Adaptive evolution of C ₄ photosynthesis through recurrent lateral gene transfer

C ₄ photosynthesis is a complex trait that confers higher productivity under warm and arid conditions [1-3]. It has evolved more than 60 times via the co-option of genes present in C ₃ ancestors followed by alteration of the patterns and levels of expression and adaptive changes in the coding sequences [4-12], but the evolutionary path to C ₄ photosynthesis is still poorly understood. The grass lineage Alloteropsis offers unparalleled opportunities for studying C ₄ evolution, because it includes a C ₃ taxon and five C ₄ species that vary significantly in C ₄ anatomy and biochemistry [13, 14]. Using phylogenetic analyses of nuclear genes and leaf transcriptomes, we show that fundamental elements of the C ₄ pathway in the grass lineage Alloteropsis were acquired via a minimum of four independent lateral gene transfers from C ₄ taxa that diverged from this group more than 20 million years ago. The transfer of genes that were already fully adapted for C ₄ function has occurred periodically over at least the last 10 million years and has been a recurrent source for the optimization of the C ₄ pathway. This report shows that plant-plant lateral nuclear gene transfers can be a potent source of genetic novelty and adaptation in flowering plants.