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5mC modification orchestrates choriogenesis and fertilization by preventing prolonged ftz-f1 expression

Author

Listed:
  • Zheng Zhao

    (South China Normal University
    Guangdong Laboratory for Lingnan Modern Agriculture
    South China Normal University)

  • Liang Li

    (South China Normal University)

  • Ruichen Zeng

    (South China Normal University)

  • Liangguan Lin

    (South China Normal University)

  • Dongwei Yuan

    (South China Normal University)

  • Yejie Wen

    (South China Normal University)

  • Na Li

    (South China Normal University
    South China Normal University)

  • Yingying Cui

    (South China Normal University)

  • Shiming Zhu

    (South China Normal University)

  • Zhi-Min Zhang

    (Jinan University)

  • Sheng Li

    (South China Normal University
    Guangdong Laboratory for Lingnan Modern Agriculture
    South China Normal University)

  • Chonghua Ren

    (South China Normal University
    South China Normal University)

Abstract

DNA methylation at the fifth position of cytosine (5-methylcytosine, 5mC) is a crucial epigenetic modification for regulating gene expression, but little is known about how it regulates gene expression in insects. Here, we pursue the detailed molecular mechanism by which DNMT1-mediated 5mC maintenance regulates female reproduction in the German cockroach, Blattella germanica. Our results show that Dnmt1 knockdown decreases the level of 5mC in the ovary, upregulating numerous genes during choriogenesis, especially the transcription factor ftz-f1. The hypomethylation at the ftz-f1 promoter region increases and prolongs ftz-f1 expression in ovarian follicle cells during choriogenesis, which consequently causes aberrantly high levels of 20-hydroxyecdysone and excessively upregulates the extracellular matrix remodeling gene Mmp1. These changes further impair choriogenesis and disrupt fertilization by causing anoikis of the follicle cells, a shortage of chorion proteins, and malformation of the sponge-like bodies. This study significantly advances our understanding of how DNA 5mC modification regulates female reproduction in insects.

Suggested Citation

  • Zheng Zhao & Liang Li & Ruichen Zeng & Liangguan Lin & Dongwei Yuan & Yejie Wen & Na Li & Yingying Cui & Shiming Zhu & Zhi-Min Zhang & Sheng Li & Chonghua Ren, 2023. "5mC modification orchestrates choriogenesis and fertilization by preventing prolonged ftz-f1 expression," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43987-5
    DOI: 10.1038/s41467-023-43987-5
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    References listed on IDEAS

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    1. Zhi-Min Zhang & Rui Lu & Pengcheng Wang & Yang Yu & Dongliang Chen & Linfeng Gao & Shuo Liu & Debin Ji & Scott B Rothbart & Yinsheng Wang & Gang Greg Wang & Jikui Song, 2018. "Structural basis for DNMT3A-mediated de novo DNA methylation," Nature, Nature, vol. 554(7692), pages 387-391, February.
    2. Sheng Li & Shiming Zhu & Qiangqiang Jia & Dongwei Yuan & Chonghua Ren & Kang Li & Suning Liu & Yingying Cui & Haigang Zhao & Yanghui Cao & Gangqi Fang & Daqi Li & Xiaoming Zhao & Jianzhen Zhang & Qiao, 2018. "The genomic and functional landscapes of developmental plasticity in the American cockroach," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
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