Morphogenetic degeneracies in the actomyosin cortex

  1. Sundar Ram Naganathan  Is a corresponding author
  2. Sebastian Fürthauer
  3. Josana Rodriguez
  4. Bruno Thomas Fievet
  5. Frank Jülicher
  6. Julie Ahringer
  7. Carlo Vittorio Cannistraci
  8. Stephan W Grill  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. Newcastle University, United Kingdom
  4. University of Cambridge, United Kingdom
  5. Technische Universität Dresden, Germany

Abstract

One of the great challenges in biology is to understand the mechanisms by which morphogenetic processes arise from molecular activities. We investigated this problem in the context of actomyosin-based cortical flow in C. elegans zygotes, where large-scale flows emerge from the collective action of actomyosin filaments and actin binding proteins (ABPs). Large-scale flow dynamics can be captured by active gel theory by considering force balances and conservation laws in the actomyosin cortex. However, which molecular activities contribute to flow dynamics and large-scale physical properties such as viscosity and active torque is largely unknown. By performing a candidate RNAi screen of ABPs and actomyosin regulators we demonstrate that perturbing distinct molecular processes can lead to similar flow phenotypes. This is indicative for a 'morphogenetic degeneracy' where multiple molecular processes contribute to the same large-scale physical property. We speculate that morphogenetic degeneracies contribute to the robustness of bulk biological matter in development.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Sundar Ram Naganathan

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    For correspondence
    sundar.naganathan@epfl.ch
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5106-8687
  2. Sebastian Fürthauer

    Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
    Competing interests
    No competing interests declared.
  3. Josana Rodriguez

    Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle, United Kingdom
    Competing interests
    No competing interests declared.
  4. Bruno Thomas Fievet

    The Gurdon Institute, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    No competing interests declared.
  5. Frank Jülicher

    Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
    Competing interests
    Frank Jülicher, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4731-9185
  6. Julie Ahringer

    The Gurdon Institute, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    Julie Ahringer, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7074-4051
  7. Carlo Vittorio Cannistraci

    Biotechnology Center (BIOTEC), Technische Universität Dresden, Dresden, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0100-8410
  8. Stephan W Grill

    Biotechnology Center (BIOTEC), Technische Universität Dresden, Dresden, Germany
    For correspondence
    stephan.grill@tu-dresden.de
    Competing interests
    No competing interests declared.

Funding

Deutsche Forschungsgemeinschaft (SPP 1782)

  • Stephan W Grill

ITN (641639)

  • Stephan W Grill

Human Frontier Science Program (LT000078/2016)

  • Sundar Ram Naganathan

Human Frontier Science Program (LT000871/2014)

  • Sebastian Fürthauer

European Research Council (281903)

  • Stephan W Grill

ITN (281903)

  • Stephan W Grill

Human Frontier Science Program (RGP0023/2014)

  • Stephan W Grill

Max-Planck-Gesellschaft (Open-access funding)

  • Sundar Ram Naganathan

Deutsche Forschungsgemeinschaft (GSC 97)

  • Stephan W Grill

Deutsche Forschungsgemeinschaft (GR 3271/2)

  • Stephan W Grill

Deutsche Forschungsgemeinschaft (GR 3271/3)

  • Stephan W Grill

Deutsche Forschungsgemeinschaft (GR 3271/4)

  • Stephan W Grill

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

Reviewing Editor

  1. Naama Barkai, Weizmann Institute of Science, Israel

Publication history

  1. Received: April 18, 2018
  2. Accepted: October 16, 2018
  3. Accepted Manuscript published: October 22, 2018 (version 1)
  4. Version of Record published: November 9, 2018 (version 2)
  5. Version of Record updated: November 13, 2018 (version 3)

Copyright

© 2018, Naganathan 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. Sundar Ram Naganathan
  2. Sebastian Fürthauer
  3. Josana Rodriguez
  4. Bruno Thomas Fievet
  5. Frank Jülicher
  6. Julie Ahringer
  7. Carlo Vittorio Cannistraci
  8. Stephan W Grill
(2018)
Morphogenetic degeneracies in the actomyosin cortex
eLife 7:e37677.
https://doi.org/10.7554/eLife.37677

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