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; Yijing Zhang

doi:10.1038/s41467-023-43178-2

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

Nat Commun. 2023 Nov 20;14(1):7538. doi: 10.1038/s41467-023-43178-2.

Authors

Zijuan Li^#^{1

2

3}, Yuyun Zhang^#^{1

2

3}, Ci-Hang Ding^#^{1

4}, Yan Chen^#⁵, Haoyu Wang^#^{1

2

6}, Jinyu Zhang^{1

2

3}, Songbei Ying¹, Meiyue Wang¹, Rongzhi Zhang^{7

8

9}, Jinyi Liu^{1

2

3}, Yilin Xie^{1

2

3}, Tengfei Tang^{1

2

6}, Huishan Diao¹, Luhuan Ye², Yili Zhuang², Wan Teng^{3

10}, Bo Zhang¹¹, Lin Huang¹², Yiping Tong^{3

10}, Wenli Zhang¹³, Genying Li^{7

8

9}, Moussa Benhamed^{14

15}, Zhicheng Dong¹⁶, Jin-Ying Gou¹⁷, Yijing Zhang¹⁸

Affiliations

¹ State Key Laboratory of Genetic Engineering, Collaborative Innovation Center of Genetics and Development, Department of Biochemistry, Institute of Plant Biology, School of Life Sciences, Fudan University, 200438, Shanghai, China.
² National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, 300 Fenglin Road, 200032, Shanghai, China.
³ University of the Chinese Academy of Sciences, 100049, Beijing, China.
⁴ Frontiers Science Center for Molecular Design Breeding, China Agricultural University, Beijing, China.
⁵ Guangdong Provincial Key Laboratory of Plant Adaptation and Molecular Design, Guangzhou Key Laboratory of Crop Gene Editing, Innovative Center of Molecular Genetics and Evolution, School of Life Sciences, Guangzhou University, 510006, Guangzhou, China.
⁶ Henan University, School of Life Science, 457000, Kaifeng, Henan, China.
⁷ Crop Research Institute, Shandong Academy of Agricultural Sciences, Jinan, China.
⁸ Ministry of Agriculture, Key Laboratory of Wheat Biology and Genetic Improvement on North Yellow and Huai River Valley, Jinan, China.
⁹ National Engineering Research Center for Wheat and Maize, Jinan, Shandong, China.
¹⁰ The State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, the Innovative Academy of Seed Design, Chinese Academy of Sciences, 100101, Beijing, China.
¹¹ Northwest Institute of Plateau Biology, Chinese Academy of Sciences, 810008, Xining, China.
¹² State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University, 611130, Wenjiang, Chengdu, China.
¹³ State Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, Jiangsu Collaborative Innovation Center for Modern Crop Production, Nanjing Agricultural University, No.1 Weigang, 210095, Nanjing, Jiangsu, China.
¹⁴ Université Paris Cité, Institute of Plant Sciences Paris-Saclay (IPS2), F-75006, Paris, France. moussa.benhamed@universite-paris-saclay.fr.
¹⁵ Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2), 91405, Orsay, France. moussa.benhamed@universite-paris-saclay.fr.
¹⁶ Guangdong Provincial Key Laboratory of Plant Adaptation and Molecular Design, Guangzhou Key Laboratory of Crop Gene Editing, Innovative Center of Molecular Genetics and Evolution, School of Life Sciences, Guangzhou University, 510006, Guangzhou, China. zc_dong@gzhu.edu.cn.
¹⁷ Frontiers Science Center for Molecular Design Breeding, China Agricultural University, Beijing, China. jygou@cau.edu.cn.
¹⁸ State Key Laboratory of Genetic Engineering, Collaborative Innovation Center of Genetics and Development, Department of Biochemistry, Institute of Plant Biology, School of Life Sciences, Fudan University, 200438, Shanghai, China. zhangyijing@fudan.edu.cn.

^# Contributed equally.

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.

MeSH terms

Epigenesis, Genetic
Epigenomics*
Genome, Plant / genetics
Histones / metabolism
Triticum* / genetics
Triticum* / metabolism

Substances

like heterochromatin protein 1
Histones