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LHP1-mediated epigenetic buffering of subgenome diversity and defense responses confers genome plasticity and adaptability in allopolyploid wheat

Author

Listed:
  • Zijuan Li

    (Fudan University
    Chinese Academy of Sciences
    University of the Chinese Academy of Sciences)

  • Yuyun Zhang

    (Fudan University
    Chinese Academy of Sciences
    University of the Chinese Academy of Sciences)

  • Ci-Hang Ding

    (Fudan University
    China Agricultural University)

  • Yan Chen

    (Guangzhou University)

  • Haoyu Wang

    (Fudan University
    Chinese Academy of Sciences
    Henan University, School of Life Science)

  • Jinyu Zhang

    (Fudan University
    Chinese Academy of Sciences
    University of the Chinese Academy of Sciences)

  • Songbei Ying

    (Fudan University)

  • Meiyue Wang

    (Fudan University)

  • Rongzhi Zhang

    (Shandong Academy of Agricultural Sciences
    Key Laboratory of Wheat Biology and Genetic Improvement on North Yellow and Huai River Valley
    National Engineering Research Center for Wheat and Maize)

  • Jinyi Liu

    (Fudan University
    Chinese Academy of Sciences
    University of the Chinese Academy of Sciences)

  • Yilin Xie

    (Fudan University
    Chinese Academy of Sciences
    University of the Chinese Academy of Sciences)

  • Tengfei Tang

    (Fudan University
    Chinese Academy of Sciences
    Henan University, School of Life Science)

  • Huishan Diao

    (Fudan University)

  • Luhuan Ye

    (Chinese Academy of Sciences)

  • Yili Zhuang

    (Chinese Academy of Sciences)

  • Wan Teng

    (University of the Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Bo Zhang

    (Chinese Academy of Sciences)

  • Lin Huang

    (Sichuan Agricultural University)

  • Yiping Tong

    (University of the Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Wenli Zhang

    (Nanjing Agricultural University)

  • Genying Li

    (Shandong Academy of Agricultural Sciences
    Key Laboratory of Wheat Biology and Genetic Improvement on North Yellow and Huai River Valley
    National Engineering Research Center for Wheat and Maize)

  • Moussa Benhamed

    (Université Paris Cité, Institute of Plant Sciences Paris-Saclay (IPS2)
    Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2))

  • Zhicheng Dong

    (Guangzhou University)

  • Jin-Ying Gou

    (China Agricultural University)

  • Yijing Zhang

    (Fudan University)

Abstract

Polyploidization is a major driver of genome diversification and environmental adaptation. However, the merger of different genomes may result in genomic conflicts, raising a major question regarding how genetic diversity is interpreted and regulated to enable environmental plasticity. By analyzing the genome-wide binding of 191 trans-factors in allopolyploid wheat, we identified like heterochromatin protein 1 (LHP1) as a master regulator of subgenome-diversified genes. Transcriptomic and epigenomic analyses of LHP1 mutants reveal its role in buffering the expression of subgenome-diversified defense genes by controlling H3K27me3 homeostasis. Stripe rust infection releases latent subgenomic variations by eliminating H3K27me3-related repression. The simultaneous inactivation of LHP1 homoeologs by CRISPR–Cas9 confers robust stripe rust resistance in wheat seedlings. The conditional repression of subgenome-diversified defenses ensures developmental plasticity to external changes, while also promoting neutral-to-non-neutral selection transitions and adaptive evolution. These findings establish an LHP1-mediated buffering system at the intersection of genotypes, environments, and phenotypes in polyploid wheat. Manipulating the epigenetic buffering capacity offers a tool to harness cryptic subgenomic variations for crop improvement.

Suggested Citation

  • Zijuan Li & Yuyun Zhang & Ci-Hang Ding & Yan Chen & Haoyu Wang & Jinyu Zhang & Songbei Ying & Meiyue Wang & Rongzhi Zhang & Jinyi Liu & Yilin Xie & Tengfei Tang & Huishan Diao & Luhuan Ye & Yili Zhuan, 2023. "LHP1-mediated epigenetic buffering of subgenome diversity and defense responses confers genome plasticity and adaptability in allopolyploid wheat," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43178-2
    DOI: 10.1038/s41467-023-43178-2
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