LAUSR

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 (TD)-derived DREB III gene. A subsequent event of ε-whole genome duplication (ε-WGD) led to two CBF/DREB1 archetypes (Clade 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 (GAT) 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. This article is protected by copyright. All rights reserved.