Successive evolutionary steps drove Pooideae grasses from tropical to temperate regions.

Abstract

Angiosperm adaptations to seasonally cold climates have occurred multiple times independently. However, the observation that less than half of all angiosperm families are represented in temperate latitudes suggests internal constraints on the evolution of cold tolerance/avoidance strategies. Similar to angiosperms as a whole, grasses are primarily tropical, but one major clade, subfamily Pooideae, radiated extensively within temperate regions. It is posited that this Pooideae niche transition was facilitated by an early origin of long-term cold responsiveness around the base of the subfamily, and that a set of more ancient pathways enabled evolution of seasonal cold tolerance. To test this, we compared transcriptome-level responses of disparate Pooideae to short-/long-term cold and with those previously known in the subtropical grass rice (Ehrhartoideae). Analyses identified several highly conserved cold-responsive 'orthogroups' within our focal Pooideae species that originated successively during the diversification of land plants, predominantly via gene duplication. The majority of conserved Pooideae cold-responsive genes appear to have ancient roles in stress responses, with most of the orthogroups also being sensitive to cold in rice. However, a subgroup of genes was likely co-opted de novo early in the Pooideae. These results highlight a plausible stepwise evolutionary trajectory for cold adaptations across Pooideae.