Innovations and stepwise evolution of CBFs/DREB1s and their regulatory networks in angiosperms

ABSTRACT The C‐repeat binding factors/dehydration‐responsive element binding protein 1s (CBFs/DREB1s) have been identified as major regulators of cold acclimation in many angiosperm plants. However, their origin and evolutionary process associated to cold responsiveness are still lacking. By integrating multi‐omics data of genomes, transcriptomes, and CBFs/DREB1s genome‐wide binding profiles, we unveil the origin and evolution of CBFs/DREB1s and their regulatory network. Gene collinearity and phylogeny analyses show that CBF/DREB1 is an innovation evolved from tandem duplication‐derived DREB III gene. A subsequent event of ε‐whole genome duplication led to two CBF/DREB1 archetypes (Clades I and II) in ancient angiosperms. In contrast to cold‐insensitivity of Clade I and their parent DREB III genes, Clade II evolved a further innovation in cold‐sensitive response and was stepwise expanded in eudicots and monocots by independent duplications. In geological time, the duplication events were mainly enriched around the Cretaceous–Paleogene (K–Pg) boundary and/or in the Late Cenozoic Ice Age, when the global average temperature significantly decreased. Consequently, the duplicated CBF/DREB1 genes contributed to the rewiring of CBFs/DREB1s‐regulatory network for cold tolerance. Altogether, our results highlight an origin and convergent evolution of CBFs/DREB1s and their regulatory network probably for angiosperms adaptation to global cooling.