Optogenetic investigation of BMP target gene expression diversity

  1. Katherine W Rogers
  2. Mohammad ElGamacy
  3. Benjamin M Jordan
  4. Patrick Müller  Is a corresponding author
  1. Friedrich Miescher Laboratory of the Max Planck Society, Germany
  2. Harvard University, United States

Abstract

Signaling molecules activate distinct patterns of gene expression to coordinate embryogenesis, but how spatiotemporal expression diversity is generated is an open question. In zebrafish, a BMP signaling gradient patterns the dorsal-ventral axis. We systematically identified target genes responding to BMP and found that they have diverse spatiotemporal expression patterns. Transcriptional responses to optogenetically delivered high- and low-amplitude BMP signaling pulses indicate that spatiotemporal expression is not fully defined by different BMP signaling activation thresholds. Additionally, we observed negligible correlations between spatiotemporal expression and transcription kinetics for the majority of analyzed genes in response to BMP signaling pulses. In contrast, spatial differences between BMP target genes largely collapsed when FGF and Nodal signaling were inhibited. Our results suggest that, similar to other patterning systems, combinatorial signaling is likely to be a major driver of spatial diversity in BMP-dependent gene expression in zebrafish.

Data availability

The RNA-sequencing data has been deposited at the GEO repository (accession number: GSE135100) and can be accessed at ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE135100. Image quantification data is available in the accompanying source data files.

The following data sets were generated

Article and author information

Author details

  1. Katherine W Rogers

    Systems Biology of Development Group, Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5700-2662
  2. Mohammad ElGamacy

    Systems Biology of Development Group, Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Benjamin M Jordan

    Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Patrick Müller

    Systems Biology of Development Group, Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, Germany
    For correspondence
    pmueller@tuebingen.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0702-6209

Funding

Max Planck Society

  • Patrick Müller

HFSP (CDA-00031/2013-C)

  • Patrick Müller

European Research Council (637840 (QUANTPATTERN))

  • Patrick Müller

European Research Council (863952 (ACE-OF-SPACE))

  • Patrick Müller

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

Reviewing Editor

  1. Markus Affolter, Biozentrum der Universität Basel, Switzerland

Version history

  1. Received: May 6, 2020
  2. Accepted: November 10, 2020
  3. Accepted Manuscript published: November 11, 2020 (version 1)
  4. Version of Record published: December 10, 2020 (version 2)

Copyright

© 2020, Rogers 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. Katherine W Rogers
  2. Mohammad ElGamacy
  3. Benjamin M Jordan
  4. Patrick Müller
(2020)
Optogenetic investigation of BMP target gene expression diversity
eLife 9:e58641.
https://doi.org/10.7554/eLife.58641

Share this article

https://doi.org/10.7554/eLife.58641

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