CLAMP and Zelda function together to promote Drosophila zygotic genome activation

  1. Jingyue Duan  Is a corresponding author
  2. Leila Rieder
  3. Megan M Colonnetta
  4. Annie Huang
  5. Mary Mckenney
  6. Scott Watters
  7. Girish Deshpande,
  8. William Jordan
  9. Nicolas Fawzi
  10. Erica Larschan  Is a corresponding author
  1. Brown University, United States
  2. Emory University, United States
  3. Princeton University, United States

Abstract

During the essential and conserved process of zygotic genome activation (ZGA), chromatin accessibility must increase to promote transcription. Drosophila is a well-established model for defining mechanisms that drive ZGA. Zelda (ZLD) is a key pioneer transcription factor (TF) that promotes ZGA in the Drosophila embryo. However, many genomic loci that contain GA-rich motifs become accessible during ZGA independent of ZLD. Therefore, we hypothesized that other early TFs that function with ZLD have not yet been identified, especially those that are capable of binding to GA-rich motifs such as CLAMP. Here, we demonstrate that Drosophila embryonic development requires maternal CLAMP to: 1) activate zygotic transcription; 2) increase chromatin accessibility at promoters of specific genes that often encode other essential TFs; 3) enhance chromatin accessibility and facilitate ZLD occupancy at a subset of key embryonic promoters. Thus, CLAMP functions as a pioneer factor which plays a targeted yet essential role in ZGA.

Data availability

To review GEO accession GSE152613:Go to https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE152613Enter token ihevsmiqnxexrod into the box

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Jingyue Duan

    Department of Molecular Biology, Cellular Biology and Biochemistry, Brown University, Providence, United States
    For correspondence
    jd774@cornell.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6416-2250
  2. Leila Rieder

    Emory University, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Megan M Colonnetta

    Department of Molecular Biology, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5685-1670
  4. Annie Huang

    Department of Molecular Biology, Cellular Biology and Biochemistry, Brown University, Providence, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Mary Mckenney

    Department of Molecular Biology, Cellular Biology and Biochemistry, Brown University, Providence, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Scott Watters

    Department of Molecular Pharmacology, Physiology, and Biotechnology, Brown University, Providence, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Girish Deshpande,

    MCB, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. William Jordan

    Department of Molecular Biology, Cellular Biology and Biochemistry, Brown University, Providence, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Nicolas Fawzi

    Department of Molecular Pharmacology, Physiology, and Biotechnology, Brown University, Providence, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Erica Larschan

    Molecular Biology, Cellular Biology and Biochemistry, Brown University, Providence, United States
    For correspondence
    erica_larschan@brown.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2484-4921

Funding

National Institute of General Medical Sciences (F32GM109663)

  • Leila Rieder

National Institute of General Medical Sciences (K99HD092625)

  • Leila Rieder

National Institute of General Medical Sciences (R00HD092625)

  • Leila Rieder

National Institute of General Medical Sciences (R35GM126994)

  • Erica Larschan

National Science Foundation (1845734)

  • Nicolas Fawzi

National Institute of General Medical Sciences (R01GM118530)

  • Nicolas Fawzi

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Yukiko M Yamashita, Whitehead Institute/MIT, United States

Version history

  1. Preprint posted: July 15, 2020 (view preprint)
  2. Received: April 30, 2021
  3. Accepted: August 2, 2021
  4. Accepted Manuscript published: August 3, 2021 (version 1)
  5. Version of Record published: August 16, 2021 (version 2)

Copyright

© 2021, Duan et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Jingyue Duan
  2. Leila Rieder
  3. Megan M Colonnetta
  4. Annie Huang
  5. Mary Mckenney
  6. Scott Watters
  7. Girish Deshpande,
  8. William Jordan
  9. Nicolas Fawzi
  10. Erica Larschan
(2021)
CLAMP and Zelda function together to promote Drosophila zygotic genome activation
eLife 10:e69937.
https://doi.org/10.7554/eLife.69937

Share this article

https://doi.org/10.7554/eLife.69937

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