Rapid diversification of St-genome-sharing species in wheat grasses (Triticeae: Poaceae) accompanied by diversifying selection of chloroplast genes

Background: The St-genome-sharing taxa are highly complex group of the species with the St nuclear genome and monophyletic origin in maternal lineages within the Triticeae, which contains more than half of polyploid species that distributed in a wide range of ecological habitats. While high level of genetic heterogeneity in plastome DNA due to a reticulate evolutionary event has been considered to link with the richness of the St-genome-sharing taxa, the relationship between the dynamics of diversification and molecular evolution is lack of understanding.

Results: Here, integrating 106 previously and 12 newly sequenced plastomes representing almost all previously recognized genomic types and genus of the Triticeae, this study applies phylogenetic reconstruction methods in combination with lineage diversification analyses, estimate of sequence evolution, and gene expression to investigate the dynamics of diversification in the tribe. Phylogenomic analysis confirmed previous phylogenetic relationships, with the St/E/V lineages (Pseudoroegneria/Lophopyrum + Thinopyrum/Dasypyrum) being suffered from a chloroplast capture event prior to polyploidization events. Analyses of diversification rates detected a significant acceleration approximately five million years ago in the St-genome-sharing taxa. Molecular tests of evolution and gene expression further indicated that radiation within the accelerated group has been accompanied by adaptive genetic changes in a few chloroplast-encoded genes directly or indirectly related to photosynthesis.

Conclusions: Our results support an important role for adaptive evolution in plastomes during accelerated diversification. In combination with plastome data, further investigations using other genomes, such as the nuclear genome, are urgently needed to enhance our understanding of the evolutionary history of the St-genome-sharing taxa, especially to determine whether adaptive changes in the nuclear genome are accelerated as well because plastome represents the maternal inheritation in angiosperms.