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

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 Zhuang, Wan Teng, Bo Zhang, Lin Huang, Yiping Tong, Wenli Zhang, Genying Li, Moussa Benhamed (), Zhicheng Dong (), Jin-Ying Gou () and Yijing Zhang ()
Additional contact information
Zijuan Li: Fudan University
Yuyun Zhang: Fudan University
Ci-Hang Ding: Fudan University
Yan Chen: Guangzhou University
Haoyu Wang: Fudan University
Jinyu Zhang: Fudan University
Songbei Ying: Fudan University
Meiyue Wang: Fudan University
Rongzhi Zhang: Shandong Academy of Agricultural Sciences
Jinyi Liu: Fudan University
Yilin Xie: Fudan University
Tengfei Tang: Fudan University
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
Bo Zhang: Chinese Academy of Sciences
Lin Huang: Sichuan Agricultural University
Yiping Tong: University of the Chinese Academy of Sciences
Wenli Zhang: Nanjing Agricultural University
Genying Li: Shandong Academy of Agricultural Sciences
Moussa Benhamed: Université Paris Cité, Institute of Plant Sciences Paris-Saclay (IPS2)
Zhicheng Dong: Guangzhou University
Jin-Ying Gou: China Agricultural University
Yijing Zhang: Fudan University

Nature Communications, 2023, vol. 14, issue 1, 1-15

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-43178-2

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