Adaptive Evolution of C4 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.