Nematic structures contribute to robust zygotic polarization in C. elegans

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. Early in the cell cycle, 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. AvailabilityAll data and code required to reproduce the results are freely available at https://doi.org/10.5281/zenodo.18135771. The latest version of the software is maintained at https://bitbucket.org/pgmsembryogenesis/polarization.