Adaptive evolution of C(4) photosynthesis through recurrent lateral gene transfer

Abstract

C(4) photosynthesis is a complex trait that confers higher productivity under warm and arid conditions. 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, 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. 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.