photosystem I protection and Photosystem II activity depending on environmental conditions. Therefore, the emergence of PGRL1{beta} contributed to the ecological dominance of grasses and the superior efficiency of NADP-ME C4 photosynthesis.