The evolution of gastrulation morphologies

Nájera, Guillermo Serrano; Weijer, Cornelis J.

doi:10.1242/dev.200885

Cited by 15 publications

(9 citation statements)

References 92 publications

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“…We highlight that our biophysical model is sufficient to explain both the wild-type and manipulated gastrulation flows in the chick embryo, which show remarkable similarities to the gastrulation patterns naturally observed in other species. Whether our framework can explain (at least partially) the gastrulation flows in different vertebrates is a separate biological question that requires additional work ( 45 ).…”

Section: Resultsmentioning

confidence: 99%

“…In the recently published paper ( 4 ), we used drugs to modulate the ability for active cell ingression and the initial extent of the prospective mesendoderm and showed that the resulting gastrulation flows mirror those naturally observed in reptiles, amphibians, and fish in a single organism, the chick embryo, consistent with our model predictions. Additional or alternative driving forces may be at play in these other species ( 45 ). For example, studies of amphibian gastrulation in Xenopus have suggested that convergent thickening serves as an additional driving force during blastopore closure ( 47 – 49 ).…”

Section: Discussionmentioning

confidence: 99%

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A mechanochemical model recapitulates distinct vertebrate gastrulation modes

Serra,

Serrano Nájera,

Chuai

et al. 2023

Sci. Adv.

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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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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

A mechanochemical model recapitulates distinct vertebrate gastrulation modes

Serra,

Serrano Nájera,

Chuai

et al. 2023

Sci. Adv.

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“…1 and 2). Mesendoderm specification is required for large-scale cell flows associated with later stage ingression and intercalation at the PS during gastrulation (27, 50). Here, we have described the distinctive set of cell flows that precede gastrulation in the chick embryo, and the relationship between early and late cell flow has yet to be examined.…”

Section: Discussionmentioning

confidence: 99%

Coupling and uncoupling of midline morphogenesis and cell flow in amniote gastrulation

Asai

Prakash

Sinha

et al. 2023

Preprint

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Large-scale cell flow characterizes gastrulation in animal development. In amniote gastrulation, a bilateral vortex-like counter-rotating cell flow, called polonaise movements, appears along the midline. Here, through experimental manipulations, we addressed relationships between the polonaise movements and morphogenesis of the primitive streak, the earliest midline structure in amniotes. Suppression of the Wnt/planar cell polarity (PCP) signaling pathway maintains the polonaise movements along a deformed primitive streak. Mitotic arrest leads to diminished extension and development of the primitive streak and maintains the early phase of the polonaise movements. Ectopically induced Vg1, an axis-inducing morphogen, generates the polonaise movements, aligned to the induced midline, but disturbs the stereotypical cell flow pattern at the authentic midline. Despite the altered cell flow, induction and extension of the primitive streak is preserved along both authentic and induced midlines. Finally, we show that ectopic axis-inducing morphogen, Vg1, is capable of initiating the polonaise movements without concomitant PS extension under mitotic arrest conditions. These results are consistent with a model wherein primitive streak morphogenesis is required for the maintenance of the polonaise movements, but the polonaise movement is not necessarily responsible for primitive streak morphogenesis. Our data describe a previously undefined relationship between the large-scale cell flow and midline morphogenesis in gastrulation.

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“…Gastrulation is a process by which cells become internalized to form inter alia a gastric cavity that the animal uses for food digestion, and thus gastrulation is primarily the origin of the endoderm that significantly contributes to the through-gut. However, in many groups of bilaterian animals, formation of endoderm and mesoderm goes hand in hand [ 2 ]. The mode of gastrulation can vary between invagination and epiboly (the ingrowing of part of the blastula cell sheet that directly leads to the formation of an outer (ectodermal) and inner (endodermal or endodermal/mesodermal) cell sheet), delamination (directional cell division of the blastula epithelium), and immigration (immigration of cells from one pole ( polar immigration ) or the complete surface of the blastula epithelium) (reviewed in Budd and Jensen [ 2 – 4 ]).…”

Section: Introductionmentioning

confidence: 99%

“…However, in many groups of bilaterian animals, formation of endoderm and mesoderm goes hand in hand [ 2 ]. The mode of gastrulation can vary between invagination and epiboly (the ingrowing of part of the blastula cell sheet that directly leads to the formation of an outer (ectodermal) and inner (endodermal or endodermal/mesodermal) cell sheet), delamination (directional cell division of the blastula epithelium), and immigration (immigration of cells from one pole ( polar immigration ) or the complete surface of the blastula epithelium) (reviewed in Budd and Jensen [ 2 – 4 ]). The place of organized cell immigration (as seen in invagination , epiboly and polar immigration ) is called the blastopore, a structure that is thus crucial for the formation of mesoderm and endoderm.…”

Section: Introductionmentioning

confidence: 99%

New insights into mesoderm and endoderm development, and the nature of the onychophoran blastopore

Janssen,

Budd

2024

Front Zool

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Background Early during onychophoran development and prior to the formation of the germ band, a posterior tissue thickening forms the posterior pit. Anterior to this thickening forms a groove, the embryonic slit, that marks the anterior–posterior orientation of the developing embryo. This slit is by some authors considered the blastopore, and thus the origin of the endoderm, while others argue that the posterior pit represents the blastopore. This controversy is of evolutionary significance because if the slit represents the blastopore, then this would support the amphistomy hypothesis that suggests that a slit-like blastopore in the bilaterian ancestor evolved into protostomy and deuterostomy. Results In this paper, we summarize our current knowledge about endoderm and mesoderm development in onychophorans and provide additional data on early endoderm- and mesoderm-determining marker genes such as Blimp, Mox, and the T-box genes. Conclusion We come to the conclusion that the endoderm of onychophorans forms prior to the development of the embryonic slit, and thus that the slit is not the primary origin of the endoderm. It is thus unlikely that the embryonic slit represents the blastopore. We suggest instead that the posterior pit indeed represents the lips of the blastopore, and that the embryonic slit (and surrounding tissue) represents a morphologically superficial archenteron-like structure. We conclude further that both endoderm and mesoderm development are under control of conserved gene regulatory networks, and that many of the features found in arthropods including the model Drosophila melanogaster are likely derived.

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The evolution of gastrulation morphologies

Cited by 15 publications

References 92 publications

A mechanochemical model recapitulates distinct vertebrate gastrulation modes

A mechanochemical model recapitulates distinct vertebrate gastrulation modes

Coupling and uncoupling of midline morphogenesis and cell flow in amniote gastrulation

New insights into mesoderm and endoderm development, and the nature of the onychophoran blastopore

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