Skip to main content
Log in

Aspects of furrow membrane formation in the cleaving Drosophila embryo

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

During blastoderm formation, the Drosophila embryo produces a large area of new membrane to accommodate the simultaneous demands of approximately four thousand newly cleaved cells. The embryo was examined with the electron microscope at various stages during cleavage in order to investigate the high membrane forming capacity of these cells. Embryos were subjected to the histochemical procedure for the demonstration of thiamine pyrophosphatase. The enzyme was present in the cisternae of the endoplasmic reticulum, Golgi bodies and the nuclear envelope. No activity could be demonstrated on the furrow surface or at the furrow tip despite closely adjacent reactive cisternae. It is concluded that the endoplasmic reticulum and Golgi bodies are not major contributors to the new surface.

Lamellar bodies were frequently observed in the cytoplasm of all stages examined. The bodies showed a lamellar periodicity of approximately 3.5 nm, and were ultrastructurally similar in appearance after a variety of fixation procedures. The distribution of these bodies was markedly related to the stage of blastoderm formation. Before the commencement of cleavage, lamellar bodies were very prominent within a region 4–5 μm. below the cell surface. As cleavage progressed, the bodies became sparse or absent from this region but were apparent at the base of the blastoderm cells or in the sub-blastoderm region, where they were not previously present. Lamellar bodies with leaflets closely associated with, or in apparent continuity with, the cleavage furrow membrane were frequently observed. In these regions the lamellar periodicity was the same as the thickness of the membrane laminae. It is suggested that these bodies play a role in the synthesis of new membrane in the furrow.

Intercellular contact specializations between the developing membranes of the furrow were restricted to incipient desmosones and point contacts where the intercellular gap was reduced to 3 nm or less.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anderson, R. O., Roels, O. A.: Myelin-like configurations in Ochromonas malhamensis. J. Ultrastruct. Res. 20, 127–139 (1967)

    Google Scholar 

  • Arnold, J. M.: Cleavage furrow formation in a telolecithal egg (Loligo pealii). I. Filaments in early furrow formation. J. Cell Biol. 41, 894–904 (1969)

    Google Scholar 

  • Bluemink, J. G.: The first cleavage of the amphibian egg. J. Ultrastruct. Res. 32, 142–166 (1970)

    Google Scholar 

  • Bluemink, J. G.: Cytokinesis and cytochalasin-induced furrow regression in the first-cleavage zygote of Xenopus laevis. Z. Zellforsch. 121, 102–126 (1971)

    Google Scholar 

  • Campiche, M.: Les inclusions lamellaires des cellules alvéolaires dans le poumon du raton. J. Ultrastruct. Res. 3, 302–312 (1960)

    Google Scholar 

  • Candiollo, L., Filogamo, G.: Lamellar bodies within the neuroblasts of the neural tube in the chick embryo. Z. Zellforsch. 69, 480–488 (1966)

    Google Scholar 

  • Cecio, A.: Electron microscopic observations of young rat liver. I. Distribution and structure of the myelin figures (lamellar bodies). Z. Zellforsch. 62, 717–742 (1964)

    Google Scholar 

  • Curgy, J. J.: Influence du mode de fixation sur la possibilité d'observer des structures myéliniques dans les hépatocytes d'embryons de poulet. J. Microscopie (Paris) 7, 63–80 (1968)

    Google Scholar 

  • Doane, W. W.: Drosophila. In: Methods in developmental biology (ed. F. H. Wilt and N. K. Wessels), p. 219–244. New York: T. Y. Crowell Co. 1967

    Google Scholar 

  • Fullilove, S. L., Jacobson, A. G.: Nuclear elongation and cytokinesis in Drosophila montana. Develop. Biol. 26, 560–577 (1971)

    Google Scholar 

  • Kessel, R. G., Decker, R. S.: Cytodifferentiation in the Rana pipiens oocyte. IV. Ultrastructural localization of thiamine pyrophosphatase and horseradish peroxidase. Z. Zellforsch. 126, 1–16 (1972)

    Google Scholar 

  • Lentz, T. L., Trinkaus, J. P.: Differentiation of the junctional complex of surface cells in the developing Fundulus blastoderm. J. Cell Biol. 48, 455–472 (1971)

    Google Scholar 

  • Mahowald, A. P.: Fine structure of pole cells and polar granules in Drosophila melanogaster. J. exp. Zool. 151, 201–207 (1962)

    Google Scholar 

  • Mahowald, A. P.: Electron microscopy of the formation of the cellular blastoderm in Drosophila melanogaster. Exp. Cell Res. 32, 457–468 (1963a)

    Google Scholar 

  • Mahowald, A. P.: Ultrastructural differentiations during formation of the blastoderm in the Drosophila melanogaster embryo. Develop. Biol. 8, 186–204 (1963b)

    Google Scholar 

  • Mahowald, A. P.: Ultrastructural observations on oogenesis in Drosophila. J. Morph. 137, 29–48 (1972)

    Google Scholar 

  • Mercer, E. H.: The evolution of intracellular phospholipid membrane systems. In: The interpretation of ultrastructure (ed. R. J. C. Harris), p. 369–384. New York and London: Academic Press 1962

    Google Scholar 

  • Okada, E., Waddington, C. H.: The submicroscopic structure of the Drosophila egg. J. Embryol. exp. Morph. 7, 583–597 (1959)

    Google Scholar 

  • Pannese, E.: Structures possibly related to the formation of new mitochondria in spinal ganglion neuroblasts. J. Ultrastruct. Res. 15, 57–65 (1966a)

    Google Scholar 

  • Pannese, E.: Expansive growth of the nuclear envelope and formation of mitochondria in ganglion neuroblasts. Z. Zellforsch. 72, 295–324 (1966b)

    Google Scholar 

  • Rabinowitz, M.: Studies on the cytology and early embryology of the egg of Drosophila melanogaster. J. Morph. 69, 1–49 (1941)

    Google Scholar 

  • Ruby, J. R., Webster, R. M.: Origin of the Golgi complex in germ cells in the developing ovary of the bat. Z. Zellforsch. 133, 1–12 (1972)

    Google Scholar 

  • Sanders, E. J.: Association of the Golgi complex with the plasma membrane of amphibian embryonic cells. Protoplasma (Wien) 76, 115–122 (1973a)

    Google Scholar 

  • Sanders, E. J.: Intercellular contact in the unincubated chick embryo. Z. Zellforsch. 141, 459–468 (1973b)

    Google Scholar 

  • Sanders, E. J., Singal, P. K.: Furrow formation in Xenopus embryos: involvement of the Golgi body as revealed by ultrastructural localization of thiamine pyrophosphatase activity. Exp. Cell Res. in press (1975)

  • Sanders, E. J., Zalik, S. E.: The blastomere periphery of Xenopus laevis, with special reference to intercellular relationships. Wilhelm Roux' Archiv 171, 181–194 (1972)

    Google Scholar 

  • Selman, G. G., Perry, M. M.: Ultrastructural changes in the surface layers of the newt's egg in relation to the mechanism of its cleavage. J. Cell Sci. 6, 207–227 (1970)

    Google Scholar 

  • Selman, G. G., Waddington, C. H.: The mechanism of cell division in the cleavage of the newt's egg. J. exp. Biol. 32, 700–733 (1955)

    Google Scholar 

  • Singal, P. K., Sanders, E. J.: An ultrastructural study of the first cleavage of Xenopus embryos. J. Ultrastruct. Res. 47, 433–451 (1974a)

    Google Scholar 

  • Singal, P. K., Sanders, E. J.: Cytomembranes in first cleavage Xenopus embryos. Inter-relationships between Golgi bodies, endoplasmic reticulum and lipid droplets. Cell Tiss. Res. 154, 189–209 (1974b)

    Google Scholar 

  • Sonnenblick, B. P.: The early embryology of Drosophila melanogaster. In: Biology of Drosophila (ed. M. Demerec), p. 62–167. New York and London: Hafner Pub. Co. 1950

    Google Scholar 

  • Spornitz, V. M.: Lamellar bodies in oocytes of Xenopus laevis and their relation to their mode of fixation. Experientia (Basel) 29, 589–591 (1973)

    Google Scholar 

  • Stoeckenius, W.: The molecular structure of lipid-water systems and cell membrane models studied with the electron microscope. In: The interpretation of ultrastructure (ed. R. J. C. Harris), p. 349–367. New York and London: Academic Press 1962

    Google Scholar 

  • Warren, L.: The biological significance of turnover of the surface membrane of animal cells. Curr. Top. Develop. Biol. 4, 197–222 (1969)

    Google Scholar 

  • Wright, T. R. F.: The genetics of embryogenesis in Drosophila. Advanc. Genetics 15, 261–395 (1970)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Supported by the Medical Research Council of Canada.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sanders, E.J. Aspects of furrow membrane formation in the cleaving Drosophila embryo. Cell Tissue Res. 156, 463–474 (1975). https://doi.org/10.1007/BF00225106

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00225106

Key words

Navigation