Jizeng Jia1,2, Yilin Xie3,4, Jingfei Cheng3,4, Chuizheng Kong5, Meiyue Wang3,4, Lifeng Gao5, Fei Zhao3,4, Jingyu Guo3,6, Kai Wang7, Guangwei Li8, Dangqun Cui8, Tiezhu Hu9, Guangyao Zhao10, Daowen Wang11, Zhengang Ru12, Yijing Zhang13,14. 1. College of Agronomy, State Key Laboratory of Wheat and Maize Crop Science, Henan Agricultural University, 63 Nongye Road, Zhengzhou, 450002, Henan, China. jiajizeng@caas.cn. 2. Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, 100081, China. jiajizeng@caas.cn. 3. 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, Shanghai, 200032, China. 4. University of the Chinese Academy of Sciences, Beijing, 100049, China. 5. Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, 100081, China. 6. Henan University, School of Life Science, Kaifeng, 457000, Henan, China. 7. Novogene Co. Ltd, Building 301, Jiuxianqiao North Road, Chaoyang District, Beijing, China. 8. College of Agronomy, State Key Laboratory of Wheat and Maize Crop Science, Henan Agricultural University, 63 Nongye Road, Zhengzhou, 450002, Henan, China. 9. Henan Institute of Science and Technology, Eastern Hualan Avenue, Xinxiang City, 453003, Henan Province, China. 10. Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, 100081, China. zhaoguangyao@caas.cn. 11. College of Agronomy, State Key Laboratory of Wheat and Maize Crop Science, Henan Agricultural University, 63 Nongye Road, Zhengzhou, 450002, Henan, China. dwwang@henau.edu.cn. 12. Henan Institute of Science and Technology, Eastern Hualan Avenue, Xinxiang City, 453003, Henan Province, China. rzgh58@163.com. 13. 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, Shanghai, 200032, China. zhangyijing@cemps.ac.cn. 14. University of the Chinese Academy of Sciences, Beijing, 100049, China. zhangyijing@cemps.ac.cn.
Abstract
BACKGROUND: Polyploidization and introgression are major events driving plant genome evolution and influencing crop breeding. However, the mechanisms underlying the higher-order chromatin organization of subgenomes and alien chromosomes are largely unknown. RESULTS: We probe the three-dimensional chromatin architecture of Aikang 58 (AK58), a widely cultivated allohexaploid wheat variety in China carrying the 1RS/1BL translocation chromosome. The regions involved in inter-chromosomal interactions, both within and between subgenomes, have highly similar sequences. Subgenome-specific territories tend to be connected by subgenome-dominant homologous transposable elements (TEs). The alien 1RS chromosomal arm, which was introgressed from rye and differs from its wheat counterpart, has relatively few inter-chromosome interactions with wheat chromosomes. An analysis of local chromatin structures reveals topologically associating domain (TAD)-like regions covering 52% of the AK58 genome, the boundaries of which are enriched with active genes, zinc-finger factor-binding motifs, CHH methylation, and 24-nt small RNAs. The chromatin loops are mostly localized around TAD boundaries, and the number of gene loops is positively associated with gene activity. CONCLUSIONS: The present study reveals the impact of the genetic sequence context on the higher-order chromatin structure and subgenome stability in hexaploid wheat. Specifically, we characterized the sequence homology-mediated inter-chromosome interactions and the non-canonical role of subgenome-biased TEs. Our findings may have profound implications for future investigations of the interplay between genetic sequences and higher-order structures and their consequences on polyploid genome evolution and introgression-based breeding of crop plants.
BACKGROUND: Polyploidization and introgression are major events driving plant genome evolution and influencing crop breeding. However, the mechanisms underlying the higher-order chromatin organization of subgenomes and alien chromosomes are largely unknown. RESULTS: We probe the three-dimensional chromatin architecture of Aikang 58 (AK58), a widely cultivated allohexaploid wheat variety in China carrying the 1RS/1BL translocation chromosome. The regions involved in inter-chromosomal interactions, both within and between subgenomes, have highly similar sequences. Subgenome-specific territories tend to be connected by subgenome-dominant homologous transposable elements (TEs). The alien 1RS chromosomal arm, which was introgressed from rye and differs from its wheat counterpart, has relatively few inter-chromosome interactions with wheat chromosomes. An analysis of local chromatin structures reveals topologically associating domain (TAD)-like regions covering 52% of the AK58 genome, the boundaries of which are enriched with active genes, zinc-finger factor-binding motifs, CHH methylation, and 24-nt small RNAs. The chromatin loops are mostly localized around TAD boundaries, and the number of gene loops is positively associated with gene activity. CONCLUSIONS: The present study reveals the impact of the genetic sequence context on the higher-order chromatin structure and subgenome stability in hexaploid wheat. Specifically, we characterized the sequence homology-mediated inter-chromosome interactions and the non-canonical role of subgenome-biased TEs. Our findings may have profound implications for future investigations of the interplay between genetic sequences and higher-order structures and their consequences on polyploid genome evolution and introgression-based breeding of crop plants.
Authors: Mayank Nk Choudhary; Ryan Z Friedman; Julia T Wang; Hyo Sik Jang; Xiaoyu Zhuo; Ting Wang Journal: Genome Biol Date: 2020-01-24 Impact factor: 13.583