Clusia genomes shed light on the evolution and diversity of crassulacean acid metabolism physiotypes

Abstract

More than 200 years ago, Alexander von Humboldt described a tree of the genus Clusia for its ability to perform crassulacean acid metabolism (CAM). This drought-adaptive metabolism allows plants to maintain photosynthesis under water limitation by temporally separating CO₂ uptake and fixation. The diversity of CAM physiotypes has fueled a debate about evolutionary constraints and the feasibility of engineering CAM into C₃ crops. The genus Clusia displays an exceptional diversity of photosynthetic physiotypes, yet genome sequences and genomic mechanisms generating this diversity remain unresolved. Here, we sequence and compare the genomes of three Clusia species spanning weak, inducible, and strong CAM. We show that polyploidization followed by transposon-mediated genic diploidization could have shaped CAM-related gene families, particularly those controlling phosphoenol-pyruvate recycling via phosphorolytic leaf starch metabolism. Our results indicate that whole-genome duplication coupled to diploidization might have driven diversification of CAM physiotypes in Clusia, providing a genomic framework for understanding CAM diversity and evolution.