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

The Neurachninae is the only grass lineage known to contain C(3), C(4), and C(3)–C(4) 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 C(4) photosynthesis. Phylogenetic analyses also showed that following their separate C(4) origins, these two taxa exchanged a gene encoding the C(4) form of phosphoenolpyruvate carboxylase. The C(3)–C(4) intermediate Neurachne minor S.T.Blake is phylogenetically distinct from the two C(4) lineages, indicating that intermediacy in this species evolved separately from transitional stages preceding C(4) origins. The Neurachninae shows a substantial capacity to evolve new photosynthetic pathways repeatedly. Enablers of these transitions might include anatomical pre-conditions in the C(3) ancestor, and frequent autopolyploidization. Transfer of key C(4) genetic elements between independently evolved C(4) 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.