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The landscape of accessible chromatin in mammalian preimplantation embryos

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  • Jingyi Wu

    (MOE Key Laboratory of Bioinformatics, Center for Stem Cell Biology and Regenerative Medicine, THU-PKU Center for Life Sciences, School of Life Sciences, Tsinghua University
    Joint Graduate Program of Peking-Tsinghua-NIBS, School of Life Sciences, Tsinghua University, Beijing)

  • Bo Huang

    (PKU-THU Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University)

  • He Chen

    (Joint Graduate Program of Peking-Tsinghua-NIBS, College of Life Sciences, Peking University)

  • Qiangzong Yin

    (MOE Key Laboratory of Bioinformatics, Center for Stem Cell Biology and Regenerative Medicine, THU-PKU Center for Life Sciences, School of Life Sciences, Tsinghua University)

  • Yang Liu

    (Joint Graduate Program of Peking-Tsinghua-NIBS, School of Life Sciences, Tsinghua University, Beijing
    MOE Key Laboratory of Bioinformatics, Center for Synthetic & Systems Biology, THU-PKU Center for Life Sciences, School of Life Sciences, Tsinghua University)

  • Yunlong Xiang

    (MOE Key Laboratory of Bioinformatics, Center for Stem Cell Biology and Regenerative Medicine, THU-PKU Center for Life Sciences, School of Life Sciences, Tsinghua University)

  • Bingjie Zhang

    (MOE Key Laboratory of Bioinformatics, Center for Stem Cell Biology and Regenerative Medicine, THU-PKU Center for Life Sciences, School of Life Sciences, Tsinghua University)

  • Bofeng Liu

    (MOE Key Laboratory of Bioinformatics, Center for Stem Cell Biology and Regenerative Medicine, THU-PKU Center for Life Sciences, School of Life Sciences, Tsinghua University)

  • Qiujun Wang

    (MOE Key Laboratory of Bioinformatics, Center for Stem Cell Biology and Regenerative Medicine, THU-PKU Center for Life Sciences, School of Life Sciences, Tsinghua University)

  • Weikun Xia

    (MOE Key Laboratory of Bioinformatics, Center for Stem Cell Biology and Regenerative Medicine, THU-PKU Center for Life Sciences, School of Life Sciences, Tsinghua University)

  • Wenzhi Li

    (Center for Stem Cell Biology and Regenerative Medicine, School of Medicine, Tsinghua University)

  • Yuanyuan Li

    (MOE Key Laboratory of Bioinformatics, Center for Stem Cell Biology and Regenerative Medicine, THU-PKU Center for Life Sciences, School of Life Sciences, Tsinghua University)

  • Jing Ma

    (MOE Key Laboratory of Bioinformatics, Center for Stem Cell Biology and Regenerative Medicine, THU-PKU Center for Life Sciences, School of Life Sciences, Tsinghua University)

  • Xu Peng

    (Singapore Institute for Clinical Sciences, Agency for Science, Technology and Research (A*STAR))

  • Hui Zheng

    (MOE Key Laboratory of Bioinformatics, Center for Stem Cell Biology and Regenerative Medicine, THU-PKU Center for Life Sciences, School of Life Sciences, Tsinghua University)

  • Jia Ming

    (Center for Stem Cell Biology and Regenerative Medicine, School of Medicine, Tsinghua University)

  • Wenhao Zhang

    (MOE Key Laboratory of Bioinformatics, Center for Stem Cell Biology and Regenerative Medicine, THU-PKU Center for Life Sciences, School of Life Sciences, Tsinghua University)

  • Jing Zhang

    (School of Life Sciences, Tsinghua University)

  • Geng Tian

    (School of Medicine, Tsinghua University)

  • Feng Xu

    (Singapore Institute for Clinical Sciences, Agency for Science, Technology and Research (A*STAR)
    Institute of Molecular and Cell Biology)

  • Zai Chang

    (School of Life Sciences, Tsinghua University)

  • Jie Na

    (Center for Stem Cell Biology and Regenerative Medicine, School of Medicine, Tsinghua University)

  • Xuerui Yang

    (Joint Graduate Program of Peking-Tsinghua-NIBS, School of Life Sciences, Tsinghua University, Beijing
    MOE Key Laboratory of Bioinformatics, Center for Synthetic & Systems Biology, THU-PKU Center for Life Sciences, School of Life Sciences, Tsinghua University)

  • Wei Xie

    (MOE Key Laboratory of Bioinformatics, Center for Stem Cell Biology and Regenerative Medicine, THU-PKU Center for Life Sciences, School of Life Sciences, Tsinghua University
    Joint Graduate Program of Peking-Tsinghua-NIBS, School of Life Sciences, Tsinghua University, Beijing)

Abstract

In mammals, extensive chromatin reorganization is essential for reprogramming terminally committed gametes to a totipotent state during preimplantation development. However, the global chromatin landscape and its dynamics in this period remain unexplored. Here we report a genome-wide map of accessible chromatin in mouse preimplantation embryos using an improved assay for transposase-accessible chromatin with high throughput sequencing (ATAC-seq) approach with CRISPR/Cas9-assisted mitochondrial DNA depletion. We show that despite extensive parental asymmetry in DNA methylomes, the chromatin accessibility between the parental genomes is globally comparable after major zygotic genome activation (ZGA). Accessible chromatin in early embryos is widely shaped by transposable elements and overlaps extensively with putative cis-regulatory sequences. Unexpectedly, accessible chromatin is also found near the transcription end sites of active genes. By integrating the maps of cis-regulatory elements and single-cell transcriptomes, we construct the regulatory network of early development, which helps to identify the key modulators for lineage specification. Finally, we find that the activities of cis-regulatory elements and their associated open chromatin diminished before major ZGA. Surprisingly, we observed many loci showing non-canonical, large open chromatin domains over the entire transcribed units in minor ZGA, supporting the presence of an unusually permissive chromatin state. Together, these data reveal a unique spatiotemporal chromatin configuration that accompanies early mammalian development.

Suggested Citation

  • Jingyi Wu & Bo Huang & He Chen & Qiangzong Yin & Yang Liu & Yunlong Xiang & Bingjie Zhang & Bofeng Liu & Qiujun Wang & Weikun Xia & Wenzhi Li & Yuanyuan Li & Jing Ma & Xu Peng & Hui Zheng & Jia Ming &, 2016. "The landscape of accessible chromatin in mammalian preimplantation embryos," Nature, Nature, vol. 534(7609), pages 652-657, June.
  • Handle: RePEc:nat:nature:v:534:y:2016:i:7609:d:10.1038_nature18606
    DOI: 10.1038/nature18606
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    Cited by:

    1. Le Tran Phuc Khoa & Wentao Yang & Mengrou Shan & Li Zhang & Fengbiao Mao & Bo Zhou & Qiang Li & Rebecca Malcore & Clair Harris & Lili Zhao & Rajesh C. Rao & Shigeki Iwase & Sundeep Kalantry & Stephani, 2024. "Quiescence enables unrestricted cell fate in naive embryonic stem cells," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. Xiaoqing Nie & Qianhua Xu & Chengpeng Xu & Fengling Chen & Qizhi Wang & Dandan Qin & Rui Wang & Zheng Gao & Xukun Lu & Xinai Yang & Yu Wu & Chen Gu & Wei Xie & Lei Li, 2023. "Maternal TDP-43 interacts with RNA Pol II and regulates zygotic genome activation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. Phoebe Lut Fei Tam & Ming Fung Cheung & Lu Yan Chan & Danny Leung, 2024. "Cell-type differential targeting of SETDB1 prevents aberrant CTCF binding, chromatin looping, and cis-regulatory interactions," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. Zhengyi Li & Haiyan Xu & Jiaqun Li & Xiao Xu & Junjiao Wang & Danya Wu & Jiateng Zhang & Juan Liu & Ziwei Xue & Guankai Zhan & Bobby Cheng Peow Tan & Di Chen & Yun-Shen Chan & Huck Hui Ng & Wanlu Liu , 2023. "Selective binding of retrotransposons by ZFP352 facilitates the timely dissolution of totipotency network," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Yan Bi & Zhifen Tu & Jianfeng Zhou & Xuehao Zhu & Hong Wang & Shaorong Gao & Yixuan Wang, 2022. "Cell fate roadmap of human primed-to-naive transition reveals preimplantation cell lineage signatures," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    6. Wen-Lan Yang & Weinan Qiu & Ting Zhang & Kai Xu & Zi-Juan Gu & Yu Zhou & Heng-Ji Xu & Zhong-Zhou Yang & Bin Shen & Yong-Liang Zhao & Qi Zhou & Ying Yang & Wei Li & Peng-Yuan Yang & Yun-Gui Yang, 2023. "Nsun2 coupling with RoRĪ³t shapes the fate of Th17 cells and promotes colitis," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    7. Hua Yu & Zhen Sun & Tianyu Tan & Hongru Pan & Jing Zhao & Ling Zhang & Jiayu Chen & Anhua Lei & Yuqing Zhu & Lang Chen & Yuyan Xu & Yaxin Liu & Ming Chen & Jinghao Sheng & Zhengping Xu & Pengxu Qian &, 2021. "rRNA biogenesis regulates mouse 2C-like state by 3D structure reorganization of peri-nucleolar heterochromatin," Nature Communications, Nature, vol. 12(1), pages 1-21, December.

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