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

Zheng Zhao, Liang Li, Ruichen Zeng, Liangguan Lin, Dongwei Yuan, Yejie Wen, Na Li, Yingying Cui, Shiming Zhu, Zhi-Min Zhang, Sheng Li () and Chonghua Ren ()
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Zheng Zhao: 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
Yingying Cui: South China Normal University
Shiming Zhu: South China Normal University
Zhi-Min Zhang: Jinan University
Sheng Li: South China Normal University
Chonghua Ren: South China Normal University

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

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-43987-5

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