ORIGINAL ARTICLE doi:10.1111/j.1558-5646.2010.01168.x COMPLEX EVOLUTIONARY TRANSITIONS AND THE SIGNIFICANCE OF C3–C4 INTERMEDIATE FORMS OF PHOTOSYNTHESIS IN MOLLUGINACEAE Pascal-Antoine Christin,1,2,3 Tammy L. Sage, 4 Erika J. Edwards,1 R. Matthew Ogburn,1 Roxana Khoshravesh,4 and Rowan F. Sage4 1Department of Ecology and Evolutionary Biology, Brown University, 80 Waterman St, Box G-W, Providence, Rhode Island 02912 2Department of Ecology and Evolution, Biophore, Quartier Sorge, University of Lausanne, 1015 Lausanne, Switzerland 3E-mail:
[email protected] 4Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, Ontario M5S3B2, Canada Received June 11, 2010 Accepted October 3, 2010 C4 photosynthesis is a series of biochemical and structural modifications to C3 photosynthesis that has evolved numerous times in flowering plants, despite requiring modification of up to hundreds of genes. To study the origin of C4 photosynthesis, we reconstructed and dated the phylogeny of Molluginaceae, and identified C4 taxa in the family. Two C4 species, and three clades with traits intermediate between C3 and C4 plants were observed in Molluginaceae. C3–C4 intermediacy evolved at least twice, and in at least one lineage was maintained for several million years. Analyses of the genes for phosphoenolpyruvate carboxylase, akeyC4 enzyme, indicate two independent origins of fully developed C4 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 C3–C4 and C4 photosynthesis is likely due to several traits that acted as developmental enablers.