HIRA and dPCIF1 coordinately establish totipotent chromatin and control orderly ZGA in Drosophila embryos

• 成果类型: Article
• 署名作者: Zhang, Guoqiang; Miao, Yaqi; Song, Yuan; Wang, Liangliang; Li, Yawei; Zhu, Yuanxiang; Zhang, Wenxin; Sun, Qinmiao; Chen, Dahua
• 署名单位: Yunnan University; Chinese Academy of Sciences; Institute of Zoology, CAS; Chinese Academy of Sciences; University of Chinese Academy of Sciences, CAS; Chinese Academy of Sciences
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-13889
• DOI: 10.1073/pnas.2410261121
• 发表日期: 2024-11-19
• 关键词: h3.3 chaperone hira; zygotic genome; dna-binding; complex; domain; zelda; accessibility; requirement; variants; protein

摘要

Early embryos undergo profound changes in their genomic architecture to establish the totipotent state, enabling pioneer factors to access chromatin and drive zygotic genome activation (ZGA). However, the mechanisms by which the totipotent state is established and properly interpreted by pioneer factors to allow orderly ZGA remain unknown. Here, we identify the H3.3- specific chaperone HIRA as a factor involving establishing totipotent-state chromatin in Drosophila early embryos. Through cophase separation with HIRA, the pioneer factor GAGA factor (GAF) efficiently binds to H3.3- marked nucleosomes to activate major- wave zygotic genes. Importantly, dPCIF1, a chromatin- associated protein, antagonized the GAF-HIRA interaction by competitively binding to HIRA, thereby restricting GAF on earlier chromatin and avoiding premature ZGA. Hence, the coordinated action of HIRA and dPCIF1 ensures sequential ZGA from the minor to major wave in early embryos. This study provides insights into understanding how a totipotent state is established and properly controlled during ZGA.