2023Science AdvancesOpen access

A mechanochemical model recapitulates distinct vertebrate gastrulation modes

Mattia Serra, Guillermo Serrano Nájera, Manli Chuai, Alex M. Plum, Sreejith Santhosh, Vamsi Spandan, Cornelis J. Weijer, L. Mahadevan

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Abstract

During vertebrate gastrulation, an embryo transforms from a layer of epithelial cells into a multilayered gastrula. This process requires the coordinated movements of hundreds to tens of thousands of cells, depending on the organism. In the chick embryo, patterns of actomyosin cables spanning several cells drive coordinated tissue flows. Here, we derive a minimal theoretical framework that couples actomyosin activity to global tissue flows. Our model predicts the onset and development of gastrulation flows in normal and experimentally perturbed chick embryos, mimicking different gastrulation modes as an active stress instability. Varying initial conditions and a parameter associated with active cell ingression, our model recapitulates distinct vertebrate gastrulation morphologies, consistent with recently published experiments in the chick embryo. Altogether, our results show how changes in the patterning of critical cell behaviors associated with different force-generating mechanisms contribute to distinct vertebrate gastrulation modes via a self-organizing mechanochemical process.

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During vertebrate gastrulation, an embryo transforms from a layer of epithelial cells into a multilayered gastrula. This process requires the coordinated movements of hundreds to tens of thousands of cells, depending on the organism. In the chick embryo, patterns of actomyosin cables spanning several cells drive coordinated tissue flows. Here, we derive a minimal theoretical framework that couples actomyosin activity to global tissue flows. Our model predicts the onset and development of gastrulation flows in normal and experimentally perturbed chick embryos, mimicking different gastrulation modes as an active stress instability. Varying initial conditions and a parameter associated with active cell ingression, our model recapitulates distinct vertebrate gastrulation morphologies, consistent with recently published experiments in the chick embryo. Altogether, our results show how changes in the patterning of critical cell behaviors associated with different force-generating mechanisms contribute to distinct vertebrate gastrulation modes via a self-organizing mechanochemical process.

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Available abstract

During vertebrate gastrulation, an embryo transforms from a layer of epithelial cells into a multilayered gastrula. This process requires the coordinated movements of hundreds to tens of thousands of cells, depending on the organism. In the chick embryo, patterns of actomyosin cables spanning several cells drive coordinated tissue flows. Here, we derive a minimal theoretical framework that couples actomyosin activity to global tissue flows. Our model predicts the onset and development of gastrulation flows in normal and experimentally perturbed chick embryos, mimicking different gastrulation modes as an active stress instability. Varying initial conditions and a parameter associated with active cell ingression, our model recapitulates distinct vertebrate gastrulation morphologies, consistent with recently published experiments in the chick embryo. Altogether, our results show how changes in the patterning of critical cell behaviors associated with different force-generating mechanisms contribute to distinct vertebrate gastrulation modes via a self-organizing mechanochemical process.

Key concepts: Gastrulation, Ingression, Embryo, Vertebrate, Cell biology, Biology, Process (computing), Embryogenesis

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