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 () and Yijing Zhang ()
Additional contact information
Yilin Xie: Fudan University
Songbei Ying: Fudan University
Zijuan Li: Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences
Yu’e Zhang: University of the Chinese Academy of Sciences
Jiafu Zhu: Guangzhou University
Jinyu Zhang: Fudan University
Meiyue Wang: Fudan University
Huishan Diao: Fudan University
Haoyu Wang: Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences
Yuyun Zhang: Fudan University
Luhuan Ye: Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences
Yili Zhuang: Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences
Fei Zhao: Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences
Wan Teng: University of the Chinese Academy of Sciences
Wenli Zhang: Nanjing Agricultural University
Yiping Tong: University of the Chinese Academy of Sciences
Jungnam Cho: Durham University
Zhicheng Dong: Guangzhou University
Yongbiao Xue: University of the Chinese Academy of Sciences
Yijing Zhang: Fudan University

Nature Communications, 2023, vol. 14, issue 1, 1-13

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-42771-9

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