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A tensile ring drives tissue flows to shape the gastrulating amniote embryo

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Science  24 Jan 2020:
Vol. 367, Issue 6476, pp. 453-458
DOI: 10.1126/science.aaw1965

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Shaping the early amniote embryo

Gastrulation is an essential step in development in which the internal tissues of the body are set apart. In birds and mammals, a similar cascade of molecular events is known to specify embryonic territories, but how they are physically remodeled has remained elusive. Working with avian embryos, Saadaoui et al. identified a cable that encircles the embryo as the engine of gastrulation and described the collective cell movements as similar to the motion of a fluid. One side of this contractile ring pulls more strongly than the other, entraining the large-scale tissue movements that shape the early body plan. The embryo margin, previously known to function in molecular regulation, thus emerges as a dual mechanical and molecular organizer of development.

Science, this issue p. 453

Abstract

Tissue morphogenesis is driven by local cellular deformations that are powered by contractile actomyosin networks. How localized forces are transmitted across tissues to shape them at a mesoscopic scale is still unclear. Analyzing gastrulation in entire avian embryos, we show that it is driven by the graded contraction of a large-scale supracellular actomyosin ring at the margin between the embryonic and extraembryonic territories. The propagation of these forces is enabled by a fluid-like response of the epithelial embryonic disk, which depends on cell division. A simple model of fluid motion entrained by a tensile ring quantitatively captures the vortex-like “polonaise” movements that accompany the formation of the primitive streak. The geometry of the early embryo thus arises from the transmission of active forces generated along its boundary.

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