EVOLUTION OF LEAF ANATOMY AND PHOTOSYNTHETIC PATHWAYS IN PORTULACACEAE

Premise of the study: Portulacaceae is a family with a remarkable diversity in photosynthetic pathways. This lineage not only has species with different C-4 biochemistry (NADP-ME and NAD-ME types) and C-3-C-4 intermediacy, but also displays different leaf anatomical configurations. Here we addressed the evolutionary history of leaf anatomy and photosynthetic pathways in Portulacaceae. Methods: Photosynthetic pathways were assessed based on leaf anatomy and carbon isotope ratios. Information on the NADP-ME and NAD-ME C-4 variants was obtained from the literature. The evolutionary relationships and trait evolution were estimated under a Bayesian framework, and divergence times were calibrated using the ages obtained in a previous study. Key results: C-4 photosynthesis is the main pathway in Portulacaceae. One clade (Cryptopetala), however, includes species that have non-Kranz anatomy and C-3 type isotope values, two of which are C-3-C-4 intermediates. The ancestral leaf anatomy for the family is uncertain. The analysis showed one origin of the C-4 pathway, which was lost in the Cryptopetala clade. Nevertheless, when a second analysis was performed taking into account the limited number of species with NAD-ME and NADP-ME data, a secondary gain of the C-4 pathway from a C-3-C-4 intermediate was inferred. Conclusions: The C-4 pathway evolved ca. 23 Myr in the Portulacaceae. The number of times that the pathway evolved in the family is uncertain. The diversity of leaf anatomical types and C-4 biochemical variants suggest multiple independent origins of C-4 photosynthesis. Evidence for a switch from C-4 to C-3-C-4 intermediacy supports the hypothesis that intermediates represent a distinct successful strategy.