1. Developmental Biology
  2. Genetics and Genomics
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Odd-paired is a pioneer-like factor that coordinates with Zelda to control gene expression in embryos

  1. Theodora Koromila
  2. Fan Gao
  3. Yasuno Iwasaki
  4. Peng He
  5. Lior Pachter
  6. J Peter Gergen
  7. Angelike Stathopoulos  Is a corresponding author
  1. California Institute of Technology, United States
  2. SUNY, United States
Research Article
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Cite this article as: eLife 2020;9:e59610 doi: 10.7554/eLife.59610

Abstract

Pioneer factors such as Zelda (Zld) help initiate zygotic transcription in Drosophila early embryos, but whether other factors support this dynamic process is unclear. Odd-paired (Opa), a zinc-finger transcription factor expressed at cellularization, controls the transition of genes from pair-rule to segmental patterns along the anterior-posterior axis. Finding that Opa also regulates expression through enhancer sog_Distal along the dorso-ventral axis, we hypothesized Opa’s role is more general. Chromatin-immunoprecipitation (ChIP-seq) confirmed its in vivo binding to sog_Distal but also identified widespread binding throughout the genome, comparable to Zld. Furthermore, chromatin assays (ATAC-seq) demonstrate that Opa, like Zld, influences chromatin accessibility genome-wide at cellularization, suggesting both are pioneer factors with common as well as distinct targets. Lastly, embryos lacking opa exhibit widespread, late patterning defects spanning both axes. Collectively, these data suggest Opa is a general timing factor and likely late-acting pioneer factor that drives a secondary wave of zygotic gene expression.

Data availability

GEO accession number SuperSeries GSE153329. SubSeries: ChIP-seq and singled-end ATAC-seq (GSE140722), and RNA-seq and paired-end ATAC-seq data access (GSE153328).RNA-seq and paired-end ATAC-seq data access: https://www.ncbi.nlm.nih.gov/geo/info/submissionftp.html, folder name: GEO_Theodora and Directory name: uploads/tkoromila_YTqdmKKoThe codes for RNA-seq, Opa ChIP-seq and ATAC-seq processing (alignment and peak calling) were uploaded to github: https://github.com/caltech-bioinformatics-resource-center/Stathopoulos_Lab

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

Article and author information

Author details

  1. Theodora Koromila

    Division of Biology, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5504-1369
  2. Fan Gao

    Division of Biology, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Yasuno Iwasaki

    Department of Biochemistry and Cell Biology, SUNY, Stonybrook, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Peng He

    Division of Biology, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2457-3554
  5. Lior Pachter

    Division of Biology and Biological Engineering and Department of Computing and Mathematical Sciences, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. J Peter Gergen

    Department of Biochemistry and Cell Biology, SUNY, Stony Brook, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Angelike Stathopoulos

    Division of Biology, California Institute of Technology, Pasadena, United States
    For correspondence
    angelike@caltech.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6597-2036

Funding

National Institute of General Medical Sciences (R35GM118146)

  • Angelike Stathopoulos

Eunice Kennedy Shriver National Institute of Child Health and Human Development (R03HD097535)

  • Angelike Stathopoulos

Bioinformatics Resource Center at the Beckman Institute of Caltech (n/a)

  • Fan Gao

Stony Brook University College of Arts and Sciences (n/a)

  • J Peter Gergen

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

Reviewing Editor

  1. Oliver Hobert, Howard Hughes Medical Institute, Columbia University, United States

Publication history

  1. Received: November 26, 2019
  2. Accepted: July 22, 2020
  3. Accepted Manuscript published: July 23, 2020 (version 1)
  4. Accepted Manuscript updated: July 24, 2020 (version 2)
  5. Version of Record published: August 10, 2020 (version 3)

Copyright

© 2020, Koromila 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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