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

Abstract

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.

C4 photosynthesis boosts growth by altering physiology, allocation and size

“…For these remaining 52 species, DNA was isolated from dried plant material using the DNeasy Plant Mini Kit (Qiagen Inc., Texas, USA), following the instructions provided. These gDNAs were used as PCR templates to amplify fragments of trnKmatK, ndhF, and ITS, following the protocols and using the primers previously publishe 6,7 . The newly generated sequences were added to those retrieved from NCBI database.…”

“…advantage associated with C 4 photosynthesis (reviewed elsewhere 1,6,7 ). We hypothesize 8 that this inconsistency arises from the large variation in growth rates among ecologically 9 diverse species, coupled with low statistical power arising from small sample sizes.…”

“…Others have argued that it may arise from environmental limitations, or differences in 11 internal resource consumption and allocation between C 3 and C 4 species 6,7 . 12…”

Loss of the Chloroplast Transit Peptide from an Ancestral C3 Carbonic Anhydrase Is Associated with C4 Evolution in the Grass Genus Neurachne

“…This is largely due to a lack of monocot lineages that not only have well-resolved molecular phylogenies but also contain closely related C 3 species, C 4 species, and, importantly, C 3 -C 4 intermediate species that use C 2 photosynthesis. The Neurachninae subtribe recently emerged as a model monocot group for research into the molecular evolution of C 4 photosynthesis, as it contains closely related species using these different photosynthetic biochemistries (Christin et al, 2012). Within Neurachne, the predominant genus in the subtribe, there is a single C 4 species (Neurachne munroi), one C 3 -C 4 intermediate (Neurachne minor, a type I C 2 species; Sage et al, 2014), and five species that are currently regarded as C 3 (Blake, 1972;Macfarlane, 2007).…”

“…The reconstructed phylogeny indicates that C 4 and C 2 photosynthesis in Neurachne spp. occurred independently and relatively recently in evolutionary terms (Christin et al, 2012). Comparisons between Neurachne spp.…”