J Integr Plant Biol ›› 2022, Vol. 64 ›› Issue (11): 2111-2125.DOI: 10.1111/jipb.13357

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  • 收稿日期:2022-05-11 接受日期:2022-08-29 出版日期:2022-11-01 发布日期:2022-11-17

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

Yuqi Nie1†, Liangyu Guo1†, Fuqiang Cui1†, Yirong Shen1, Xiaoxue Ye2, Deyin Deng1, Shuo Wang1*, Jianhua Zhu3,4* and Wenwu Wu1*   

  1. 1 State Key Laboratory of Subtropical Silviculture, School of Forestry and Biotechnology, Zhejiang A & F University, Hangzhou 311300, China
    2 Institute of Tropical Biosciences and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, China
    3 School of Life Sciences, Anhui Agricultural University, Hefei 230036, China
    4 Department of Plant Science and Landscape Architecture, University of Maryland, College Park, Maryland 20742, USA

    † These authors contributed equally to the work.
    * Correspondences: Shuo Wang (wangshuo@zafu.edu.cn); Jianhua Zhu (jhzhu@umd.edu); Wenwu Wu (wwwu@zafu.edu.cn, Dr. Wu is fully responsible for the distribution of the materials associated with this article)
  • Received:2022-05-11 Accepted:2022-08-29 Online:2022-11-01 Published:2022-11-17

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.

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