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Satb2 acts as a gatekeeper for major developmental transitions during early vertebrate embryogenesis

Author

Listed:
  • Saurabh J. Pradhan

    (Indian Institute of Science Education and Research)

  • Puli Chandramouli Reddy

    (Indian Institute of Science Education and Research)

  • Michael Smutny

    (Institute of Science and Technology Austria
    Warwick Medical School, University of Warwick)

  • Ankita Sharma

    (Indian Institute of Science Education and Research)

  • Keisuke Sako

    (Institute of Science and Technology Austria)

  • Meghana S. Oak

    (Indian Institute of Science Education and Research)

  • Rini Shah

    (Indian Institute of Science Education and Research)

  • Mrinmoy Pal

    (Indian Institute of Science Education and Research)

  • Ojas Deshpande

    (Indian Institute of Science Education and Research
    Tata Institute of Fundamental Research)

  • Greg Dsilva

    (Indian Institute of Science Education and Research)

  • Yin Tang

    (Yale University School of Medicine)

  • Rakesh Mishra

    (Centre for Cellular and Molecular Biology)

  • Girish Deshpande

    (Princeton University)

  • Antonio J. Giraldez

    (Yale University School of Medicine)

  • Mahendra Sonawane

    (Tata Institute of Fundamental Research)

  • Carl-Philipp Heisenberg

    (Institute of Science and Technology Austria)

  • Sanjeev Galande

    (Indian Institute of Science Education and Research
    Shiv Nadar University, Gautam Buddha Nagar)

Abstract

Zygotic genome activation (ZGA) initiates regionalized transcription underlying distinct cellular identities. ZGA is dependent upon dynamic chromatin architecture sculpted by conserved DNA-binding proteins. However, the direct mechanistic link between the onset of ZGA and the tissue-specific transcription remains unclear. Here, we have addressed the involvement of chromatin organizer Satb2 in orchestrating both processes during zebrafish embryogenesis. Integrative analysis of transcriptome, genome-wide occupancy and chromatin accessibility reveals contrasting molecular activities of maternally deposited and zygotically synthesized Satb2. Maternal Satb2 prevents premature transcription of zygotic genes by influencing the interplay between the pluripotency factors. By contrast, zygotic Satb2 activates transcription of the same group of genes during neural crest development and organogenesis. Thus, our comparative analysis of maternal versus zygotic function of Satb2 underscores how these antithetical activities are temporally coordinated and functionally implemented highlighting the evolutionary implications of the biphasic and bimodal regulation of landmark developmental transitions by a single determinant.

Suggested Citation

  • Saurabh J. Pradhan & Puli Chandramouli Reddy & Michael Smutny & Ankita Sharma & Keisuke Sako & Meghana S. Oak & Rini Shah & Mrinmoy Pal & Ojas Deshpande & Greg Dsilva & Yin Tang & Rakesh Mishra & Giri, 2021. "Satb2 acts as a gatekeeper for major developmental transitions during early vertebrate embryogenesis," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26234-7
    DOI: 10.1038/s41467-021-26234-7
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    References listed on IDEAS

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    1. Jingyi Wu & Jiawei Xu & Bofeng Liu & Guidong Yao & Peizhe Wang & Zili Lin & Bo Huang & Xuepeng Wang & Tong Li & Senlin Shi & Nan Zhang & Fuyu Duan & Jia Ming & Xiangyang Zhang & Wenbin Niu & Wenyan So, 2018. "Publisher Correction: Chromatin analysis in human early development reveals epigenetic transition during ZGA," Nature, Nature, vol. 560(7718), pages 27-27, August.
    2. Cheol-Hee Kim & Takaya Oda & Motoyuki Itoh & Di Jiang & Kristin Bruk Artinger & Settara C. Chandrasekharappa & Wolfgang Driever & Ajay B. Chitnis, 2000. "Repressor activity of Headless/Tcf3 is essential for vertebrate head formation," Nature, Nature, vol. 407(6806), pages 913-916, October.
    3. Jingyi Wu & Jiawei Xu & Bofeng Liu & Guidong Yao & Peizhe Wang & Zili Lin & Bo Huang & Xuepeng Wang & Tong Li & Senlin Shi & Nan Zhang & Fuyu Duan & Jia Ming & Xiangyang Zhang & Wenbin Niu & Wenyan So, 2018. "Chromatin analysis in human early development reveals epigenetic transition during ZGA," Nature, Nature, vol. 557(7704), pages 256-260, May.
    4. Miler T. Lee & Ashley R. Bonneau & Carter M. Takacs & Ariel A. Bazzini & Kate R. DiVito & Elizabeth S. Fleming & Antonio J. Giraldez, 2013. "Nanog, Pou5f1 and SoxB1 activate zygotic gene expression during the maternal-to-zygotic transition," Nature, Nature, vol. 503(7476), pages 360-364, November.
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