Evolutionary history of CAM photosynthesis in Neotropical Clusia: insights from genomics, anatomy, physiology and climate

Clusia is a remarkable genus of Neotropical woody plants as its members engage in either C-3 photosynthesis or employ, to varying degrees, crassulacean acid metabolism (CAM) photosynthesis. Information about the evolutionary history of CAM in Clusia is scarce. Restriction site-associated sequencing of 64 species (20% of the genus) provided strong support for most of the previously recognized nine lineages. Ancestral reconstruction using maximum parsimony or maximum likelihood under a one-rate model suggested that CAM evolved at least four times independently from a most recent common ancestor (MRCA) with C-3, whereas a maximum likelihood two-rate model suggested that CAM was already present in the MRCA followed by reversions to C-3 in several lineages. Phylogenetic generalized least square analysis assessed variation in seven leaf anatomical traits and CAM activity measured as delta C-13. Results indicate that CAM is highly correlated with palisade mesophyll layer thickness and cell size. In addition, correlation between 19 bioclimatic variables and delta C-13 was evaluated. It was found that CAM is positively correlated with habitats with a more severe dry season and greater precipitation seasonality. Since CAM is weakly and/or only periodically expressed in many Clusia spp., and thus not readily reflected in delta C-13, future analysis of phylogenetically-informed CAM expression in Clusia must include physiological measurements such as CO2 exchange and/or diel changes in leaf acidity for each species under investigation.

Automated summary

The study found that CAM photosynthesis in Clusia evolved independently at least four times from a common ancestor with C-3 photosynthesis, and is highly correlated with leaf anatomical traits and habitat characteristics. Future studies on CAM expression in Clusia need to include physiological measurements to accurately assess its expression.