Abstract:During embryonic development, mechanical forces are essential for cellular rearrangements driving tissue morphogenesis. Here, we show that in the early zebrafish embryo, friction forces are generated at the interface between anterior axial mesoderm (prechordal plate, ppl) progenitors migrating towards the animal pole and neurectoderm progenitors moving in the opposite direction towards the vegetal pole of the embryo. These friction forces lead to global rearrangement of cells within the neurectoderm and determ… Show more
“…We further show that cell division, the main driver of cell rearrangements at this stage 13 , is required for fluid-like behavior and for the progress of gastrulation movements. Our results demonstrate the power of a hydrodynamic approach to tissue-wide morphogenetic processes [14][15][16] and provide a simple, unified mechanical picture of amniote gastrulation. A tensile embryo margin, in addition to directing tissue motion, could act as an interface between mechanical and molecular cues, and play a central role in embryonic self-organization.…”
Tissue morphogenesis is driven by local cellular deformations, themselves powered by contractile actomyosin networks. While it is well demonstrated that cell-generated forces at the microscopic scale underlie a variety of local morphogenetic processes (e.g. lengthening/ narrowing 1-4 , bending 5-8 , or folding 9,10 ), how such local forces are transmitted across tissues to shape them at a mesoscopic scale remains largely unknown. Here, by performing a quantitative analysis of gastrulation in entire avian embryos, we show that the formation of the primitive streak and the associated large-scale rotational tissue flows (i.e. 'polonaise' movements 11,12 ) are integral parts of a global process that is captured by the laws of fluid mechanics. We identify a large-scale supracellular actomyosin ring (2 mm in diameter and 250 µm thick) that shapes the embryo by exerting a graded tension along the margin between the embryonic and extra-embryonic territories. Tissue-wide flows arise from the transmission of these localized forces across the embryonic disk and are quantitatively recapitulated by a fluid-mechanical model based on the Stokes equations for viscous flow. We further show that cell division, the main driver of cell rearrangements at this stage 13 , is required for fluid-like behavior and for the progress of gastrulation movements. Our results demonstrate the power of a hydrodynamic approach to tissue-wide morphogenetic processes [14][15][16] and provide a simple, unified mechanical picture of amniote gastrulation. A tensile embryo margin, in addition to directing tissue motion, could act as an interface between mechanical and molecular cues, and play a central role in embryonic self-organization.
“…We further show that cell division, the main driver of cell rearrangements at this stage 13 , is required for fluid-like behavior and for the progress of gastrulation movements. Our results demonstrate the power of a hydrodynamic approach to tissue-wide morphogenetic processes [14][15][16] and provide a simple, unified mechanical picture of amniote gastrulation. A tensile embryo margin, in addition to directing tissue motion, could act as an interface between mechanical and molecular cues, and play a central role in embryonic self-organization.…”
Tissue morphogenesis is driven by local cellular deformations, themselves powered by contractile actomyosin networks. While it is well demonstrated that cell-generated forces at the microscopic scale underlie a variety of local morphogenetic processes (e.g. lengthening/ narrowing 1-4 , bending 5-8 , or folding 9,10 ), how such local forces are transmitted across tissues to shape them at a mesoscopic scale remains largely unknown. Here, by performing a quantitative analysis of gastrulation in entire avian embryos, we show that the formation of the primitive streak and the associated large-scale rotational tissue flows (i.e. 'polonaise' movements 11,12 ) are integral parts of a global process that is captured by the laws of fluid mechanics. We identify a large-scale supracellular actomyosin ring (2 mm in diameter and 250 µm thick) that shapes the embryo by exerting a graded tension along the margin between the embryonic and extra-embryonic territories. Tissue-wide flows arise from the transmission of these localized forces across the embryonic disk and are quantitatively recapitulated by a fluid-mechanical model based on the Stokes equations for viscous flow. We further show that cell division, the main driver of cell rearrangements at this stage 13 , is required for fluid-like behavior and for the progress of gastrulation movements. Our results demonstrate the power of a hydrodynamic approach to tissue-wide morphogenetic processes [14][15][16] and provide a simple, unified mechanical picture of amniote gastrulation. A tensile embryo margin, in addition to directing tissue motion, could act as an interface between mechanical and molecular cues, and play a central role in embryonic self-organization.
“…Zebrafish embryos have an average diameter of 600 μm and the ppl migrates along the circumference of the embryo and reaches the animal pole in about 4 h. Ppl cell fate specification can be visualized by the expression of the goosecoid ( gsc ) marker gene (Schulte-Merker et al, 1994). We used the zebrafish transgenic line expressing gsc::mEGFP (Smutny et al, 2017), to analyze gsc expression as well as cell shape and movement of ppl cells in vivo. As shown in Figure 9 and Video 7, using TipTracker we were able to follow the cluster of ppl cells, enabling uninterrupted imaging for several hours.10.7554/eLife.26792.016Figure 9.Imaging of Zebrafish prechordal plate using TipTracker with the LavisionBiotech TriM Scope II.( A ) Schematic representation of the shield stage of a six hpf gsc::mEGFP Zebrafish embryo.…”
Roots navigate through soil integrating environmental signals to orient their growth. The Arabidopsis root is a widely used model for developmental, physiological and cell biological studies. Live imaging greatly aids these efforts, but the horizontal sample position and continuous root tip displacement present significant difficulties. Here, we develop a confocal microscope setup for vertical sample mounting and integrated directional illumination. We present TipTracker – a custom software for automatic tracking of diverse moving objects usable on various microscope setups. Combined, this enables observation of root tips growing along the natural gravity vector over prolonged periods of time, as well as the ability to induce rapid gravity or light stimulation. We also track migrating cells in the developing zebrafish embryo, demonstrating the utility of this system in the acquisition of high-resolution data sets of dynamic samples. We provide detailed descriptions of the tools enabling the easy implementation on other microscopes.DOI:
http://dx.doi.org/10.7554/eLife.26792.001
“…Indeed, application of external strain can polarize cells in Xenopus gastrulae [15,16], and mechanical forces resulting from mesoderm and/or endoderm internalization have also been suggested as a contributing factor during germ band extension in Drosophila [17,18]. Similarly, friction between anterior axial mesoderm and the overlying neuroectoderm in zebrafish gastrulae is required for proper morphogenesis of the neural plate [19]**. Finally, the enveloping layer (EVL), the outermost epithelial cell layer, is required for doming and spreading of the blastoderm underlying epiboly during zebrafish gastrulation [20]*.…”
Section: Interactions Between Cells Of Adjacent Germ Layersmentioning
It is during gastrulation that the primordial germ layers are specified, embryonic axes become morphologically manifest, and the embryonic body plan begins to take shape. As morphogenetic movements push and pull nascent tissues into position within the gastrula, new interactions are established between neighboring cells and tissues. These interactions represent an emergent property within gastrulating embryos, and serve to regulate and promote ensuing morphogenesis that establishes the next set of cell/tissue contacts, and so on. Several recent studies demonstrate the critical roles of such interactions during gastrulation, including those between germ layers, along embryonic axes, and at tissue boundaries. Emergent tissue interactions result from - and result in - morphogen signaling, cell contacts, and mechanical forces within the gastrula. Together, these comprise a dynamic and complex regulatory cascade that drives gastrulation morphogenesis.
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