Fs(1)yb Is Required for Ovary Follicle Cell Differentiation in Drosophila Melanogaster and Has Genetic Interactions with the Notch Group of Neurogenic Genes (original) (raw)

Abstract

Phenotypic and genetic analyses demonstrate that fs(1)Yb activity is required in the soma for the development of a subset of ovarian follicle cells and to support later stages of egg maturation. Mutations in fs(1)Yb cause a range of ovarian phenotypes, from the improper segregation of egg chambers to abnormal dorsal appendage formation. The mutant phenotypes associated with fs(1)Yb are very similar to the ovarian aberrations produced by temperature-sensitive alleles of Notch and Delta. Possible functional or regulatory interactions between fs(1)Yb and Notch are suggested by genetic studies. A duplication of the Notch locus partially suppresses the female-sterility caused by fs(1)Yb mutations, while reducing Notch dosage makes the fs(1)Yb mutant phenotype more severe. In addition, fs(1)Yb alleles also interact with genes that are known to act with or regulate Notch activity, including Delta, daughterless, and mastermind. However, differences between the mutant ovarian phenotype of fs(1)Yb and that of Notch or Delta indicate that the genes do not have completely overlapping functions in the ovary. We propose that fs(1)Yb acts as an ovary-specific factor that determines follicle cell fate.

Full Text

The Full Text of this article is available as a PDF (4.7 MB).

Selected References

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

  1. Artavanis-Tsakonas S., Simpson P. Choosing a cell fate: a view from the Notch locus. Trends Genet. 1991 Nov-Dec;7(11-12):403–408. doi: 10.1016/0168-9525(91)90264-q. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Clark I., Giniger E., Ruohola-Baker H., Jan L. Y., Jan Y. N. Transient posterior localization of a kinesin fusion protein reflects anteroposterior polarity of the Drosophila oocyte. Curr Biol. 1994 Apr 1;4(4):289–300. doi: 10.1016/s0960-9822(00)00068-3. [DOI] [PubMed] [Google Scholar]
  4. Corbin V., Michelson A. M., Abmayr S. M., Neel V., Alcamo E., Maniatis T., Young M. W. A role for the Drosophila neurogenic genes in mesoderm differentiation. Cell. 1991 Oct 18;67(2):311–323. doi: 10.1016/0092-8674(91)90183-y. [DOI] [PubMed] [Google Scholar]
  5. Couso J. P., Bishop S. A., Martinez Arias A. The wingless signalling pathway and the patterning of the wing margin in Drosophila. Development. 1994 Mar;120(3):621–636. doi: 10.1242/dev.120.3.621. [DOI] [PubMed] [Google Scholar]
  6. Couso J. P., Martinez Arias A. Notch is required for wingless signaling in the epidermis of Drosophila. Cell. 1994 Oct 21;79(2):259–272. doi: 10.1016/0092-8674(94)90195-3. [DOI] [PubMed] [Google Scholar]
  7. Fehon R. G., Kooh P. J., Rebay I., Regan C. L., Xu T., Muskavitch M. A., Artavanis-Tsakonas S. Molecular interactions between the protein products of the neurogenic loci Notch and Delta, two EGF-homologous genes in Drosophila. Cell. 1990 May 4;61(3):523–534. doi: 10.1016/0092-8674(90)90534-l. [DOI] [PubMed] [Google Scholar]
  8. Fortini M. E., Artavanis-Tsakonas S. Notch: neurogenesis is only part of the picture. Cell. 1993 Dec 31;75(7):1245–1247. doi: 10.1016/0092-8674(93)90611-s. [DOI] [PubMed] [Google Scholar]
  9. Goode S., Wright D., Mahowald A. P. The neurogenic locus brainiac cooperates with the Drosophila EGF receptor to establish the ovarian follicle and to determine its dorsal-ventral polarity. Development. 1992 Sep;116(1):177–192. doi: 10.1242/dev.116.1.177. [DOI] [PubMed] [Google Scholar]
  10. Grossniklaus U., Bellen H. J., Wilson C., Gehring W. J. P-element-mediated enhancer detection applied to the study of oogenesis in Drosophila. Development. 1989 Oct;107(2):189–200. doi: 10.1242/dev.107.2.189. [DOI] [PubMed] [Google Scholar]
  11. Heitzler P., Simpson P. The choice of cell fate in the epidermis of Drosophila. Cell. 1991 Mar 22;64(6):1083–1092. doi: 10.1016/0092-8674(91)90263-x. [DOI] [PubMed] [Google Scholar]
  12. Jan Y. N., Jan L. Y. Genes required for specifying cell fates in Drosophila embryonic sensory nervous system. Trends Neurosci. 1990 Dec;13(12):493–498. doi: 10.1016/0166-2236(90)90083-m. [DOI] [PubMed] [Google Scholar]
  13. Kidd S., Kelley M. R., Young M. W. Sequence of the notch locus of Drosophila melanogaster: relationship of the encoded protein to mammalian clotting and growth factors. Mol Cell Biol. 1986 Sep;6(9):3094–3108. doi: 10.1128/mcb.6.9.3094. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kopczynski C. C., Alton A. K., Fechtel K., Kooh P. J., Muskavitch M. A. Delta, a Drosophila neurogenic gene, is transcriptionally complex and encodes a protein related to blood coagulation factors and epidermal growth factor of vertebrates. Genes Dev. 1988 Dec;2(12B):1723–1735. doi: 10.1101/gad.2.12b.1723. [DOI] [PubMed] [Google Scholar]
  15. Lin H., Wolfner M. F. Cloning and analysis of fs(1) Ya, a maternal effect gene required for the initiation of Drosophila embryogenesis. Mol Gen Genet. 1989 Jan;215(2):257–265. doi: 10.1007/BF00339726. [DOI] [PubMed] [Google Scholar]
  16. Montell D. J., Rorth P., Spradling A. C. slow border cells, a locus required for a developmentally regulated cell migration during oogenesis, encodes Drosophila C/EBP. Cell. 1992 Oct 2;71(1):51–62. doi: 10.1016/0092-8674(92)90265-e. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Ramos R. G., Grimwade B. G., Wharton K. A., Scottgale T. N., Artavanis-Tsakonas S. Physical and functional definition of the Drosophila Notch locus by P element transformation. Genetics. 1989 Oct;123(2):337–348. doi: 10.1093/genetics/123.2.337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rebay I., Fleming R. J., Fehon R. G., Cherbas L., Cherbas P., Artavanis-Tsakonas S. Specific EGF repeats of Notch mediate interactions with Delta and Serrate: implications for Notch as a multifunctional receptor. Cell. 1991 Nov 15;67(4):687–699. doi: 10.1016/0092-8674(91)90064-6. [DOI] [PubMed] [Google Scholar]
  20. Ruohola-Baker H., Jan L. Y., Jan Y. N. The role of gene cassettes in axis formation during Drosophila oogenesis. Trends Genet. 1994 Mar;10(3):89–94. doi: 10.1016/0168-9525(94)90231-3. [DOI] [PubMed] [Google Scholar]
  21. Wharton K. A., Johansen K. M., Xu T., Artavanis-Tsakonas S. Nucleotide sequence from the neurogenic locus notch implies a gene product that shares homology with proteins containing EGF-like repeats. Cell. 1985 Dec;43(3 Pt 2):567–581. doi: 10.1016/0092-8674(85)90229-6. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. 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]
  24. de Celis J. F., Garcia-Bellido A. Modifications of the notch function by Abruptex mutations in Drosophila melanogaster. Genetics. 1994 Jan;136(1):183–194. doi: 10.1093/genetics/136.1.183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. de-la-Concha A., Dietrich U., Weigel D., Campos-Ortega J. A. Functional interactions of neurogenic genes of Drosophila melanogaster. Genetics. 1988 Mar;118(3):499–508. doi: 10.1093/genetics/118.3.499. [DOI] [PMC free article] [PubMed] [Google Scholar]