The landscape of RNA Pol II binding reveals a stepwise transition during ZGA

Bofeng Liu, Qianhua Xu, Qiujun Wang, Su Feng, Fangnong Lai, Peizhe Wang, Fangyuan Zheng, Yunlong Xiang, Jingyi Wu, Junwei Nie, Cui Qiu, Weikun Xia, Lijia Li, Guang Yu, Zili Lin, Kai Xu, Zhuqing Xiong, Feng Kong, Ling Liu, Chunyi Huang, Yang Yu, Jie Na and Wei Xie ()
Additional contact information
Bofeng Liu: Tsinghua University
Qianhua Xu: Tsinghua University
Qiujun Wang: Tsinghua University
Su Feng: Vazyme Biotech Co., Ltd
Fangnong Lai: Tsinghua University
Peizhe Wang: Tsinghua University
Fangyuan Zheng: Vazyme Biotech Co., Ltd
Yunlong Xiang: Tsinghua University
Jingyi Wu: Tsinghua University
Junwei Nie: Vazyme Biotech Co., Ltd
Cui Qiu: Vazyme Biotech Co., Ltd
Weikun Xia: Tsinghua University
Lijia Li: Tsinghua University
Guang Yu: Tsinghua University
Zili Lin: Tsinghua University
Kai Xu: Tsinghua University
Zhuqing Xiong: Tsinghua University
Feng Kong: Tsinghua University
Ling Liu: Tsinghua University
Chunyi Huang: Tsinghua University
Yang Yu: Chinese Academy of Sciences
Jie Na: Tsinghua University
Wei Xie: Tsinghua University

Nature, 2020, vol. 587, issue 7832, 139-144

Abstract: Abstract Zygotic genome activation (ZGA) is the first transcription event in life1. However, it is unclear how RNA polymerase is engaged in initiating ZGA in mammals. Here, by developing small-scale Tn5-assisted chromatin cleavage with sequencing (Stacc–seq), we investigated the landscapes of RNA polymerase II (Pol II) binding in mouse embryos. We found that Pol II undergoes ‘loading’, ‘pre-configuration’, and ‘production’ during the transition from minor ZGA to major ZGA. After fertilization, Pol II is preferentially loaded to CG-rich promoters and accessible distal regions in one-cell embryos (loading), in part shaped by the inherited parental epigenome. Pol II then initiates relocation to future gene targets before genome activation (pre-configuration), where it later engages in full transcription elongation upon major ZGA (production). Pol II also maintains low poising at inactive promoters after major ZGA until the blastocyst stage, coinciding with the loss of promoter epigenetic silencing factors. Notably, inhibition of minor ZGA impairs the Pol II pre-configuration and embryonic development, accompanied by aberrant retention of Pol II and ectopic expression of one-cell targets upon major ZGA. Hence, stepwise transition of Pol II occurs when mammalian life begins, and minor ZGA has a key role in the pre-configuration of transcription machinery and chromatin for genome activation.

Date: 2020
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DOI: 10.1038/s41586-020-2847-y

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