C4 eudicots are not younger than C4 monocots

Abstract

C₄ photosynthesis is a plant adaptation to high levels of photorespiration. Physiological models predict that atmospheric CO₂ concentration selected for C₄ grasses only after it dropped below a critical threshold during the Oligocene (∼30 Ma), a hypothesis supported by phylogenetic and molecular dating analyses. However the same models predict that CO₂ should have reached much lower levels before selecting for C₄ eudicots, making C₄ eudicots younger than C₄ grasses. In this study, different phylogenetic datasets were combined in order to conduct the first comparative analysis of the age of C₄ origins in eudicots. Our results suggested that all lineages of C₄ eudicots arose during the last 30 million years, with the earliest before 22 Ma in Chenopodiaceae and Aizoaceae, and the latest probably after 2 Ma in Flaveria. C₄ eudicots are thus not globally younger than C₄ monocots. All lineages of C₄ plants evolved in a similar low CO₂ atmosphere that predominated during the last 30 million years. Independent C₄ origins were probably driven by different combinations of specific factors, including local ecological characteristics such as habitat openness, aridity, and salinity, as well as the speciation and dispersal history of each clade. Neither the lower number of C₄ species nor the frequency of C₃–C₄ intermediates in eudicots can be attributed to a more recent origin, but probably result from variation in diversification and evolutionary rates among the different groups that evolved the C₄ pathway.