Transposable element-initiated enhancer-like elements generate the subgenome-biased spike specificity of polyploid wheat

Yilin Xie; Songbei Ying; Zijuan Li; Yu'e Zhang; Jiafu Zhu; Jinyu Zhang; Meiyue Wang; Huishan Diao; Haoyu Wang; Yuyun Zhang; Luhuan Ye; Yili Zhuang; Fei Zhao; Wan Teng; Wenli Zhang; Yiping Tong; Jungnam Cho; Zhicheng Dong; Yongbiao Xue; Yijing Zhang

doi:10.1038/s41467-023-42771-9

Transposable element-initiated enhancer-like elements generate the subgenome-biased spike specificity of polyploid wheat

Nat Commun. 2023 Nov 17;14(1):7465. doi: 10.1038/s41467-023-42771-9.

Authors

Yilin Xie^#^{1

2

3}, Songbei Ying^#¹, Zijuan Li^#^{2

3}, Yu'e Zhang^#^{3

4}, Jiafu Zhu^#⁵, Jinyu Zhang^{1

2

3}, Meiyue Wang¹, Huishan Diao¹, Haoyu Wang^{2

6}, Yuyun Zhang^{1

2

3}, Luhuan Ye^{2

3}, Yili Zhuang^{2

3}, Fei Zhao^{2

3}, Wan Teng^{3

4}, Wenli Zhang⁷, Yiping Tong^{3

4}, Jungnam Cho⁸, Zhicheng Dong⁹, Yongbiao Xue^{10

11

12

13}, Yijing Zhang¹⁴

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, Shanghai, 200438, 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, Shanghai, 200032, China.
³ University of the Chinese Academy of Sciences, Beijing, 100049, China.
⁴ State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, and The Innovation Academy of Seed Design, Chinese Academy of Sciences, Beijing, 100101, 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, Guangzhou, 510006, China.
⁶ Henan University, School of Life Science, Kaifeng, Henan, 457000, China.
⁷ State Key Laboratory for Crop Genetics and Germplasm Enhancement, CIC-MCP, Nanjing Agricultural University, No.1 Weigang, Nanjing, Jiangsu, 210095, China.
⁸ Department of Biosciences, Durham University, Durham, DH1 3LE, United Kingdom. jungnam.cho@durham.ac.uk.
⁹ 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, Guangzhou, 510006, China. zc_dong@gzhu.edu.cn.
¹⁰ University of the Chinese Academy of Sciences, Beijing, 100049, China. ybxue@genetics.ac.cn.
¹¹ State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, and The Innovation Academy of Seed Design, Chinese Academy of Sciences, Beijing, 100101, China. ybxue@genetics.ac.cn.
¹² Beijing Institute of Genomics, Chinese Academy of Sciences, and China National Centre for Bioinformation, Beijing, 100101, China. ybxue@genetics.ac.cn.
¹³ Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou, 225009, China. ybxue@genetics.ac.cn.
¹⁴ 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, Shanghai, 200438, China. zhangyijing@fudan.edu.cn.

^# Contributed equally.

Abstract

Transposable elements (TEs) comprise ~85% of the common wheat genome, which are highly diverse among subgenomes, possibly contribute to polyploid plasticity, but the causality is only assumed. Here, by integrating data from gene expression cap analysis and epigenome profiling via hidden Markov model in common wheat, we detect a large proportion of enhancer-like elements (ELEs) derived from TEs producing nascent noncoding transcripts, namely ELE-RNAs, which are well indicative of the regulatory activity of ELEs. Quantifying ELE-RNA transcriptome across typical developmental stages reveals that TE-initiated ELE-RNAs are mainly from RLG_famc7.3 specifically expanded in subgenome A. Acquisition of spike-specific transcription factor binding likely confers spike-specific expression of RLG_famc7.3-initiated ELE-RNAs. Knockdown of RLG_famc7.3-initiated ELE-RNAs resulted in global downregulation of spike-specific genes and abnormal spike development. These findings link TE expansion to regulatory specificity and polyploid developmental plasticity, highlighting the functional impact of TE-driven regulatory innovation on polyploid evolution.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

DNA Transposable Elements* / genetics
Gene Expression Regulation
Polyploidy
RNA
Transcriptome
Triticum* / genetics

Substances

DNA Transposable Elements
RNA