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

• Published in: Nature communications Vol. 14; no. 1; pp. 8234 - 14
• Main Authors: Zhao, Zheng, Li, Liang, Zeng, Ruichen, Lin, Liangguan, Yuan, Dongwei, Wen, Yejie, Li, Na, Cui, Yingying, Zhu, Shiming, Zhang, Zhi-Min, Li, Sheng, Ren, Chonghua
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 12.12.2023; Nature Publishing Group; Nature Portfolio
• Subjects: 38/1; 38/89; 38/91; 631/136; 631/337/176/1988; 631/601/1737; Animals; Anoikis; Blattella germanica; Chorion; Cockroaches; Cytosine; Deoxyribonucleic acid; DNA; DNA methylation; DNA-Binding Proteins - metabolism; DNMT1 protein; Epigenetics; Extracellular matrix; Female; Females; Fertilization; Fertilization - genetics; Gene expression; Gene Expression Regulation; Humanities and Social Sciences; Insecta - metabolism; Insects; Molecular modelling; multidisciplinary; Reproduction; Science; Science (multidisciplinary); Transcription Factors - metabolism
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-023-43987-5

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. The mechanism by which DNA methylation regulates female reproduction in insects is largely unknown. Here Zhao et al . demonstrate that the 5mC modification orchestrates timely choriogenesis and proper fertilization by preventing prolonged ftz-f1 expression in the German cockroach.