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Widespread contribution of transposable elements to the rewiring of mammalian 3D genomes

Author

Listed:
  • Mayank N. K. Choudhary

    (Washington University in St. Louis
    Washington University in St. Louis)

  • Kara Quaid

    (Washington University in St. Louis
    Washington University in St. Louis)

  • Xiaoyun Xing

    (Washington University in St. Louis
    Washington University in St. Louis)

  • Heather Schmidt

    (Washington University in St. Louis
    Washington University in St. Louis)

  • Ting Wang

    (Washington University in St. Louis
    Washington University in St. Louis)

Abstract

Transposable elements (TEs) are major contributors of genetic material in mammalian genomes. These often include binding sites for architectural proteins, including the multifarious master protein, CTCF, which shapes the 3D genome by creating loops, domains, compartment borders, and RNA-DNA interactions. These play a role in the compact packaging of DNA and have the potential to facilitate regulatory function. In this study, we explore the widespread contribution of TEs to mammalian 3D genomes by quantifying the extent to which they give rise to loops and domain border differences across various cell types and species using several 3D genome mapping technologies. We show that specific families and subfamilies of TEs have contributed to lineage-specific 3D chromatin structures across mammalian species. In many cases, these loops may facilitate sustained interaction between distant cis-regulatory elements and target genes, and domains may segregate chromatin state to impact gene expression in a lineage-specific manner. An experimental validation of our analytical findings using CRISPR-Cas9 to delete a candidate TE resulted in disruption of species-specific 3D chromatin structure. Taken together, we comprehensively quantify and selectively validate our finding that TEs contribute to shaping 3D genome organization and may, in some cases, impact gene regulation during the course of mammalian evolution.

Suggested Citation

  • Mayank N. K. Choudhary & Kara Quaid & Xiaoyun Xing & Heather Schmidt & Ting Wang, 2023. "Widespread contribution of transposable elements to the rewiring of mammalian 3D genomes," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36364-9
    DOI: 10.1038/s41467-023-36364-9
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    References listed on IDEAS

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    Cited by:

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    2. Botong Zhou & Ping Hu & Guichun Liu & Zhou Chang & Zhiwei Dong & Zihe Li & Yuan Yin & Zunzhe Tian & Ge Han & Wen Wang & Xueyan Li, 2024. "Evolutionary patterns and functional effects of 3D chromatin structures in butterflies with extensive genome rearrangements," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. Alan Y. Du & Jason D. Chobirko & Xiaoyu Zhuo & Cédric Feschotte & Ting Wang, 2024. "Regulatory transposable elements in the encyclopedia of DNA elements," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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