COMPLEX EVOLUTIONARY TRANSITIONS AND THE SIGNIFICANCE OF C3-C4 INTERMEDIATE FORMS OF PHOTOSYNTHESIS IN MOLLUGINACEAE

C-4 photosynthesis is a series of biochemical and structural modifications to C-3 photosynthesis that has evolved numerous times in flowering plants, despite requiring modification of up to hundreds of genes. To study the origin of C-4 photosynthesis, we reconstructed and dated the phylogeny of Molluginaceae, and identified C-4 taxa in the family. Two C-4 species, and three clades with traits intermediate between C-3 and C-4 plants were observed in Molluginaceae. C-3-C-4 intermediacy evolved at least twice, and in at least one lineage was maintained for several million years. Analyses of the genes for phosphoenolpyruvate carboxylase, a key C-4 enzyme, indicate two independent origins of fully developed C-4 photosynthesis in the past 10 million years, both within what was previously classified as a single species, Mollugo cerviana. The propensity of Molluginaceae to evolve C-3-C-4 and C-4 photosynthesis is likely due to several traits that acted as developmental enablers. Enlarged bundle sheath cells predisposed some lineages for the evolution of C-3-C-4 intermediacy and the C-4 biochemistry emerged via co-option of photorespiratory recycling in C-3-C-4 intermediates. These evolutionarily stable transitional stages likely increased the evolvability of C-4 photosynthesis under selection environments brought on by climate and atmospheric change in recent geological time.