Evolutionary rewiring of the wheat transcriptional regulatory network by lineage-specific transposable elements

    • 1National 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, Shanghai 200032, China;
    • 2University of the Chinese Academy of Sciences, Beijing, 100049, China;
    • 3The 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, Beijing 100101, China;
    • 4State Key Laboratory for Crop Genetics and Germplasm Enhancement, Collaborative Innovation Center for Modern Crop Production co-sponsored by Province and Ministry (CIC-MCP), Nanjing Agricultural University, Nanjing, Jiangsu 210095, China;
    • 5Shanghai Center for Plant Stress Biology, National Key Laboratory of Plant Molecular Genetics, Center of Excellence in Molecular Plant Sciences, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China;
    • 6Henan University, School of Life Science, Kaifeng, Henan 457000, China;
    • 7Beijing Institute of Genomics, Chinese Academy of Sciences, and National Centre for Bioinformation, Beijing 100101 China;
    • 8Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou 225009, China;
    • 9State 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
    • 10 These authors contributed equally to this work.
Published September 9, 2021. Vol 31 Issue 12, pp. 2276-2289. https://doi.org/10.1101/gr.275658.121
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Abstract

More than 80% of the wheat genome consists of transposable elements (TEs), which act as major drivers of wheat genome evolution. However, their contributions to the regulatory evolution of wheat adaptations remain largely unclear. Here, we created genome-binding maps for 53 transcription factors (TFs) underlying environmental responses by leveraging DAP-seq in Triticum urartu, together with epigenomic profiles. Most TF binding sites (TFBSs) located distally from genes are embedded in TEs, whose functional relevance is supported by purifying selection and active epigenomic features. About 24% of the non-TE TFBSs share significantly high sequence similarity with TE-embedded TFBSs. These non-TE TFBSs have almost no homologous sequences in non-Triticeae species and are potentially derived from Triticeae-specific TEs. The expansion of TE-derived TFBS linked to wheat-specific gene responses, suggesting TEs are an important driving force for regulatory innovations. Altogether, TEs have been significantly and continuously shaping regulatory networks related to wheat genome evolution and adaptation.

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