Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1991 Mar;127(3):525–533. doi: 10.1093/genetics/127.3.525

Requirement for Cell-Proliferation Control Genes in Drosophila Oogenesis

J Szabad 1, V A Jursnich 1, P J Bryant 1
PMCID: PMC1204380  PMID: 2016052

Abstract

Genes that are required for cell proliferation control in Drosophila imaginal discs were tested for function in the female germ-line and follicle cells. Chimeras and mosaics were produced in which developing oocytes and nurse cells were mutant at one of five imaginal disc overgrowth loci (fat, lgd, lgl, c43 and dco) while the enveloping follicle cells were normal. The chimeras were produced by transplantation of pole cells and the mosaics were produced by X-ray-induced mitotic recombination using the dominant female-sterile technique. The results show that each of the genes tested plays an essential role in the development or function of the female germ line. The fat, lgl and c43 homozygous germ-line clones fail to produce eggs, indicating a germ-line requirement for the corresponding genes. Perdurance of the fat(+) gene product in mitotic recombination clones allows the formation of a few infertile eggs from fat homozygous germ-line cells. The lgd homozygous germ-line clones give rise to a few eggs with abnormal chorionic appendages, a defect thought to result from defective cell communication between the mutant germ-line and the nonmutant follicle cells. One allele of dco (dco(le88)) prevents egg development when homozygous in the germ line, whereas the dco(18) allele has no effect on germ-line development. Fs(2)Ugra, a recently described follicle cell-dependent dominant female-sterile mutation, allowed the analysis of egg primordia in which fat, lgd or lgl homozygous mutant follicle cells surrounded normal oocytes. The results show that the fat and lgd genes are not required for follicle cell functions, while absence of lgl function in follicles prevents egg development. Whereas the products of these genes are necessary for the cell interactions that control cell proliferation in imaginal discs, they may be needed for cell interactions that control other aspects of development in the ovary.

Full Text

The Full Text of this article is available as a PDF (2.8 MB).

Selected References

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

  1. Bryant P. J., Fraser S. E. Wound healing, cell communication, and DNA synthesis during imaginal disc regeneration in Drosophila. Dev Biol. 1988 May;127(1):197–208. doi: 10.1016/0012-1606(88)90201-1. [DOI] [PubMed] [Google Scholar]
  2. Bryant P. J., Huettner B., Held L. I., Jr, Ryerse J., Szidonya J. Mutations at the fat locus interfere with cell proliferation control and epithelial morphogenesis in Drosophila. Dev Biol. 1988 Oct;129(2):541–554. doi: 10.1016/0012-1606(88)90399-5. [DOI] [PubMed] [Google Scholar]
  3. Bryant P. J., Levinson P. Intrinsic growth control in the imaginal primordia of Drosophila, and the autonomous action of a lethal mutation causing overgrowth. Dev Biol. 1985 Feb;107(2):355–363. doi: 10.1016/0012-1606(85)90317-3. [DOI] [PubMed] [Google Scholar]
  4. Bryant P. J., Schubiger G. Giant and duplicated imaginal discs in a new lethal mutant of Drosophila melanogaster. Dev Biol. 1971 Feb;24(2):233–263. doi: 10.1016/0012-1606(71)90097-2. [DOI] [PubMed] [Google Scholar]
  5. Jursnich V. A., Fraser S. E., Held L. I., Jr, Ryerse J., Bryant P. J. Defective gap-junctional communication associated with imaginal disc overgrowth and degeneration caused by mutations of the dco gene in Drosophila. Dev Biol. 1990 Aug;140(2):413–429. doi: 10.1016/0012-1606(90)90090-6. [DOI] [PubMed] [Google Scholar]
  6. Kastenbaum M. A., Bowman K. O. Tables for determining the statistical significance of mutation frequencies. Mutat Res. 1970 May;9(5):527–549. doi: 10.1016/0027-5107(70)90038-2. [DOI] [PubMed] [Google Scholar]
  7. King R. C., Storto P. D. The role of the otu gene in Drosophila oogenesis. Bioessays. 1988 Jan;8(1):18–24. doi: 10.1002/bies.950080106. [DOI] [PubMed] [Google Scholar]
  8. Klämbt C., Müller S., Lützelschwab R., Rossa R., Totzke F., Schmidt O. The Drosophila melanogaster l(2)gl gene encodes a protein homologous to the cadherin cell-adhesion molecule family. Dev Biol. 1989 Jun;133(2):425–436. doi: 10.1016/0012-1606(89)90046-8. [DOI] [PubMed] [Google Scholar]
  9. Komitopoulou K., Gans M., Margaritis L. H., Kafatos F. C., Masson M. Isolation and Characterization of Sex-Linked Female-Sterile Mutants in DROSOPHILA MELANOGASTER with Special Attention to Eggshell Mutants. Genetics. 1983 Dec;105(4):897–920. doi: 10.1093/genetics/105.4.897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Konrad K. D., Engstrom L., Perrimon N., Mahowald A. P. Genetic analysis of oogenesis and the role of maternal gene expression in early development. Dev Biol (N Y 1985) 1985;1:577–617. doi: 10.1007/978-1-4615-6814-8_13. [DOI] [PubMed] [Google Scholar]
  11. Lehmann R., Nüsslein-Volhard C. Abdominal segmentation, pole cell formation, and embryonic polarity require the localized activity of oskar, a maternal gene in Drosophila. Cell. 1986 Oct 10;47(1):141–152. doi: 10.1016/0092-8674(86)90375-2. [DOI] [PubMed] [Google Scholar]
  12. Lützelschwab R., Klämbt C., Rossa R., Schmidt O. A protein product of the Drosophila recessive tumor gene, l (2) giant gl, potentially has cell adhesion properties. EMBO J. 1987 Jun;6(6):1791–1797. doi: 10.1002/j.1460-2075.1987.tb02432.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Martin P., Martin A., Shearn A. Studies of l(3)c43hs1 a polyphasic, temperature-sensitive mutant of Drosophila melanogaster with a variety of imaginal disc defects. Dev Biol. 1977 Feb;55(2):213–232. doi: 10.1016/0012-1606(77)90168-3. [DOI] [PubMed] [Google Scholar]
  14. Mayer U., Nüsslein-Volhard C. A group of genes required for pattern formation in the ventral ectoderm of the Drosophila embryo. Genes Dev. 1988 Nov;2(11):1496–1511. doi: 10.1101/gad.2.11.1496. [DOI] [PubMed] [Google Scholar]
  15. Perrimon N., Engstrom L., Mahowald A. P. Zygotic lethals with specific maternal effect phenotypes in Drosophila melanogaster. I. Loci on the X chromosome. Genetics. 1989 Feb;121(2):333–352. doi: 10.1093/genetics/121.2.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Perrimon N., Gans M. Clonal analysis of the tissue specificity of recessive female-sterile mutations of Drosophila melanogaster using a dominant female-sterile mutation Fs(1)K1237. Dev Biol. 1983 Dec;100(2):365–373. doi: 10.1016/0012-1606(83)90231-2. [DOI] [PubMed] [Google Scholar]
  17. Perrimon N., Mahowald A. P. l(1)hopscotch, A larval-pupal zygotic lethal with a specific maternal effect on segmentation in Drosophila. Dev Biol. 1986 Nov;118(1):28–41. doi: 10.1016/0012-1606(86)90070-9. [DOI] [PubMed] [Google Scholar]
  18. Perrimon N. The maternal effect of lethal(1)discs-large-1: a recessive oncogene of Drosophila melanogaster. Dev Biol. 1988 Jun;127(2):392–407. doi: 10.1016/0012-1606(88)90326-0. [DOI] [PubMed] [Google Scholar]
  19. Ryerse J. S., Nagel B. A. Gap junction distribution in the Drosophila wing disc mutants vg, l(2)gd, l(3)c43hs1, and l(2)gl4. Dev Biol. 1984 Oct;105(2):396–403. doi: 10.1016/0012-1606(84)90296-3. [DOI] [PubMed] [Google Scholar]
  20. Schüpbach T. Germ line and soma cooperate during oogenesis to establish the dorsoventral pattern of egg shell and embryo in Drosophila melanogaster. Cell. 1987 Jun 5;49(5):699–707. doi: 10.1016/0092-8674(87)90546-0. [DOI] [PubMed] [Google Scholar]
  21. Szabad J., Erdélyi M., Hoffmann G., Szidonya J., Wright T. R. Isolation and characterization of dominant female sterile mutations of Drosophila melanogaster. II. Mutations on the second chromosome. Genetics. 1989 Aug;122(4):823–835. doi: 10.1093/genetics/122.4.823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Szabad J., Erdélyi M., Szidonya J. Characterization of Fs(2)1, a germ-line dependent dominant female sterile mutation of Drosophila. Acta Biol Hung. 1987;38(2):257–266. [PubMed] [Google Scholar]
  23. Taubert H, Szabad J. Genetic control of cell proliferation in female germ line cells of Drosophila: mosaic analysis of five discless mutations. Mol Gen Genet. 1987 Oct;209(3):545–551. doi: 10.1007/BF00331161. [DOI] [PubMed] [Google Scholar]
  24. Wieschaus E. A combined genetic and mosaic approach to the study of oogenesis in Drosophila. Basic Life Sci. 1980;16:85–94. doi: 10.1007/978-1-4684-7968-3_7. [DOI] [PubMed] [Google Scholar]
  25. Wieschaus E., Szabad J. The development and function of the female germ line in Drosophila melanogaster: a cell lineage study. Dev Biol. 1979 Jan;68(1):29–46. doi: 10.1016/0012-1606(79)90241-0. [DOI] [PubMed] [Google Scholar]
  26. Woods D. F., Bryant P. J. Molecular cloning of the lethal(1)discs large-1 oncogene of Drosophila. Dev Biol. 1989 Jul;134(1):222–235. doi: 10.1016/0012-1606(89)90092-4. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES