Zebrafish embryonic explants undergo genetically encoded self-assembly

  1. Alexandra Schauer
  2. Diana Pinheiro
  3. Robert Hauschild
  4. Carl-Philipp Heisenberg  Is a corresponding author
  1. Institute of Science and Technology Austria, Austria

Abstract

Embryonic stem cell cultures are thought to self-organize into embryoid bodies, able to undergo symmetry-breaking, germ layer specification and even morphogenesis. Yet, it is unclear how to reconcile this remarkable self-organization capacity with classical experiments demonstrating key roles for extrinsic biases by maternal factors and/or extraembryonic tissues in embryogenesis. Here, we show that zebrafish embryonic tissue explants, prepared prior to germ layer induction and lacking extraembryonic tissues, can specify all germ layers and form a seemingly complete mesendoderm anlage. Importantly, explant organization requires polarized inheritance of maternal factors from dorsal-marginal regions of the blastoderm. Moreover, induction of endoderm and head-mesoderm, which require peak Nodal-signaling levels, is highly variable in explants, reminiscent of embryos with reduced Nodal signals from the extraembryonic tissues. Together, these data suggest that zebrafish explants do not undergo bona-fide self-organization, but rather display features of genetically encoded self-assembly, where intrinsic genetic programs control the emergence of order.

Data availability

All data generated and analyzed in the manuscript are provided as Source Data Files. The Custom Script used has been uploaded as Source code 1.

Article and author information

Author details

  1. Alexandra Schauer

    Life Sciences, Institute of Science and Technology Austria, Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
  2. Diana Pinheiro

    Life Sciences, Institute of Science and Technology Austria, Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
  3. Robert Hauschild

    Life Sciences, Institute of Science and Technology Austria, Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9843-3522
  4. Carl-Philipp Heisenberg

    Life Sciences, Institute of Science and Technology Austria, Klosterneuburg, Austria
    For correspondence
    heisenberg@ist.ac.at
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0912-4566

Funding

H2020 European Research Council (MECSPEC742573)

  • Carl-Philipp Heisenberg

Austrian Academy of Sciences

  • Alexandra Schauer

European Molecular Biology Organization (850-2017)

  • Diana Pinheiro

Human Frontier Science Program (LT000429/2018-L2)

  • Diana Pinheiro

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

Ethics

Animal experimentation: All animal experiments in this study were performed in strict accordance with the guidelines of the Ethics and Animal Welfare Committee (ETK) in Austria. The respective approval number that covers the performed experiments is 66.018/0010-WF/II/3b/2014.

Reviewing Editor

  1. Ashley Bruce

Publication history

  1. Received: January 15, 2020
  2. Accepted: April 5, 2020
  3. Accepted Manuscript published: April 6, 2020 (version 1)
  4. Version of Record published: April 29, 2020 (version 2)

Copyright

© 2020, Schauer 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. Alexandra Schauer
  2. Diana Pinheiro
  3. Robert Hauschild
  4. Carl-Philipp Heisenberg
(2020)
Zebrafish embryonic explants undergo genetically encoded self-assembly
eLife 9:e55190.
https://doi.org/10.7554/eLife.55190

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