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

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Abstract

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, a key C4 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. Enlarged bundle sheath cells predisposed some lineages for the evolution of C3–C4 intermediacy and the C4 biochemistry emerged via co-option of photorespiratory recycling in C3–C4 intermediates. These evolutionarily stable transitional stages likely increased the evolvability of C4 photosynthesis under selection environments brought on by climate and atmospheric change in recent geological time.

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