Molecular evolution of C4 photosynthesis in grasses using comparative transcriptomics

The evolution of adaptations, some of impressive complexity, help organisms to survive in a variety of environments. However, evolutionary innovations are often restricted to certain taxonomic groups with evolutionary precursors. Evolutionary novelties usually arise through the co-option of pre-existing genes into new functions and by comparing organisms with and without the trait of interest, the ancestral state of the co-opted elements can be inferred. This allows us to identify the properties that facilitated their co-option, and therefore increase the evolvability of the complex trait itself. Such comparative studies can gain their power by comparing convergent phenotypes, which provide natural replicates. One example of a convergent complex trait is C4 photosynthesis, an adaptation that results from the coordinated action of multiple enzymes to boost primary productivity in tropical conditions. It evolved more than 62 times in flowering plants, with at least 22 independent origins within the grass family alone. I studied the molecular evolution of coding genes and differential expression patterns in C4 and non-C4 grasses and my research showed: I) that ancestrally highly expressed genes copies had been preferentially co-opted for the C4 pathway; II) that the emergence of a C4 pathway in some taxa required the increased expression of just a few key C4 genes. In addition, III) some C4 genes were transferred across species boundaries and that IV) reticulate evolution punctuated the history of grasses, potentially promoting the spread of adaptive features. Together, these results lead to a new model of C4 evolution, where some components are first accumulated for reasons unrelated to C4, but serve as preadaptations that then allow the transition to a rudimentary C4 pathway via few changes. This event creates strong selective pressure for improvements of the C4 trait over long evolutionary times, and involves important re-programming of gene expression patterns, and impressive parallel adaptation of the translated proteins. Biochemical predisposition likely explains the recurrent C4 origins, as seen in grasses. The recurrent transfer of C4-adaptive loci across species might further have contributed to the observed bursts of C4 lineages in some parts of the grass phylogeny.