Abstract

Formation of the anteroposterior and dorsoventral body axis in Caenorhabditis elegans depends on cortical flows and advection of polarity determinants. The role of this patterning mechanism in tissue polarization after formation of cell-cell contacts is not fully understood. Here, we demonstrate that planar asymmetries are established during left-right symmetry breaking: Centripetal cortical flows asymmetrically and differentially advect anterior polarity determinants (aPARs) from contacts to the medial cortex, resulting in their unmixing from apical myosin. Contact localization and advection of PAR-6 requires balanced CDC-42 activation, while asymmetric retention and advection of PAR-3 can occur independently of PAR-6. Concurrent asymmetric retention of PAR-3, E-cadherin/HMR-1 and opposing retention of antagonistic CDC-42 and Wnt pathway components leads to planar asymmetries. The most obvious mark of planar asymmetry, retention of PAR-3 at a single cell-cell contact, is required for proper cytokinetic cell intercalation. Hence, our data uncover how planar polarity is established in a system without the canonical planar cell polarity pathway through planar asymmetric retention of aPARs.

Highlights

  • Gradients in cortical tension can give rise to translocation of the contractile actomyosin network underlying the plasma membrane, a phenomenon called cortical flow (Chalut and Paluch, 2016)

  • More than 20 years ago, the concept was established that blastomeres in C. elegans are specified by a process of stepwise, binary diversification involving the Wnt pathway genes lit-1/NLK and pop-1/TCF/LEF (Kaletta et al, 1997; Lin et al, 1998)

  • Since the C. elegans embryo can be considered a squamous-like epithelium, this specification system will most likely require planar polarized domains to prevent cell-cell mixing at cell fate boundaries and during cell division, since cell divisions usually generate anteroposteriorly staggered configurations

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Summary

Introduction

Gradients in cortical tension can give rise to translocation of the contractile actomyosin network underlying the plasma membrane, a phenomenon called cortical flow (Chalut and Paluch, 2016). Planar Asymmetry Establishment in C. elegans formation of cell-cell contacts, where contact-dependent asymmetries determine cortical flow dynamics, which in turn determine spindle orientation through coupling to microtubule dynamics (Sugioka and Bowerman, 2018). These roles of cortical flow in patterning are orthologous in higher organisms, where they have been shown to drive decision making processes in development (Woolner and Papalopulu, 2012; Maître et al, 2016; Roubinet et al, 2017)

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