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Evolutionary epigenomic analyses in mammalian early embryos reveal species-specific innovations and conserved principles of imprinting.

ABSTRACT: While mouse remains the most popular model, the conservation of parental-to-embryonic epigenetic transition across mammals is poorly defined. Through analysis of oocytes and early embryos in human, bovine, porcine, rat, and mouse, we revealed remarkable species-specific innovations as no single animal model fully recapitulates the human epigenetic transition. In rodent oocytes, transcription-dependent DNA methylation allows methylation of maternal imprints but not intergenic paternal imprints. Unexpectedly, prevalent DNA hypermethylation, paralleled by H3K36me2/3, also occurs in nontranscribed regions in porcine and bovine oocytes, except for megabase-long “CpG continents (CGCs)” where imprinting control regions preferentially reside. Broad H3K4me3 and H3K27me3 domains exist in nonhuman oocytes, yet only rodent H3K27me3 survives beyond genome activation. Coincidently, regulatory elements preferentially evade H3K27me3 in rodent oocytes, and failure to do so causes aberrant embryonic gene repression. Hence, the diverse mammalian innovations of parental-to-embryonic transition center on a delicate “to-methylate-or-not” balance in establishing imprints while protecting other regulatory regions.

SUBMITTER: Lu X

PROVIDER: S-EPMC8612685 | biostudies-literature | 2021 Nov

REPOSITORIES: biostudies-literature

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Evolutionary epigenomic analyses in mammalian early embryos reveal species-specific innovations and conserved principles of imprinting.

Lu Xukun X Zhang Yu Y Wang Lijuan L Wang Leyun L Wang Huili H Xu Qianhua Q Xiang Yunlong Y Chen Chaolei C Kong Feng F Xia Weikun W Lin Zili Z Ma Sinan S Liu Ling L Wang Xiangguo X Ni Hemin H Li Wei W Guo Yong Y Xie Wei W

Science advances 20211124 48

While mouse remains the most popular model, the conservation of parental-to-embryonic epigenetic transition across mammals is poorly defined. Through analysis of oocytes and early embryos in human, bovine, porcine, rat, and mouse, we revealed remarkable species-specific innovations as no single animal model fully recapitulates the human epigenetic transition. In rodent oocytes, transcription-dependent DNA methylation allows methylation of maternal imprints but not intergenic paternal imprints. U ...[more]

PMID: 34818044

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Project description:Brugia malayi is a human filarial nematode responsible for elephantiasis, a debilitating condition that is part of a broader spectrum of diseases called filariasis, including lymphatic filariasis and river blindness. Almost all filarial nematode species infecting humans live in mutualism with Wolbachia endosymbionts, present in somatic hypodermal tissues but also in the female germline which ensures their vertical transmission to the nematode progeny. These α-proteobacteria potentially provision their host with essential metabolites and protect the parasite against the vertebrate immune response. In the absence of Wolbachia wBm, B. malayi females become sterile, and the filarial nematode lifespan is greatly reduced. In order to better comprehend this symbiosis, we investigated the adaptation of wBm to the host nematode soma and germline, and we characterized these cellular environments to highlight their specificities. Dual RNAseq experiments were performed at the tissue-specific and ovarian developmental stage levels, reaching the resolution of the germline mitotic proliferation and meiotic differentiation stages. We found that most wBm genes, including putative effectors, are not differentially regulated between infected tissues. However, two wBm genes involved in stress responses are upregulated in the hypodermal chords compared to the germline, indicating that this somatic tissue represents a harsh environment to which wBm have adapted. A comparison of the B. malayi and C. elegans germline transcriptomes reveals a poor conservation of genes involved in the production of oocytes, with the filarial germline proliferative zone relying on a majority of genes absent from C. elegans. The first orthology map of the B. malayi genome presented here, together with tissue-specific expression enrichment analyses, indicate that the early steps of oogenesis are a developmental process involving genes specific to filarial nematodes, that likely result from evolutionary innovations supporting the filarial parasitic lifestyle.

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Evolutionary epigenomic analyses in mammalian early embryos reveal species-specific innovations and conserved principles of imprinting.

Publications

Evolutionary epigenomic analyses in mammalian early embryos reveal species-specific innovations and conserved principles of imprinting.

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