TY - JOUR

T1 - Whole-genome transcriptome and DNA methylation dynamics of pre-implantation embryos reveal progression of embryonic genome activation in buffaloes

AU - Fu, Penghui

AU - Zhang, Du

AU - Yang, Chunyan

AU - Yuan, Xiang

AU - Luo, Xier

AU - Zheng, Haiying

AU - Deng, Yanfei

AU - Liu, Qingyou

AU - Cui, Kuiqing

AU - Gao, Fei

AU - Shi, Deshun

N1 - Publisher Copyright: © 2023, The Author(s).

PY - 2023

Y1 - 2023

N2 - Background: During mammalian pre-implantation embryonic development (PED), the process of maternal-to-zygote transition (MZT) is well orchestrated by epigenetic modification and gene sequential expression, and it is related to the embryonic genome activation (EGA). During MZT, the embryos are sensitive to the environment and easy to arrest at this stage in vitro. However, the timing and regulation mechanism of EGA in buffaloes remain obscure. Results: Buffalo pre-implantation embryos were subjected to trace cell based RNA-seq and whole-genome bisulfite sequencing (WGBS) to draw landscapes of transcription and DNA-methylation. Four typical developmental steps were classified during buffalo PED. Buffalo major EGA was identified at the 16-cell stage by the comprehensive analysis of gene expression and DNA methylation dynamics. By weighted gene co-expression network analysis, stage-specific modules were identified during buffalo maternal-to-zygotic transition, and key signaling pathways and biological process events were further revealed. Programmed and continuous activation of these pathways was necessary for success of buffalo EGA. In addition, the hub gene, CDK1, was identified to play a critical role in buffalo EGA. Conclusions: Our study provides a landscape of transcription and DNA methylation in buffalo PED and reveals deeply the molecular mechanism of the buffalo EGA and genetic programming during buffalo MZT. It will lay a foundation for improving the in vitro development of buffalo embryos. Graphical Abstract: [Figure not available: see fulltext.]

AB - Background: During mammalian pre-implantation embryonic development (PED), the process of maternal-to-zygote transition (MZT) is well orchestrated by epigenetic modification and gene sequential expression, and it is related to the embryonic genome activation (EGA). During MZT, the embryos are sensitive to the environment and easy to arrest at this stage in vitro. However, the timing and regulation mechanism of EGA in buffaloes remain obscure. Results: Buffalo pre-implantation embryos were subjected to trace cell based RNA-seq and whole-genome bisulfite sequencing (WGBS) to draw landscapes of transcription and DNA-methylation. Four typical developmental steps were classified during buffalo PED. Buffalo major EGA was identified at the 16-cell stage by the comprehensive analysis of gene expression and DNA methylation dynamics. By weighted gene co-expression network analysis, stage-specific modules were identified during buffalo maternal-to-zygotic transition, and key signaling pathways and biological process events were further revealed. Programmed and continuous activation of these pathways was necessary for success of buffalo EGA. In addition, the hub gene, CDK1, was identified to play a critical role in buffalo EGA. Conclusions: Our study provides a landscape of transcription and DNA methylation in buffalo PED and reveals deeply the molecular mechanism of the buffalo EGA and genetic programming during buffalo MZT. It will lay a foundation for improving the in vitro development of buffalo embryos. Graphical Abstract: [Figure not available: see fulltext.]

KW - Buffalo

KW - DNA methylome

KW - Embryonic genome activation

KW - Maternal-to-zygote transition

KW - Transcriptome

U2 - 10.1186/s40104-023-00894-5

DO - 10.1186/s40104-023-00894-5

M3 - Journal article

C2 - 37430306

AN - SCOPUS:85164463468

VL - 14

JO - Journal of Animal Science and Biotechnology

JF - Journal of Animal Science and Biotechnology

SN - 1674-9782

M1 - 94

ER -