Dissecting the subcellular forces sculpting earlyC. elegansembryos

Abstract

SummaryEmbryo shape is governed by the mechanics of individual cells, the strength of intercellular interactions, and geometrical constraints. Models in which cells interact through surface tensions successfully predict cell arrangement within aggregates. However, predicting cell shape dynamics remains challenging because of difficulties in measuring temporal changes in tensions. Here, we dissect the spatiotemporal changes in cellular surface tensions that sculpt the early nematode embryo, using AFM measurements and inverse modeling. We validate a hybrid tension inference pipeline that combines dynamic information from cell geometry and cortical myosin enrichment. The inferred spatiotemporal tensions allow prediction of morphogenesis in wild-type embryos as well as phenotypic changes arising from protein depletion. We further uncover a direct and non-affine contribution of cadherins to cell contact tensions, whose magnitude is comparable to cadherins’ indirect contribution via actomyosin regulation. Overall, our inference pipeline allows characterization of the forces underlying morphogenesis and their relationship to molecular processes.HighlightsP lineage cells have lower cortical tensions than AB lineage cellsThe balance between cortical and cell-cell interfacial tensions determines, together with the confinement within the eggshell, the shape of theC. elegansembryo.Abundance of Myosin-II is a good predictor of cortical tension but is not sufficient to determine tension at cell-cell contacts.Myosin-informed tension inference allows determination of the spatiotemporal evolution of all surface tensions within the embryo.Cadherins contribute non-linearly to tension at cell-cell contacts.Open AccessFor the purpose of Open Access, the author has applied a CC BY public copyright license to any Author Accepted Manuscript version arising from this submission.