Physically asymmetric division of the C. elegans zygote ensures invariably successful embryogenesis

  1. Radek Jankele
  2. Rob Jelier
  3. Pierre Gönczy  Is a corresponding author
  1. Swiss Federal Institute of Technology, Switzerland
  2. Katholieke Universiteit Leuven, Belgium

Abstract

Asymmetric divisions that yield daughter cells of different sizes are frequent during early embryogenesis, but the importance of such a physical difference for successful development remains poorly understood. Here, we investigated this question using the first division of C. elegans embryos, which yields a large AB cell and a small P1 cell. We equalized AB and P1 sizes using acute genetic inactivation or optogenetic manipulation of the spindle positioning protein LIN-5. We uncovered that only some embryos tolerated equalization, and that there was a size asymmetry threshold for viability. Cell lineage analysis of equalized embryos revealed an array of defects, including faster cell cycle progression in P1 descendants, as well as defects in cell positioning, division orientation and cell fate. Moreover, equalized embryos were more susceptible to external compression. Overall, we conclude that unequal first cleavage is essential for invariably successful embryonic development of C. elegans.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.Source data files and code have been provided as individual files for: Figure 1 - supplement 1-3, Figures 2, Figure 2 - supplement 1, Figure 5, Figure 5 - supplement 1, and Figure 6 - supplement 1.Further, the lineaging data, as well as the source code used for their analysis, are available from GitHub: https://github.com/UPGON/worm-rules-eLifeThese include code and source data for Figures 3, 4, and 6, and accompanying supplements, as well as for Figure 6 - supplement 2 and 3). Results of the statistical tests are reported in Supplementary File 6

The following data sets were generated

Article and author information

Author details

  1. Radek Jankele

    Swiss Institute for Experimental Cancer Research, School of Life Sciences, Swiss Federal Institute of Technology, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  2. Rob Jelier

    Centre of Microbial and Plant Genetics, Katholieke Universiteit Leuven, Leuven, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  3. Pierre Gönczy

    Swiss Institute of Experimental Cancer Research, Swiss Federal Institute of Technology, Lausanne, Switzerland
    For correspondence
    pierre.gonczy@epfl.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6305-6883

Funding

Swiss National Science Foundation (31003A_155942)

  • Radek Jankele
  • Pierre Gönczy

Research Foundation Flanders (G055017N)

  • Rob Jelier

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

Reviewing Editor

  1. Michael B Eisen, University of California, Berkeley, United States

Version history

  1. Received: August 3, 2020
  2. Accepted: February 22, 2021
  3. Accepted Manuscript published: February 23, 2021 (version 1)
  4. Accepted Manuscript updated: February 25, 2021 (version 2)
  5. Version of Record published: March 18, 2021 (version 3)

Copyright

© 2021, Jankele 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. Radek Jankele
  2. Rob Jelier
  3. Pierre Gönczy
(2021)
Physically asymmetric division of the C. elegans zygote ensures invariably successful embryogenesis
eLife 10:e61714.
https://doi.org/10.7554/eLife.61714

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