Skip to main content
Log in

Genetical analysis ofvisual system disorganizer (vid), a new gene involved in normal development of eye and optic lobe of the brain inDrosophila melanogaster

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

A neuroanatomical screening of a collection of P-element mutagenized flies has been carried out with the aim of finding new mutants affecting the optic lobe of the adult brain inDrosophila melanogaster. We have identified a new gene that is involved in the development of the adult axon array in the optic ganglia and in the ommatidia assembly. We have named this locusvisual system disorganizer (vid). Reversional mutagenesis demonstrated that thevid mutant was the result of a P-element insertion in theDrosophila genome and allowed us to generate independent alleles, some of which resulted in semilethality, like thevid original mutant, while the others were completely lethal. A genetic somatic mosaic analysis indicated that thevid gene is required in the eye for its normal development by inductive effects. This analysis also suggests an inductive effect of thevid gene on the distal portion of the optic lobe, particularly the lamina and the first optic chiasma. Moreover, the absence of mutant phenotype in the proximal region of the optic ganglia, including the medulla, the second optic chiasma, and the lobula complex underlying mosaic eyes, is suggestive of an autonomously acting mechanism of thevid gene in the optic lobe. The complete or partial lethality generated by different mutations at thevid locus suggests that this gene's role may not be limited to the visual system, but may also affect a vital function duringDrosophila development.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Anderson, H., 1978a. Postembryonic development of the visual system of the locust,Schistocerca gregaria. I. Patterns of growth and developmental interactions in the retina and optic lobe. J. Embryol. Exp. Morphol. 45: 55–83.

    Google Scholar 

  • Anderson, H., 1978b. Postembryonic development of the visual system of the locust,Schistocerca gregaria. II. An experimental investigation of the formation of the retina-lamina projection. J. Embryol. Exp. Morphol. 46: 147–170.

    Google Scholar 

  • Ashburner, M., 1989. Drosophila. A laboratory manual. Cold Spring Harbor Laboratory Press. New York, USA.

    Google Scholar 

  • Banerjee, U., P.J. Renfranz, J.A. Pollock & S. Benzer, 1987. Molecular characterization and expression ofsevenless, a gene involved in neuronal pattern formation in theDrosophila eye. Cell 49: 281–291.

    Google Scholar 

  • Benzer, S., 1967. Behavioral mutants ofDrosophila isolated by countercurrent distribution. Proc. Natl. Acad. Sci. USA. 58: 1112–1119.

    Google Scholar 

  • Braitenberg, V., 1967. Pattern of projection in the visual system of the fly. I. Retina-lamina Projections. Exp. Brain Res. 3: 271–298.

    Google Scholar 

  • Brunner, A., T. Twardzik & S. Schneuwly, 1994. TheDrosophila giant lens gene plays a dual role in eye and optic lobe development: Inhibition of differentiation of ommatidial cells and interference in photoreceptor axon guidance. Mech. Dev. 48: 175–185.

    Google Scholar 

  • Cagan, R., 1993. Cell fate specification in the developingDrosophila retina. Development, Suppl., 19–28.

  • Campos, A.R., K.F. Fischbach & H. Steller, 1992. Survival of photoreceptor neurons in the compound eye ofDrosophila depends on connections with the optic ganglia. Development 114: 355–366.

    Google Scholar 

  • Canal, I., C.I. Farinas, M. Gho & A. Ferrus, 1994. The presynaptic cell determines the number of synapses in theDrosophila optic ganglia. Eur. J. Neurosci. 6(9): 1423–1431.

    Google Scholar 

  • Cheyette, B.N., P.J. Green, K. Martin, H. Garren, V. Hartenstein & S.L. Zipursky, 1994. TheDrosophila sine oculis locus encodes a homeodomain-containing protein required for the development of the entire visual system. Neuron 12(5): 977–996.

    Google Scholar 

  • Duus, K.M., W.S. Welshons & J.R. Girton, 1992.Blackpatch, a Neural Degeneration Mutation That Interacts with theNotch Locus inDrosophila. Dev. Biol. 151: 34–47.

    Google Scholar 

  • Ebens, A.J., H. Garren, B.N.R. Cheyette & S.L. Zipursky, 1993. TheDrosophila anachronism locus: A glycoprotein secreted by glia inhibits neuroblast proliferation. Cell 74: 15–27.

    Google Scholar 

  • Ellis, M.C., E.M. O'Neill & G.M. Rubin, 1993. Expression ofDrosophila glass protein and evidence for negative regulation of its activity in non-neuronal cells by another DNA-binding protein. Development 119: 855–865.

    Google Scholar 

  • Fischbach, K.F., 1983. Neural cell types surviving congenital sensory deprivation in the optic lobes ofDrosophila melanogaster. Dev. Biol. 95: 1–18.

    Google Scholar 

  • Fischbach, K.-F. & A.P.M. Dittrich, 1989. The optic lobe ofDrosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res. 258: 441–475.

    Google Scholar 

  • Fischbach, K.F. & M. Heisenberg, 1981. Structural brain mutant ofDrosophila melanogaster with reduced cell number in the medulla cortex and with normal optomotor yaw response. Proc. Natl. Acad. Sci. 78(2): 1105–1109.

    Google Scholar 

  • Fischbach, K.F. & G. Technau, 1984. Cell Degeneration in the Developing Optic Lobes of thesine oculis andsmall-optic-lobes Mutants ofDrosophila melanogaster. Dev. Biol. 104: 219–239.

    Google Scholar 

  • Freeman, M., C. Klämbt, C. Goodman & G.M. Rubin, 1992. Theargos gene encodes a diffusible factor that regulates cell fate decisions in theDrosophila eye. Cell 69: 963–975.

    Google Scholar 

  • Fujita, S.C., S.L. Zipursky, S. Benzer, A. Ferrus & S.L. Shotwell, 1982. Monoclonal antibodies against the Drosophila nervous system. Proc. Natl. Acad. Sci. 79: 7929–7933.

    Google Scholar 

  • Garen, S.H. & D.R. Kankel, 1983. Golgi and genetic mosaic analyses of visual system mutants inDrosophila. Dev. Biol. 96: 445–466.

    Google Scholar 

  • Garrity, P.A., Y. Rao, I. Salecker, J. McGlade, T. Pawson & S.L. Zipursky, 1996.Drosophila photoreceptor axon guidance and targeting requires the Dreadlocks SH2/SH3 adapter protein. Cell 85: 639–650.

    Google Scholar 

  • Green, P., A.Y. Hartenstein & V. Hartenstein, 1993. The embryonic development of theDrosophila visual system. Cell Tissue Res. 273: 583–598.

    Google Scholar 

  • Hafen, E. & K. Basler, 1990. Mechanisms of positional signalling in the developing eye ofDrosophila studied by ectopic expression ofsevenless andrough. J. Cell Sci. Suppl. 13: 157–168.

    Google Scholar 

  • Halter, D.A., J. Urban, C. Rickert, S.S. Ner., K. Ito, A.A. Travers & G.M. Technau, 1995. The homeobox generepo is required for the differentiation and maintenance of glia function in the embryonic nervous system ofDrosophila melanogaster. Development 121: 317–322.

    Google Scholar 

  • Harris, W.A., W.S. Stark & J.A. Walker, 1976. Genetic dissection of the photoreceptor system in the compound eye ofDrosophila melanogaster. J. Physiol. 256: 415–439.

    Google Scholar 

  • Heberlein, V. & G.M. Rubin, 1991.Star is required in a subset of photoreceptor cells in the developingDrosophila retina and displays dosage sensitive interactions withrough. Dev. Biol. 144: 353–361.

    Google Scholar 

  • Heisenberg, M. & K. Böhl, 1978. Isolation of anatomical brain mutants ofDrosophila by histological means. Z. Naturforsch 34: 143–147.

    Google Scholar 

  • Heisenberg, M., R. Wonneberger & R. Wolf, 1978. Optomotorblind — ADrosophila mutant of the lobula plate giant neurones. J. Comp. Physiol. 124: 287–296.

    Google Scholar 

  • Hofbauer, A. & J.A. Campos-Ortega, 1990. Proliferation pattern and early differentiation of the optic lobe inDrosophila melanogaster. Roux's Arch. Dev. Biol. 198: 264–274.

    Google Scholar 

  • Huang, Z. & S. Kunes, 1996. Hedgehog, transmitted along retinal axons, triggers neurogenesis in the developing visual centers of theDrosophila brain. Cell 86: 411–422.

    Google Scholar 

  • Jäger, R.F. & K.F. Fischbach, 1987. Some improvements of the Heisenberg-Böhl method for mass histology ofDrosophila heads. Droso. Inform. Ser. 66: 162–165.

    Google Scholar 

  • Kankel, D.R. & J.C. Hall, 1976. Fate Mapping of Nervous System and Other Internal Tissues in Genetic Mosaics ofDrosophila melanogaster. Dev. Biol. 48: 1–24.

    Google Scholar 

  • Kaphingst, K. & S. Kunes, 1994. Pattern formation in the visual centers of theDrosophila brain.wingless acts viadecapentaplegic to specify the dorsoventral axis. Cell 78: 437–448.

    Google Scholar 

  • Karpilow, J., A. Kolodkin, T. Bork & T. Venkatesh, 1989. Neuronal development in theDrosophila compound eye:rap gene function is required in photoreceptor cell R8 for ommatidial pattern formation. Genes Dev. 3: 1834–1844.

    Google Scholar 

  • Kramer, S., S.R. West & Y. Hiromi, 1995. Cell fate control in theDrosophila retina by the orphan receptor seven-up: its role in the decisions mediated by the ras signaling pathway. Development 121: 1361–1372.

    Google Scholar 

  • Kretzchmar, D., A. Brunner, V. Wiersdorff, G.O. Pflugfelder, M. Heisenberg & S. Schneuwly, 1992.giant lens, a gene involved in cell determination and axon guidance in the visual system ofDrosophila melanogaster. EMBO J. 11(7): 2531–2539.

    Google Scholar 

  • Kunes, S., C. Wilson & H. Steller, 1993. Independent Guidance of Retinal Axons in the Developing Visual System ofDrosophila. J. Neurosci. 13(2): 752–767.

    Google Scholar 

  • Laski, F.A., D.C. Rio & G.M. Rubin, 1986. Tissue Specificity of Drosophila P Element Transposition Is Regulated at the Level of mRNA Splicing. Cell 44: 7–19.

    Google Scholar 

  • Lipshitz, H.D. & D.R. Kankel, 1985. Specificity of Gene Action during Central Nervous System Development inDrosophila melanogaster: Analysis of thelethal (1) optic ganglion reduced Locus. Dev. Biol. 108: 56–77.

    Google Scholar 

  • Liu, H., C. Ma & K. Moses, 1996. Identification and functional characterization of conserved promoter elements fromglass: a retinal development gene ofDrosophila. Mech. Dev. 56: 773–782.

    Google Scholar 

  • Martin, K.A., B. Poeck, H. Roth, A.J. Ebens, L.C. Ballard & S.L. Zipursky, 1995. Mutations disrupting neuronal connectivity in theDrosophila visual system. Neuron 14(2): 229–240.

    Google Scholar 

  • Meinertzhagen, I.A. & T.E. Hanson, 1993. The development of the optic lobe, pp. 1363–1491 in The Development of Drosophila melanogaster, edited by M. Bate and A. Martinez-Arias. Cold Spring Harbor Laboratory Press, New York.

    Google Scholar 

  • Meyerowitz, E.M. & D.R. Kankel, 1978. A Genetic Analysis of Visual System Development inDrosophila melanogaster. Dev. Biol. 62: 112–142.

    Google Scholar 

  • Moses, K. & G.M. Rubin, 1991.glass encodes a site-specific DNA-binding protein that is regulated in response to positional signals in the developingDrosophila eye. Genes Dev. 5: 583–593.

    Google Scholar 

  • Okano, H., S. Hayashi, T. Tanimura, K. Sawamoto, S. Yoshikawa, J. Watanabe, M. Iwasaki, S. Hirose, K. Mikoshiba & C. Montell, 1992. Regulation ofDrosophila neural development by a putative secreted protein. Differentiation 52: 1–11.

    Google Scholar 

  • Palazzolo, M.J., D.R. Hyde, K. Vijay Raghavan, K. Mecklenburg, S. Benzer & E. Meyerowitz, 1989. Use of a New Strategy to Isolate and Characterize 436Drosophila cDNA Clones Corresponding to RNAs Detected in Adult Heads but Not in Early Embryos. Neuron 3: 527–539.

    Google Scholar 

  • Pflugfelder, G.O., H. Roth, B. Poeck, S. Kerscher, H. Schwarz, B. Jonschker & M. Heisenberg, 1992. Thelethal(l)optomotor-blind gene ofDrosophila melanogaster is a major organizer of optic lobe development: isolation and characterization of the gene. Proc. Natl. Acad. Sci. 89: 1199–1203.

    Google Scholar 

  • Power, M.E., 1943a. The brain ofDrosophila melanogaster. J. Morphol. 72: 517–559.

    Google Scholar 

  • Power, M.E., 1943b. The effect of reduction in number of ommatidia upon the brain ofDrosophila melanogaster. J. Exp. Zool. 94: 33–71.

    Google Scholar 

  • Ramos, R.P.G., G.L. Igloi, B. Lichte, U. Baumann, D. Maier, T. Schneider, J.H. Brandstätter, A. Fröhlich & K.F. Fischbach, 1993. Theirregular chiasma C-roughest locus ofDrosophila, which affects axonal projections and programmed cell death, encodes a novel immunoglobulin-like protein. Genes Dev. 7: 2533–2547.

    Google Scholar 

  • Ready, D.F., 1989. A multifaceted approach to neural development. Trends Neurosci. 12(3): 102–110.

    Google Scholar 

  • Ready, D.F., T.E. Hanson & S. Benzer, 1976. Development of theDrosophila retina, a neurocrystalline lattice. Dev. Biol. 53: 217–240.

    Google Scholar 

  • Reinke, R. & S.L. Zipursky, 1988. Cell-cell interaction in theDrosophila retina: TheBride of sevenless gene is required in photoreceptor cell R8 for R7 cell development. Cell 55: 321–330.

    Google Scholar 

  • Robertson, H.M. & W.R. Engels, 1989. Modified P Elements That Mimic the P Cytotype inDrosophila melanogaster. Genetics 123: 815–824.

    Google Scholar 

  • Robertson, H.M., C.R. Preston, R.W. Phillis, D.M. Johnson-Schlitz, W.K. Benz & W.R. Engels, 1988. A Stable Genomic Source of P Element Transposase inDrosophila melanogaster. Genetics 118: 461–470.

    Google Scholar 

  • Rubin, G.M., 1989. Development of theDrosophila retina: inductive events studied at single cell resolution. Cell 57: 519–520.

    Google Scholar 

  • Saint, R., B. Kalionis, T.J. Lockett & A. Elizur, 1988. Pattern formation in the developing eye ofDrosophila melanogaster is regulated by the homeo-box gene,rough. Nature 334: 151–154.

    Google Scholar 

  • Sawamoto, K., M. Okabe, T. Tanimura, S. Hayashi, K. Mikoshiba & H. Okano, 1996.argos is required for projection of photoreceptor axons during optic lobes development inDrosophila. Dev. Dynamics 205: 162–171.

    Google Scholar 

  • Schneider, T., C. Reiter, E. Eule, B. Bader, B. Lichte, Z. Nie, T. Schimansky, R.G. Ramos & K.F. Fischbach, 1995. Restricted expression of the Irre C-rst protein is required for normal axonal projections of columnar visual neurons. Neuron 15(2): 259–271.

    Google Scholar 

  • Selleck, S.B. & H. Steller, 1991. The Influence of Retinal Innervation on Neurogenesis in the First Optic Ganglion ofDrosophila. Neuron 6: 83–99.

    Google Scholar 

  • Serikaku, M.A. & J.E. O'Tousa, 1994.Sine oculis is a homeobox gene required forDrosophila visual system development. Genetics 138(4): 1137–1150.

    Google Scholar 

  • Steller, H., K.F. Fischbach & G.M. Rubin, 1987.disconnected: A Locus Required for Neuronal Pathway Formation in the Visual System ofDrosophila. Cell 50: 1139–1153.

    Google Scholar 

  • Strausfeld, N.J., 1976. Atlas of an Insect Brain. Springer-Verlag Press, Berlin.

    Google Scholar 

  • Tomlinson, A., 1988. Cellular interactions in the developing Drosophila eye. Development 104: 183–193.

    Google Scholar 

  • Tomlinson, A. & D.E. Ready, 1987. Neuronal differentiation in theDrosophila ommatidium. Dev. Biol. 120: 366–376.

    Google Scholar 

  • White, K. & D.R. Kankel, 1978. Patterns of cell division and cell movement in the formation of the imaginal nervous system inDrosophila melanogaster. Dev. Biol. 65: 296–321.

    Google Scholar 

  • Wolff, T. & D.F. Ready, 1993. Pattern formation in theDrosophila retina, pp. 1277–1325 in The Development ofDrosophila melanogaster, edited by M. Bate & A. Martinez-Arias. Cold Spring Harbor Laboratory Press, New York.

    Google Scholar 

  • Xiong, W.C. & C. Montell, 1995. Defective glia induce neuronal apoptosis in therepo visual system ofDrosophila. Neuron 14(3): 581–590.

    Google Scholar 

  • Xiong, W.C., H. Okano, N.H. Patel, J.A. Blendy & C. Montell, 1994.repo encodes a glial specific homeodomain protein required in theDrosophila nervous system. Genes Dev. 8: 981–994.

    Google Scholar 

  • Zipursky, S.L., T.R. Venkatesh & S. Benzer, 1985. From monoclonal antibody to gene for a neuron-specific glycoprotein inDrosophila. Proc. Natl. Acad. Sci. 82: 1855–1859.

    Google Scholar 

  • Zucker, C.S., A.F. Cowan & G.M. Rubin, 1985. Isolation and structure of a rhodopsin gene fromD. melanogaster. Cell 40: 851–858.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rachidi, M., Lopes, C. & Benichou, JC. Genetical analysis ofvisual system disorganizer (vid), a new gene involved in normal development of eye and optic lobe of the brain inDrosophila melanogaster . Genetica 99, 31–45 (1997). https://doi.org/10.1007/BF02259496

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02259496

Key words

Navigation