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. 1992 Aug;131(4):883–894. doi: 10.1093/genetics/131.4.883

Mosaic Analysis Gives an Estimate of the Extent of Genomic Involvement in the Development of the Visual System in Drosophila Melanogaster

H M Thaker 1, D R Kankel 1
PMCID: PMC1205099  PMID: 1516819

Abstract

To investigate the role of vital loci in the development of the visual system of Drosophila, we induced mitotic recombination in individuals heterozygous for recessive organismal lethals and selected for analysis the resulting mosaics with homozygous mutant eye clones. Heads bearing clones were serially sectioned, silver-stained and examined for aberrations in the ommatidia and the neural structures to which they project. In our screen of 68 lines bearing diepoxybutane-induced X-linked lethals, 26 yielded few or no homozygous mutant clones (putative cell-lethals). Of the rest, 20 lines produced individuals with morphologically abnormal eye clones showing various degrees of aberrations in the ommatidial architecture. In 14 of these 20, the laminar cartridges innervated by the mutant clones were also disorganized. Clones with normal structure were found in 18 of the lines, and three lines were resistant to the induction of mitotic recombination. In a single line, comparatively normal clones in the eye projected to a lamina with subtle but consistent abnormalities. To the extent that we have a representative sample, these results suggest that about two-thirds of all vital genes may be essential for the normal assembly and neural connectivity of the eye. This points to a high degree of pleiotropy in the manner in which information in the genome of the fly is used in development.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Akam M. The molecular basis for metameric pattern in the Drosophila embryo. Development. 1987 Sep;101(1):1–22. [PubMed] [Google Scholar]
  2. Baker N. E., Rubin G. M. Effect on eye development of dominant mutations in Drosophila homologue of the EGF receptor. Nature. 1989 Jul 13;340(6229):150–153. doi: 10.1038/340150a0. [DOI] [PubMed] [Google Scholar]
  3. Benzer S. BEHAVIORAL MUTANTS OF Drosophila ISOLATED BY COUNTERCURRENT DISTRIBUTION. Proc Natl Acad Sci U S A. 1967 Sep;58(3):1112–1119. doi: 10.1073/pnas.58.3.1112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cagan R. L., Ready D. F. Notch is required for successive cell decisions in the developing Drosophila retina. Genes Dev. 1989 Aug;3(8):1099–1112. doi: 10.1101/gad.3.8.1099. [DOI] [PubMed] [Google Scholar]
  5. Campos-Ortega J. A. On compound eye development in Drosophila melanogaster. Curr Top Dev Biol. 1980;15(Pt 1):347–371. doi: 10.1016/s0070-2153(08)60123-4. [DOI] [PubMed] [Google Scholar]
  6. Campos A. R., Grossman D., White K. Mutant alleles at the locus elav in Drosophila melanogaster lead to nervous system defects. A developmental-genetic analysis. J Neurogenet. 1985 Jun;2(3):197–218. doi: 10.3109/01677068509100150. [DOI] [PubMed] [Google Scholar]
  7. Datta S., Kankel D. R. l(1)trol and l(1)devl, loci affecting the development of the adult central nervous system in Drosophila melanogaster. Genetics. 1992 Mar;130(3):523–537. doi: 10.1093/genetics/130.3.523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fischbach K. F. Neural cell types surviving congenital sensory deprivation in the optic lobes of Drosophila melanogaster. Dev Biol. 1983 Jan;95(1):1–18. doi: 10.1016/0012-1606(83)90002-7. [DOI] [PubMed] [Google Scholar]
  9. Fujita S. C., Zipursky S. L., Benzer S., Ferrús A., Shotwell S. L. Monoclonal antibodies against the Drosophila nervous system. Proc Natl Acad Sci U S A. 1982 Dec;79(24):7929–7933. doi: 10.1073/pnas.79.24.7929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Garcia-Bellido A., Merriam J. R. Clonal parameters of tergite development in Drosophila. Dev Biol. 1971 Oct;26(2):264–276. doi: 10.1016/0012-1606(71)90126-6. [DOI] [PubMed] [Google Scholar]
  11. Garcia-Bellido A., Robbins L. G. Viability of Female Germ-Line Cells Homozygous for Zygotic Lethals in DROSOPHILA MELANOGASTER. Genetics. 1983 Feb;103(2):235–247. doi: 10.1093/genetics/103.2.235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Harris W. A., Stark W. S., Walker J. A. Genetic dissection of the photoreceptor system in the compound eye of Drosophila melanogaster. J Physiol. 1976 Apr;256(2):415–439. doi: 10.1113/jphysiol.1976.sp011331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Harte P. J., Kankel D. R. Analysis of visual system development in Drosophila melanogaster: mutations at the Glued locus. Dev Biol. 1983 Sep;99(1):88–102. doi: 10.1016/0012-1606(83)90256-7. [DOI] [PubMed] [Google Scholar]
  14. Hinton C W. The Behavior of an Unstable Ring Chromosome of Drosophila Melanogaster. Genetics. 1955 Nov;40(6):951–961. doi: 10.1093/genetics/40.6.951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Judd B. H., Shen M. W., Kaufman T. C. The anatomy and function of a segment of the X chromosome of Drosophila melanogaster. Genetics. 1972 May;71(1):139–156. doi: 10.1093/genetics/71.1.139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kunes S., Steller H. Ablation of Drosophila photoreceptor cells by conditional expression of a toxin gene. Genes Dev. 1991 Jun;5(6):970–983. doi: 10.1101/gad.5.6.970. [DOI] [PubMed] [Google Scholar]
  17. Levis R., Hazelrigg T., Rubin G. M. Separable cis-acting control elements for expression of the white gene of Drosophila. EMBO J. 1985 Dec 16;4(13A):3489–3499. doi: 10.1002/j.1460-2075.1985.tb04108.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lipshitz H. D., Kankel D. R. Specificity of gene action during central nervous system development in Drosophila melanogaster: analysis of the lethal (1) optic ganglion reduced locus. Dev Biol. 1985 Mar;108(1):56–77. doi: 10.1016/0012-1606(85)90009-0. [DOI] [PubMed] [Google Scholar]
  19. Mlodzik M., Hiromi Y., Weber U., Goodman C. S., Rubin G. M. The Drosophila seven-up gene, a member of the steroid receptor gene superfamily, controls photoreceptor cell fates. Cell. 1990 Jan 26;60(2):211–224. doi: 10.1016/0092-8674(90)90737-y. [DOI] [PubMed] [Google Scholar]
  20. O'Kane C. J., Gehring W. J. Detection in situ of genomic regulatory elements in Drosophila. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9123–9127. doi: 10.1073/pnas.84.24.9123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Palazzolo M. J., Hyde D. R., VijayRaghavan K., Mecklenburg K., Benzer S., Meyerowitz E. Use of a new strategy to isolate and characterize 436 Drosophila cDNA clones corresponding to RNAs detected in adult heads but not in early embryos. Neuron. 1989 Oct;3(4):527–539. doi: 10.1016/0896-6273(89)90211-0. [DOI] [PubMed] [Google Scholar]
  22. Perrimon N., Engstrom L., Mahowald A. P. The effects of zygotic lethal mutations on female germ-line functions in Drosophila. Dev Biol. 1984 Oct;105(2):404–414. doi: 10.1016/0012-1606(84)90297-5. [DOI] [PubMed] [Google Scholar]
  23. Ready D. F. A multifaceted approach to neural development. Trends Neurosci. 1989 Mar;12(3):102–110. doi: 10.1016/0166-2236(89)90166-5. [DOI] [PubMed] [Google Scholar]
  24. Reardon J. T., Liljestrand-Golden C. A., Dusenbery R. L., Smith P. D. Molecular Analysis of Diepoxybutane-Induced Mutations at the rosy Locus of Drosophila melanogaster. Genetics. 1987 Feb;115(2):323–331. doi: 10.1093/genetics/115.2.323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ripoll P. Behavior of somatic cells homozygous for zygotic lethals in Drosophila melanogaster. Genetics. 1977 Jun;86(2 Pt 1):357–376. [PMC free article] [PubMed] [Google Scholar]
  26. Ripoll P., Garcia-Bellido A. Cell autonomous lethals in Drosophila melanogaster. Nat New Biol. 1973 Jan 3;241(105):15–16. doi: 10.1038/newbio241015a0. [DOI] [PubMed] [Google Scholar]
  27. Ripoll P., García-Bellido A. Viability of Homozygous Deficiencies in Somatic Cells of DROSOPHILA MELANOGASTER. Genetics. 1979 Mar;91(3):443–453. doi: 10.1093/genetics/91.3.443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rubin G. M. Development of the Drosophila retina: inductive events studied at single cell resolution. Cell. 1989 May 19;57(4):519–520. doi: 10.1016/0092-8674(89)90120-7. [DOI] [PubMed] [Google Scholar]
  29. Selleck S. B., Steller H. The influence of retinal innervation on neurogenesis in the first optic ganglion of Drosophila. Neuron. 1991 Jan;6(1):83–99. doi: 10.1016/0896-6273(91)90124-i. [DOI] [PubMed] [Google Scholar]
  30. Shearn A., Rice T., Garen A., Gehring W. Imaginal disc abnormalities in lethal mutants of Drosophila. Proc Natl Acad Sci U S A. 1971 Oct;68(10):2594–2598. doi: 10.1073/pnas.68.10.2594. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Simon M. A., Bowtell D. D., Dodson G. S., Laverty T. R., Rubin G. M. Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the sevenless protein tyrosine kinase. Cell. 1991 Nov 15;67(4):701–716. doi: 10.1016/0092-8674(91)90065-7. [DOI] [PubMed] [Google Scholar]
  32. Stern C. Somatic Crossing over and Segregation in Drosophila Melanogaster. Genetics. 1936 Nov;21(6):625–730. doi: 10.1093/genetics/21.6.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Stewart M., Murphy C., Fristrom J. W. The recovery and preliminary characterization of X chromosome mutants affecting imaginal discs of Drosophila melanogaster. Dev Biol. 1972 Jan;27(1):71–83. doi: 10.1016/0012-1606(72)90113-3. [DOI] [PubMed] [Google Scholar]
  34. Suzuki D. T. Temperature-sensitive mutations in Drosophila melanogaster. Science. 1970 Nov 13;170(3959):695–706. doi: 10.1126/science.170.3959.695. [DOI] [PubMed] [Google Scholar]
  35. Tomlinson A. Cellular interactions in the developing Drosophila eye. Development. 1988 Oct;104(2):183–193. doi: 10.1242/dev.104.2.183. [DOI] [PubMed] [Google Scholar]
  36. Wilson C., Pearson R. K., Bellen H. J., O'Kane C. J., Grossniklaus U., Gehring W. J. P-element-mediated enhancer detection: an efficient method for isolating and characterizing developmentally regulated genes in Drosophila. Genes Dev. 1989 Sep;3(9):1301–1313. doi: 10.1101/gad.3.9.1301. [DOI] [PubMed] [Google Scholar]
  37. Woods D. F., Bryant P. J. The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell. 1991 Aug 9;66(3):451–464. doi: 10.1016/0092-8674(81)90009-x. [DOI] [PubMed] [Google Scholar]
  38. Young M. W., Judd B. H. Nonessential Sequences, Genes, and the Polytene Chromosome Bands of DROSOPHILA MELANOGASTER. Genetics. 1978 Apr;88(4):723–742. doi: 10.1093/genetics/88.4.723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Zipursky S. L., Venkatesh T. R., Teplow D. B., Benzer S. Neuronal development in the Drosophila retina: monoclonal antibodies as molecular probes. Cell. 1984 Jan;36(1):15–26. doi: 10.1016/0092-8674(84)90069-2. [DOI] [PubMed] [Google Scholar]
  40. Zusman S., Patel-King R. S., Ffrench-Constant C., Hynes R. O. Requirements for integrins during Drosophila development. Development. 1990 Mar;108(3):391–402. doi: 10.1242/dev.108.3.391. [DOI] [PubMed] [Google Scholar]

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