Scanning electron microscopy of Drosophila melanogaster embryogenesis

Fr, Turner; Ap, Mahowald

doi:10.1016/0012-1606(77)90225-1

Cited by 200 publications

(14 citation statements)

References 15 publications

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“…This phase of embryogenesis spans stage 13 to the end of stage 15 and at 25°C corresponds to ∼9.3 h to ∼13 h, respectively, after egg lay (note, however, that our experiments were performed at room temperature, ∼20–23°C on embryos typically aged overnight at 18°C). The staging and morphology of the embryo are described in detail for both living specimens and fixed and sectioned material in Campos-Ortega and Hartenstein 1997(see pages 72–86), and has been studied by scanning electron microscopy (Turner and Mahowald 1977, Turner and Mahowald 1979) and is documented in this study by video time-lapsed analysis. (See also Flybase at http://flybase.bio.indiana.edu:82/images/lk/Animation/gas trulation-dorsal.mpg.…”

Section: Resultsmentioning

confidence: 99%

Multiple Forces Contribute to Cell Sheet Morphogenesis for Dorsal Closure in Drosophila

Kiehart

Galbraith

Edwards

et al. 2000

The Journal of Cell Biology

620

753

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The molecular and cellular bases of cell shape change and movement during morphogenesis and wound healing are of intense interest and are only beginning to be understood. Here, we investigate the forces responsible for morphogenesis during dorsal closure with three approaches. First, we use real-time and time-lapsed laser confocal microscopy to follow actin dynamics and document cell shape changes and tissue movements in living, unperturbed embryos. We label cells with a ubiquitously expressed transgene that encodes GFP fused to an autonomously folding actin binding fragment from fly moesin. Second, we use a biomechanical approach to examine the distribution of stiffness/tension during dorsal closure by following the response of the various tissues to cutting by an ultraviolet laser. We tested our previous model (Young, P.E., A.M. Richman, A.S. Ketchum, and D.P. Kiehart. 1993. Genes Dev. 7:29–41) that the leading edge of the lateral epidermis is a contractile purse-string that provides force for dorsal closure. We show that this structure is under tension and behaves as a supracellular purse-string, however, we provide evidence that it alone cannot account for the forces responsible for dorsal closure. In addition, we show that there is isotropic stiffness/tension in the amnioserosa and anisotropic stiffness/tension in the lateral epidermis. Tension in the amnioserosa may contribute force for dorsal closure, but tension in the lateral epidermis opposes it. Third, we examine the role of various tissues in dorsal closure by repeated ablation of cells in the amnioserosa and the leading edge of the lateral epidermis. Our data provide strong evidence that both tissues appear to contribute to normal dorsal closure in living embryos, but surprisingly, neither is absolutely required for dorsal closure. Finally, we establish that the Drosophila epidermis rapidly and reproducibly heals from both mechanical and ultraviolet laser wounds, even those delivered repeatedly. During healing, actin is rapidly recruited to the margins of the wound and a newly formed, supracellular purse-string contracts during wound healing. This result establishes the Drosophila embryo as an excellent system for the investigation of wound healing. Moreover, our observations demonstrate that wound healing in this insect epidermal system parallel wound healing in vertebrate tissues in situ and vertebrate cells in culture (for review see Kiehart, D.P. 1999. Curr. Biol. 9:R602–R605).

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Section: Resultsmentioning

confidence: 99%

Multiple Forces Contribute to Cell Sheet Morphogenesis for Dorsal Closure in Drosophila

Kiehart

Galbraith

Edwards

et al. 2000

The Journal of Cell Biology

620

753

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“…The double sheet then merges with the same structure of the next furrow to generate two separate bilayers, one belonging to the blastomere and one enclosing the yolk. The latter constitutes the yolk sac membrane and has been identified with scanning electron microscopy (49). The mature Ret protein is expected to be present on the surface of the yolk sac membrane, facing the inner surface of the germband with its extracellular domain.…”

Section: Discussion Ret Expression In Endoderm Derivativesmentioning

confidence: 99%

Expression pattern of Drosophila ret suggests a common ancestral origin between the metamorphosis precursors in insect endoderm and the vertebrate enteric neurons

Hahn¹

2001

Proceedings of the National Academy of Sciences

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The RET gene, encoding a receptor tyrosine kinase, is unusual among human protooncogenes in that its mutant alleles are implicated in a developmental defect involving enteric neurons as well as in tumorigenesis. The cells affected in both types of disorders are derived from the neural crest. Targeted disruption of mouse ret has revealed an additional role in kidney development. Here we report the analysis of a ret homolog in Drosophila melanogaster, an arthropod with no neural crest. Drosophila ret (D-ret) encodes a protein of 1,235 amino acids that has all of the domains identified in the vertebrate ret, including a cadherin motif. During embryogenesis, D-ret mRNA is first detected in the yolk sac at the late gastrula stage. In the postgastrula, D-ret is expressed in the foregut neurons, excretory system, peripheral ganglia, and the central nervous system. Thus, despite the wide divergence of early embryonic fate maps between vertebrates and invertebrates, D-ret is expressed in cells that are presumed to be the functional equivalents of the ret-expressing cells in vertebrates. Unexpectedly, D-ret is also expressed in the imaginal islands of the endodermal gut. These cells are proliferation-competent precursors for adult midgut that are diffusely embedded in the growth-arrested juvenile gut. These ret-expressing nonneuronal cells are strikingly analogous to vertebrate enteric neurons in their topography, but not in their cell fate. Our finding suggests a previously unrecognized phylogenetic relationship between the ret-expressing cells in vertebrates and the precursor reserves of metamorphosing insects.

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“…During this process, ∼1200 cells along the ventral midline (a group roughly 70 cells long and 18 cells wide) apically constrict in a coordinated way (Fig. 2), leading to invagination of a tube of cells that will form the embryonic mesoderm (Kam et al, 1991;Sweeton et al, 1991;Turner and Mahowald, 1977). Ventral furrow cells constrict asymmetrically, with cells exhibiting more constriction along the dorsal-ventral (DV) axis than along the anterior-posterior (AP) axis, where tension is highest.…”

Section: Introductionmentioning

confidence: 99%

Orchestrating morphogenesis: building the body plan by cell shape changes and movements

Perez-Vale

Peifer

2020

Development

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During embryonic development, a simple ball of cells re-shapes itself into the elaborate body plan of an animal. This requires dramatic cell shape changes and cell movements, powered by the contractile force generated by actin and myosin linked to the plasma membrane at cell-cell and cell-matrix junctions. Here, we review three morphogenetic events common to most animals: apical constriction, convergent extension and collective cell migration. Using the fruit fly Drosophila as an example, we discuss recent work that has revealed exciting new insights into the molecular mechanisms that allow cells to change shape and move without tearing tissues apart. We also point out parallel events at work in other animals, which suggest that the mechanisms underlying these morphogenetic processes are conserved.

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Scanning electron microscopy of Drosophila melanogaster embryogenesis

Cited by 200 publications

References 15 publications

Multiple Forces Contribute to Cell Sheet Morphogenesis for Dorsal Closure in Drosophila

Multiple Forces Contribute to Cell Sheet Morphogenesis for Dorsal Closure in Drosophila

Expression pattern of Drosophila ret suggests a common ancestral origin between the metamorphosis precursors in insect endoderm and the vertebrate enteric neurons

Orchestrating morphogenesis: building the body plan by cell shape changes and movements

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