Multiple photosynthetic transitions, polyploidy, and lateral gene transfer in the grass subtribe Neurachninae

The Neurachninae is the only grass lineage known to contain C3, C4, and C3–C4 intermediate species, and as such has been suggested as a model system for studies of photosynthetic pathway evolution in the Poaceae; however, a lack of a robust phylogenetic framework has hindered this possibility. In this study, plastid and nuclear markers were used to reconstruct evolutionary relationships among Neurachninae species. In addition, photosynthetic types were determined with carbon isotope ratios, and genome sizes with flow cytometry. A high frequency of autopolyploidy was found in the Neurachninae, including in Neurachne munroi F.Muell. and Paraneurachne muelleri S.T.Blake, which independently evolved C4 photosynthesis. Phylogenetic analyses also showed that following their separate C4 origins, these two taxa exchanged a gene encoding the C4 form of phosphoenolpyruvate carboxylase. The C3–C4 intermediate Neurachne minor S.T.Blake is phylogenetically distinct from the two C4 lineages, indicating that intermediacy in this species evolved separately from transitional stages preceding C4 origins. The Neurachninae shows a substantial capacity to evolve new photosynthetic pathways repeatedly. Enablers of these transitions might include anatomical pre-conditions in the C3 ancestor, and frequent autopolyploidization. Transfer of key C4 genetic elements between independently evolved C4 taxa may have also facilitated a rapid adaptation of photosynthesis in these grasses that had to survive in the harsh climate appearing during the late Pliocene in Australia.