Physically asymmetric division of the C. elegans zygote ensures invariably successful embryogenesis
- Swiss Federal Institute of Technology Lausanne (EPFL), Switzerland
- 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
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Dataset of traced lineages for embryos between 4- to 100-cell stage for Jankele et al.Dryad Digital Repository, doi:10.5061/dryad.ghx3ffbmx.
Article and author information
Author details
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
© 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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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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During Caenorhabditis elegans development, multiple cells migrate long distances or extend processes to reach their final position and/or attain proper shape. The Wnt signalling pathway stands out as one of the major coordinators of cell migration or cell outgrowth along the anterior-posterior body axis. The outcome of Wnt signalling is fine-tuned by various mechanisms including endocytosis. In this study, we show that SEL-5, the C. elegans orthologue of mammalian AP2-associated kinase AAK1, acts together with the retromer complex as a positive regulator of EGL-20/Wnt signalling during the migration of QL neuroblast daughter cells. At the same time, SEL-5 in cooperation with the retromer complex is also required during excretory canal cell outgrowth. Importantly, SEL-5 kinase activity is not required for its role in neuronal migration or excretory cell outgrowth, and neither of these processes is dependent on DPY-23/AP2M1 phosphorylation. We further establish that the Wnt proteins CWN-1 and CWN-2, together with the Frizzled receptor CFZ-2, positively regulate excretory cell outgrowth, while LIN-44/Wnt and LIN-17/Frizzled together generate a stop signal inhibiting its extension.
