Nematic structures contribute to robust zygotic polarization in C. elegans
- 1CMPG, M2S Department, KU Leuven, Heverlee, Belgium
- 2MeBioS, Department of Biosystems, KU Leuven, Heverlee, Belgium
- 3ISREC, School of Life Sciences, EPFL, Lausanne, Switzerland
Abstract
The C. elegans zygote is a powerful model for asymmetric cell division. Its strikingly patterned cortex features thick F-actin bundles and myosin foci, contractile nematic structures that drive characteristic surface ruffles. Approximately 30 min after fertilization, symmetry breaks near the sperm-contributed centrosomes, typically at the presumptive posterior pole, and is marked by local downregulation of contractility. This initiates a cortical flow that polarizes the cell and enables PAR proteins to establish anterior and posterior domains. While biochemical mechanisms maintaining these domains are well understood, the mechanical role of cortical architecture in polarization remains unclear. We developed a three-dimensional (3D) mechanical model of C. elegans zygote polarization that represents the actin bundles and myosin foci of the cortex as a network of stiff contractile filaments. We measured cortical flow with high spatiotemporal resolution by tracking myosin foci, and used these data alongside mechanical properties from the literature to parametrize the model. The model simulates the complete polarization process in 3D, from symmetry breaking through domain stabilization, and reproduces key cortical dynamics including flow profiles, surface ruffles, and tension anisotropy. Domain arrest near the embryo midpoint emerges from density-dependent contractility regulation, in which cortical material redistribution during flow creates a mechanical negative feedback that balances anterior and posterior tension. We find that compressive flow aligns actin bundles in the anterior domain and generates anisotropic tension perpendicular to the flow direction. Although this alignment is not essential for polarization when symmetry breaking occurs at the pole, it contributes to this process when symmetry breaking occurs laterally. In such cases, anisotropic tension from aligned bundles drives axis convergence by rotating the posterior domain towards the nearest pole. Nematic cortical structures therefore ensure robust alignment of the polarization axis. Author summary: The first division of the C. elegans embryo is asymmetric and establishes its anterior and posterior ends, along the long axis of the elongated, ellipsoid egg. Polarization relies on a thin layer of contractile actomyosin beneath the cell surface, the cortex. The zygotic cortex is strikingly patterned, with a network of actin-fiber bundles, and clusters of myosin motors at the junctions. Does this cortical structure contribute to the process of cell polarization? We built a three-dimensional biomechanical model of the polarizing zygote that represents the contractile actin-bundle network. The model was kept simple, carefully parametrized by measured features where possible, and compared to detailed measurements of cortical movement. It reproduces the observed polarizing cortical flows and surface patterns. As the polarization progresses, the bundles align along the short axis of the embryo, but this is not required for the flow or polarization. Occasionally, polarization is triggered lateral to the long axis. Our model shows that bundle alignment then reorients the anterior and posterior domains during the flow, aligning them with the egg’s long axis. This illustrates how the physical architecture of a cellular structure contributes to a reliable developmental outcome.
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BibTeX
@article{vanslambrouck2026nematic,
title = {{Nematic structures contribute to robust zygotic polarization in C. elegans}},
author = {Michiel Vanslambrouck and Jef Vangheel and Ella Linxia Müller and Bart Smeets and Pierre Gönczy and Rob Jelier},
journal = {PLOS Computational Biology},
year = {2026},
month = sep,
doi = {10.1371/journal.pcbi.1014792},
url = {https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1014792},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Nematic structures contribute to robust zygotic polarization in C. elegans
AU - Michiel Vanslambrouck
AU - Jef Vangheel
AU - Ella Linxia Müller
AU - Bart Smeets
AU - Pierre Gönczy
AU - Rob Jelier
PY - 2026
DA - 2026/09/23
JO - PLOS Computational Biology
DO - 10.1371/journal.pcbi.1014792
UR - https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1014792
AB - The C. elegans zygote is a powerful model for asymmetric cell division. Its strikingly patterned cortex features thick F-actin bundles and myosin foci, contractile nematic structures that drive characteristic surface ruffles. Approximately 30 min after fertilization, symmetry breaks near the sperm-contributed centrosomes, typically at the presumptive posterior pole, and is marked by local downregulation of contractility. This initiates a cortical flow that polarizes the cell and enables PAR proteins to establish anterior and posterior domains. While biochemical mechanisms maintaining these domains are well understood, the mechanical role of cortical architecture in polarization remains unclear. We developed a three-dimensional (3D) mechanical model of C. elegans zygote polarization that represents the actin bundles and myosin foci of the cortex as a network of stiff contractile filaments. We measured cortical flow with high spatiotemporal resolution by tracking myosin foci, and used these data alongside mechanical properties from the literature to parametrize the model. The model simulates the complete polarization process in 3D, from symmetry breaking through domain stabilization, and reproduces key cortical dynamics including flow profiles, surface ruffles, and tension anisotropy. Domain arrest near the embryo midpoint emerges from density-dependent contractility regulation, in which cortical material redistribution during flow creates a mechanical negative feedback that balances anterior and posterior tension. We find that compressive flow aligns actin bundles in the anterior domain and generates anisotropic tension perpendicular to the flow direction. Although this alignment is not essential for polarization when symmetry breaking occurs at the pole, it contributes to this process when symmetry breaking occurs laterally. In such cases, anisotropic tension from aligned bundles drives axis convergence by rotating the posterior domain towards the nearest pole. Nematic cortical structures therefore ensure robust alignment of the polarization axis. Author summary: The first division of the C. elegans embryo is asymmetric and establishes its anterior and posterior ends, along the long axis of the elongated, ellipsoid egg. Polarization relies on a thin layer of contractile actomyosin beneath the cell surface, the cortex. The zygotic cortex is strikingly patterned, with a network of actin-fiber bundles, and clusters of myosin motors at the junctions. Does this cortical structure contribute to the process of cell polarization? We built a three-dimensional biomechanical model of the polarizing zygote that represents the contractile actin-bundle network. The model was kept simple, carefully parametrized by measured features where possible, and compared to detailed measurements of cortical movement. It reproduces the observed polarizing cortical flows and surface patterns. As the polarization progresses, the bundles align along the short axis of the embryo, but this is not required for the flow or polarization. Occasionally, polarization is triggered lateral to the long axis. Our model shows that bundle alignment then reorients the anterior and posterior domains during the flow, aligning them with the egg’s long axis. This illustrates how the physical architecture of a cellular structure contributes to a reliable developmental outcome.
SN - 1553-7358
ER -