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The embryonic development of the Drosophila visual system

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Abstract

We have used electron-microscopic studies, bromodeoxyuridine (BrdU) incorporation and antibody labeling to characterize the development of the Drosophila larval photoreceptor (or Bolwig's) organ and the optic lobe, and have investigated the role of Notch in the development of both. The optic lobe and Bolwig's organ develop by invagination from the posterior procephalic region. After cells in this region undergo four postblastoderm divisions, a total of approximately 85 cells invaginate. The optic lobe invagination loses contact with the outer surface of the embryo and forms an epithelial vesicle attached to the brain. Bolwig's organ arises from the ventralmost portion of the optic lobe invagination, but does not become incorporated in the optic lobe; instead, its 12 cells remain in the head epidermis until late in embryogenesis when they move in conjunction with head involution to reach their final position alongside the pharynx. Early, before head involution, the cells of Bolwig's organ form a superficial group of 7 cells arranged in a ‘rosette’ pattern and a deep group of 5 cells. Later, all neurons move out of the surface epithelium. Unlike adult photoreceptors, they do not form rhabdomeres; instead, they produce multiple, branched processes, which presumably carry the photopigment. Notch is essential for two aspects of the early development of the visual system. First, it delimits the number of cells incorporated into Bolwig's organ. Second, it is required for the maintenance of the epithelial character of the optic lobe cells during and after its invagination.

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References

  • Artavanis-Tsakonas S (1988) The molecular biology of the Notch locus and the fine tuning of differentiation in Drosophila. Trends Genet 4:95–100

    Google Scholar 

  • Bier E, Vaessin H, Shepherd S, Lee K, McCall K, Barbel S, Ackerman L, Carretto R, Uemura T, Grell E, Jan LY, Jan YN (1989) Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev 3:1273–1287

    Google Scholar 

  • Bodmer R, Carretto R, Jan YN (1989) Neurogenesis of the peripheral nervous system in Drosophila embryos: DNA replication patterns and cell lineages. Neuron 3:21–32

    Google Scholar 

  • Bolwig N (1946) Senses and sense organs of the anterior end of the house fly larvae. Vidensk Med Dansk Naturh Foren 109:81–217

    Google Scholar 

  • Cagan RL, Ready DF (1989) Notch is required for successive cell decisions in the developing Drosophila retina. Genes Dev 3:1099–1112

    Google Scholar 

  • Campos-Ortega JA (1988) Cellular interactions during early neurogenesis of Drosophila melanogaster. Trends Neurosci 11:400–405

    Google Scholar 

  • Campos-Ortega JA, Hartenstein V (1985a) Development of the nervous system. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry, and pharmacology, vol 5. Pergamon Press, Oxford, pp 49–85

    Google Scholar 

  • Campos-Ortega JA, Hartenstein V (1985b) The embryonic development of Drosophila melanogaster. Springer, Berlin

    Google Scholar 

  • Chen TY (1929) On the development of imaginal buds in normal and mutant Drosophila melanogaster. J Morphol 47:135–199

    Google Scholar 

  • Copenhaver PF, Taghert PH (1990) Neurogenesis in the insect enteric nervous system: generation of premigratory neurons from an epithelial placode. Development 109:17–28

    Google Scholar 

  • Corbin V, Michelson AM, Abmayr SM, Neel B, Alcamo E, Maniatis T, Young MW (1991) A role for the Drosophila neurogenic genes in mesoderm differentiation. Cell 67:311–323

    Google Scholar 

  • Ellsworth JK (1933) The photoreceptive organs of fleshfly larva, Lucilia sericata (Meigen): an experimental and anatomical study. Ann Entomol Soc Am 26:200–215

    Google Scholar 

  • Fehon RG, Johansen K, Rebay I, Artavanis-Tsakonas S (1991) Complex cellular and subcellular regulation of Notch expression during embryonic and imaginal development of Drosophila: implications for Notch function. J Cell Biol 113:657–669

    Google Scholar 

  • Hartenstein V (1988) Development of Drosophila larval sensory organs: spatiotemporal pattern of sensory neurones, peripheral axonal pathways and sensilla differentiation. Development 102:869–886

    Google Scholar 

  • Hartenstein V, Campos-Ortega JA (1984) Early neurogenesis in wildtype Drosophila melanogaster. Rouxs Arch Dev Biol 193:308–325

    Google Scholar 

  • Hartenstein V, Campos-Ortega JA (1986) The peripheral nervous system of mutants of early neurogenesis in Drosophila melanogaster. Rouxs Arch Dev Biol 195:210–221

    Google Scholar 

  • Hartenstein V, Jan YN (1992) Studying Drosophila embryogenesis with PlacZ enhancer trap lines. Rouxs Arch Dev Biol 201:194–220

    Google Scholar 

  • Hartenstein V, Posakony JW (1990) A dual function of the Notch gene in Drosophila sensillum development. Dev Biol 142:13–30

    Google Scholar 

  • Hartenstein V, Hartenstein A, Rugendorff AE, Green P (1991) The embryonic development of the Drosophila visual system (abstract). 32nd Annual Drosophila Research Conference, Chicago

  • Hartenstein AY, Rugendorff AE, Tepass U, Hartenstein V (1992) The function of the neurogenic genes during epithelial development in the Drosophila embryo. Development 116:1203–1220

    Google Scholar 

  • Heitzler P, Simpson P (1991) The choice of cell fate in the epidermis of Drosophila. Cell 64:1083–1092

    Google Scholar 

  • Hewitt CG (1914) The house-fly (Musca domestica)

  • Hofbauer A (1979) Die Entwicklung der optischen Ganglien bei Drosophila melanogaster. Inaugural-Dissertation, University of Freiburg i.Br.

  • Hofbauer A, Campos-Ortega JA (1990) Proliferation pattern and early differentiation of the optic lobes in Drosophila melanogaster. Rouxs Arch Dev Biol 198:264–274

    Google Scholar 

  • Hoppe PE, Greenspan RJ (1990) The Notch locus of Drosophila is required in epidermal cells for epidermal development. Development 109:875–885

    Google Scholar 

  • Jürgens G, Lehmann R, Schardin M, Nüsslein-Volhard C (1986) Segmental organisation of the head in the embryo of Drosophila melanogaster. Rouxs Arch Dev Biol 195:359–377

    Google Scholar 

  • Kidd S, Kelley MR, Young MW (1986) Sequence of the Notch locus of Drosophila melanogaster: relationship of the encoded protein to mammalian clotting and growth factors. Mol Cell Biol 6:3094–3108

    Google Scholar 

  • Kidd S, Baylies MK, Gasic GP, Young MW (1989) Structure and distribution of the Notch protein in developing Drosophila. Genes Dev 3:1113–1129

    Google Scholar 

  • Lehmann R, Jimenez F, Dietrich U, Campos-Ortega JA (1983) On the phenotype and development of mutants of early neurogenesis in Drosophila melanogaster. Rouxs Arch Dev Biol 192:62–74

    Google Scholar 

  • Lindsley DL, Grell EH (1968) Genetic variations of Drosophila melanogaster. (Publication no 627) Carnegie Institution of Washington

  • Madhavan MM, Schneiderman HA (1977) Histological analysis of the dynamics of growth of imaginal discs and histoblast nests during larval development of Drosophila melanogaster. Rouxs Arch Dev Biol 183:269–305

    Google Scholar 

  • Panayotou G, End P, Aumailley M, Timpl R, Engel J (1989) Domains of laminin with growth-factor activity. Cell 56:93–101

    Google Scholar 

  • Paulus HF (1989) Das Homologisieren in der Feinstrukturforschung: das Bolwig Organ der höheren Dipteren und seine Homologisierung mit Stemmata und Ommatidien eines ursprünglichen Facettenauges der Mandibulata. Zool Beitr NF 32:437–478

    Google Scholar 

  • Pollock JA, Benzer S (1988) Transcript localization of four opsin genes in the three visual organs of Drosophila melanogaster, RH2 is ocellus specific. Nature 333:779–782

    Google Scholar 

  • Poulson DF (1950) Histogenesis, organogenesis, and differentiation in the embryo of Drosophila melanogaster (Meigen). In: Demerec M (ed) Biology of Drosophila. Wiley, New York, pp 168–274

    Google Scholar 

  • Ready DF, Hanson TE, Benzer S (1976) Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol 53:217–240

    Google Scholar 

  • Ruohola H, Bremer KA, Beker D, Swedlow JR, Jan LY, Jan YN (1991) Role of neurogenic genes in establishment of follicle cell fate and oocyte polarity during oogenesis in Drosophila. Cell 66:433–439

    Google Scholar 

  • Shellenbarger DL, Mohler JD (1975) Temperature sensitive mutations of the Notch locus in Drosophila melanogaster. Genetics 81:143–162

    Google Scholar 

  • Steller H, Fischbach KF, Rubin G (1987) Disconnected: a locus required for neuronal pathway formation. Cell 50:1139–1153

    Google Scholar 

  • Tepass U, Theres C, Knust E (1990) crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia. Cell 61:787–799

    Google Scholar 

  • Tix S, Minden J, Technau GM (1987) Pre-existing neuronal pathways in the developing optic lobes of Drosophila. Development 105:739–746

    Google Scholar 

  • Turner FR, Mahowald AP (1979) Scanning electron microscopy of Drosophila embryogenesis. III. Formation of the head and caudal segments. Dev Biol 68:96–109

    Google Scholar 

  • Wharton KA, Johansen KM, Xu T, Artavanis-Tsakonas S (1985) Nucleotide sequence from the neurogenic locus Notch implies a gene product that shares homology with proteins containing EGF-like repeats. Cell 43:567–581

    Google Scholar 

  • White K, Kankel DR (1978) Patterns of cell division and cell movement in the formation of the imaginal nervous system in Drosophila melanogaster. Dev Biol 65:296–321

    Google Scholar 

  • Zipursky SI, Venkatesh TR, Teplow DB, Benzer S (1984) Neuronal development in the Drosophila retina: monoclonal antibodies as molecular probes. Cell 36:15–26

    Google Scholar 

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  1. Department of Biology, University of California Los Angeles, 90024, Los Angeles, CA, USA

    Patricia Green, Amelia Y. Hartenstein & Volker Hartenstein

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  1. Patricia Green
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  2. Amelia Y. Hartenstein
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  3. Volker Hartenstein
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Green, P., Hartenstein, A.Y. & Hartenstein, V. The embryonic development of the Drosophila visual system. Cell Tissue Res 273, 583–598 (1993). https://doi.org/10.1007/BF00333712

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  • DOI: https://doi.org/10.1007/BF00333712

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