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

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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

(2020) Dataset of traced lineages for embryos between 4- to 100-cell stage for Jankele et al.
Dryad Digital Repository, doi:10.5061/dryad.ghx3ffbmx.

https://doi.org/10.5061/dryad.ghx3ffbmx

Article and author information

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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.
Rob Jelier

Centre of Microbial and Plant Genetics, Katholieke Universiteit Leuven, Leuven, Belgium

Competing interests
The authors declare that no competing interests exist.
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.

"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.

Copyright

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.