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Summary: Increasing studies suggest that the biased retention of stress‐related transcription factors (TFs) after whole‐genome duplications (WGDs) could rewire gene transcriptional networks, facilitating plant adaptation to challenging environments. However, the role of posttranscriptional factors (e.g. RNA‐binding proteins, RBPs) following WGDs has been largely ignored.Uncovering thousands of RBPs in 21 representative angiosperm species, we integrate genomic, transcriptomic, regulatomic, and paleotemperature datasets to unravel their evolutionary trajectories and roles in adapting to challenging environments.We reveal functional enrichments of RBP genes in stress responses and identify their convergent retention across diverse angiosperms from independent WGDs, coinciding with global cooling periods. Numerous RBP duplicates derived from WGDs are then identified as cold‐induced. A significant overlap of 29 orthogroups between WGD‐derived and cold‐induced RBP genes across diverse angiosperms highlights a correlation between WGD and cold stress. Notably, we unveil an orthogroup (Glycine‐rich RNA‐binding Proteins 7/8, GRP7/8) and relevant TF duplicates (CCA1/LHY, RVE4/8, CBF2/4, etc.), co‐retained in different angiosperms post‐WGDs. Finally, we illustrate their roles in rewiring circadian and cold‐regulatory networks at both transcriptional and posttranscriptional levels during global cooling.Altogether, we underline the adaptive evolution of RBPs in angiosperms after WGDs during global cooling, improving our understanding of plants surviving periods of environmental turmoil. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]