Abstract
Adaptation to temperate environments is common in the grass subfamily Pooideae, suggesting an ancestral origin of cold climate adaptation. Here, we investigated substitution rates of genes involved in low-temperature-induced (LTI) stress responses to test the hypothesis that adaptive molecular evolution of LTI pathway genes was important for Pooideae evolution.Substitution rates and signatures of positive selection were analyzed using 4330 gene trees including three warm climate-adapted species (maize (Zea mays), sorghum (Sorghum bicolor), and rice (Oryza sativa)) and five temperate Pooideae species (Brachypodium distachyon, wheat (Triticum aestivum), barley (Hordeum vulgare), Lolium perenne and Festuca pratensis).Nonsynonymous substitution rate differences between Pooideae and warm habitat-adapted species were elevated in LTI trees compared with all trees. Furthermore, signatures of positive selection were significantly stronger in LTI trees after the rice and Pooideae split but before the Brachypodium divergence (P < 0.05). Genome-wide heterogeneity in substitution rates was also observed, reflecting divergent genome evolution processes within these grasses.Our results provide evidence for a link between adaptation to cold habitats and adaptive evolution of LTI stress responses in early Pooideae evolution and shed light on a poorly understood chapter in the evolutionary history of some of the world's most important temperate crops.
Highlights
The grass family (Poaceae) consists of c. 10 000 species, most of which belong to two major clades: BEP (Bambusoideae, Ehrhartoideae and Pooideae) (Soreng et al, 2000) and PACCMAD (Panicoideae, Arundinoideae, Centothecoideae, Chloridoideae, Micrairoideae, Aristidoideae and Danthonioideae) (Gabriel Sanchez-Ken et al, 2007)
No completely sequenced core Pooideae (CP) genome is available yet, and we selected species with large sequence resources distributed across two different CP clades: wheat (Triticum aestivum) and barley (Hordeum vulgare) belonging to the Hordeeae, and Lolium perenne and Festuca pratensis belonging to Poaeae
Wheat coding sequences (CDSs) were compiled from a combination of transcripts from the unigene collection at the National Center for Biotechnology Information (NCBI; http://www.ncbi.nlm.nih. gov/unigene), putative unique transcripts (PUTs) were downloaded from the plant genome database, and a collection of full-length wheat cDNAs were downloaded from the Hordeeae full-length CDS DataBase
Summary
The grass family (Poaceae) consists of c. 10 000 species, most of which belong to two major clades: BEP (Bambusoideae, Ehrhartoideae and Pooideae) (Soreng et al, 2000) and PACCMAD (Panicoideae, Arundinoideae, Centothecoideae, Chloridoideae, Micrairoideae, Aristidoideae and Danthonioideae) (Gabriel Sanchez-Ken et al, 2007). One of the most species-rich grass subfamilies, have successfully adapted to and diversified in cool climate ecosystems (Hartley, 1973; Edwards & Smith, 2010). It is unknown if cold and freezing tolerance evolved before, coincidentally with or during Pooideae evolution. All four remaining tribes belong to a species-rich clade in which the basal chromosome number is seven, referred to as the core Pooideae (CP) (Fig. 1) (Soreng et al, 2000; Hilu, 2004). The CP encompass Hordeeae, Bromeae, and Poeae, in which all agriculturally important Pooideae crops belong
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