Competition between histone and transcription factor binding regulates the onset of transcription in zebrafish embryos

  1. Shai R Joseph
  2. Máté Pálfy
  3. Lennart Hilbert
  4. Mukesh Kumar
  5. Jens Karschau
  6. Vasily Zaburdaev
  7. Andrej Shevchenko
  8. Nadine L Vastenhouw  Is a corresponding author
  1. Max Planck Institute of Molecular Cell Biology and Genetics, Germany
  2. Max Planck Institute for the Physics of Complex Systems, Germany
  3. Center for Systems Biology Dresden, Germany

Abstract

Upon fertilization, the genome of animal embryos remains transcriptionally inactive until the maternal-to-zygotic transition. At this time, the embryo takes control of its development and transcription begins. How the onset of zygotic transcription is regulated remains unclear. Here, we show that a dynamic competition for DNA binding between nucleosome-forming histones and transcription factors regulates zebrafish genome activation. Taking a quantitative approach, we found that the concentration of non-DNA bound core histones sets the time for the onset of transcription. The reduction in nuclear histone concentration that coincides with genome activation does not affect nucleosome density on DNA, but allows transcription factors to compete successfully for DNA binding. In agreement with this, transcription factor binding is sensitive to histone levels and the concentration of transcription factors also affects the time of transcription. Our results demonstrate that the relative levels of histones and transcription factors regulate the onset of transcription in the embryo.

Article and author information

Author details

  1. Shai R Joseph

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Máté Pálfy

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Lennart Hilbert

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4478-5607
  4. Mukesh Kumar

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Jens Karschau

    Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Vasily Zaburdaev

    Center for Systems Biology Dresden, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Andrej Shevchenko

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Nadine L Vastenhouw

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    For correspondence
    vastenhouw@mpi-cbg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8782-9775

Funding

Human Frontier Science Program (CDA00060/2012)

  • Nadine L Vastenhouw

Deutsche Forschungsgemeinschaft

  • Shai R Joseph
  • Mukesh Kumar

Max-Planck-Gesellschaft

  • Vasily Zaburdaev
  • Andrej Shevchenko
  • Nadine L Vastenhouw

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

Reviewing Editor

  1. Karen Adelman, Harvard University, United States

Publication history

  1. Received: November 23, 2016
  2. Accepted: April 19, 2017
  3. Accepted Manuscript published: April 20, 2017 (version 1)
  4. Version of Record published: May 31, 2017 (version 2)

Copyright

© 2017, Joseph 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. Shai R Joseph
  2. Máté Pálfy
  3. Lennart Hilbert
  4. Mukesh Kumar
  5. Jens Karschau
  6. Vasily Zaburdaev
  7. Andrej Shevchenko
  8. Nadine L Vastenhouw
(2017)
Competition between histone and transcription factor binding regulates the onset of transcription in zebrafish embryos
eLife 6:e23326.
https://doi.org/10.7554/eLife.23326
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