Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1999 Feb;151(2):739–748. doi: 10.1093/genetics/151.2.739

Mosaic analysis in the drosophila ovary reveals a common hedgehog-inducible precursor stage for stalk and polar cells.

M Tworoger 1, M K Larkin 1, Z Bryant 1, H Ruohola-Baker 1
PMCID: PMC1460513  PMID: 9927465

Abstract

The fates of two small subgroups of the ovarian follicle cells appear to be linked: mutations in Notch, Delta, fs(1)Yb, or hedgehog cause simultaneous defects in the specification of stalk cells and polar cells. Both of these subgroups are determined in the germarium, and both cease division early in oogenesis. To test the possibility that these subgroups are related by lineage, we generated dominantly marked mitotic clones in ovaries. Small, restricted clones in stalk cells and polar cells were found adjacent to each other at a frequency much too high to be explained by independent induction. We therefore propose a model in which stalk cells and polar cells are derived from a precursor population that is distinct from the precursors for other follicle cells. We support and extend this model by characterization of mutants that affect stalk and polar cell formation. We find that ectopic expression of Hedgehog can induce both polar and stalk cell fate, presumably by acting on the precursor stage. In contrast, we find that stall affects neither the induction of the precursors nor the decision between the stalk cell and polar cell fate but, rather, some later differentiation step of stalk cells. In addition, we show that ectopic polar and stalk cells disturb the anterior-posterior polarity of the underlying oocyte.

Full Text

The Full Text of this article is available as a PDF (464.6 KB).

Selected References

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

  1. Anderson K. One signal, two body axes. Science. 1995 Jul 28;269(5223):489–490. doi: 10.1126/science.7542799. [DOI] [PubMed] [Google Scholar]
  2. Artavanis-Tsakonas S., Matsuno K., Fortini M. E. Notch signaling. Science. 1995 Apr 14;268(5208):225–232. doi: 10.1126/science.7716513. [DOI] [PubMed] [Google Scholar]
  3. BECKER H. J. Uber Rontgenmosaikflecken und Defektmutationen am Auge von Drosophila und die Entwicklungsphysiologie des Auges. Z Indukt Abstamm Vererbungsl. 1957;88(3):333–373. [PubMed] [Google Scholar]
  4. Bender L. B., Kooh P. J., Muskavitch M. A. Complex function and expression of Delta during Drosophila oogenesis. Genetics. 1993 Apr;133(4):967–978. doi: 10.1093/genetics/133.4.967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bobola N., Jansen R. P., Shin T. H., Nasmyth K. Asymmetric accumulation of Ash1p in postanaphase nuclei depends on a myosin and restricts yeast mating-type switching to mother cells. Cell. 1996 Mar 8;84(5):699–709. doi: 10.1016/s0092-8674(00)81048-x. [DOI] [PubMed] [Google Scholar]
  6. Brower D. L., Smith R. J., Wilcox M. Differentiation within the gonads of Drosophila revealed by immunofluorescence. J Embryol Exp Morphol. 1981 Jun;63:233–242. [PubMed] [Google Scholar]
  7. Cummings C. A., Cronmiller C. The daughterless gene functions together with Notch and Delta in the control of ovarian follicle development in Drosophila. Development. 1994 Feb;120(2):381–394. doi: 10.1242/dev.120.2.381. [DOI] [PubMed] [Google Scholar]
  8. Forbes A. J., Lin H., Ingham P. W., Spradling A. C. hedgehog is required for the proliferation and specification of ovarian somatic cells prior to egg chamber formation in Drosophila. Development. 1996 Apr;122(4):1125–1135. doi: 10.1242/dev.122.4.1125. [DOI] [PubMed] [Google Scholar]
  9. Gho M., Schweisguth F. Frizzled signalling controls orientation of asymmetric sense organ precursor cell divisions in Drosophila. Nature. 1998 May 14;393(6681):178–181. doi: 10.1038/30265. [DOI] [PubMed] [Google Scholar]
  10. Golic K. G. Site-specific recombination between homologous chromosomes in Drosophila. Science. 1991 May 17;252(5008):958–961. doi: 10.1126/science.2035025. [DOI] [PubMed] [Google Scholar]
  11. Grammont M., Dastugue B., Couderc J. L. The Drosophila toucan (toc) gene is required in germline cells for the somatic cell patterning during oogenesis. Development. 1997 Dec;124(24):4917–4926. doi: 10.1242/dev.124.24.4917. [DOI] [PubMed] [Google Scholar]
  12. Harrison D. A., Perrimon N. Simple and efficient generation of marked clones in Drosophila. Curr Biol. 1993 Jul 1;3(7):424–433. doi: 10.1016/0960-9822(93)90349-s. [DOI] [PubMed] [Google Scholar]
  13. Jan Y. N., Jan L. Y. Asymmetric cell division. Nature. 1998 Apr 23;392(6678):775–778. doi: 10.1038/33854. [DOI] [PubMed] [Google Scholar]
  14. Johnson E., Wayne S., Nagoshi R. fs (1) Yb is required for ovary follicle cell differentiation in Drosophila melanogaster and has genetic interactions with the Notch group of neurogenic genes. Genetics. 1995 May;140(1):207–217. doi: 10.1093/genetics/140.1.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Johnson R. L., Tabin C. The long and short of hedgehog signaling. Cell. 1995 May 5;81(3):313–316. doi: 10.1016/0092-8674(95)90381-x. [DOI] [PubMed] [Google Scholar]
  16. Larkin M. K., Holder K., Yost C., Giniger E., Ruohola-Baker H. Expression of constitutively active Notch arrests follicle cells at a precursor stage during Drosophila oogenesis and disrupts the anterior-posterior axis of the oocyte. Development. 1996 Nov;122(11):3639–3650. doi: 10.1242/dev.122.11.3639. [DOI] [PubMed] [Google Scholar]
  17. Margolis J., Spradling A. Identification and behavior of epithelial stem cells in the Drosophila ovary. Development. 1995 Nov;121(11):3797–3807. doi: 10.1242/dev.121.11.3797. [DOI] [PubMed] [Google Scholar]
  18. Ray R. P., Schüpbach T. Intercellular signaling and the polarization of body axes during Drosophila oogenesis. Genes Dev. 1996 Jul 15;10(14):1711–1723. doi: 10.1101/gad.10.14.1711. [DOI] [PubMed] [Google Scholar]
  19. Rongo C., Lehmann R. Regulated synthesis, transport and assembly of the Drosophila germ plasm. Trends Genet. 1996 Mar;12(3):102–109. doi: 10.1016/0168-9525(96)81421-1. [DOI] [PubMed] [Google Scholar]
  20. Ruohola H., Bremer K. A., Baker D., Swedlow J. R., Jan L. Y., Jan Y. N. Role of neurogenic genes in establishment of follicle cell fate and oocyte polarity during oogenesis in Drosophila. Cell. 1991 Aug 9;66(3):433–449. doi: 10.1016/0092-8674(81)90008-8. [DOI] [PubMed] [Google Scholar]
  21. Sil A., Herskowitz I. Identification of asymmetrically localized determinant, Ash1p, required for lineage-specific transcription of the yeast HO gene. Cell. 1996 Mar 8;84(5):711–722. doi: 10.1016/s0092-8674(00)81049-1. [DOI] [PubMed] [Google Scholar]
  22. Xu T., Caron L. A., Fehon R. G., Artavanis-Tsakonas S. The involvement of the Notch locus in Drosophila oogenesis. Development. 1992 Aug;115(4):913–922. doi: 10.1242/dev.115.4.913. [DOI] [PubMed] [Google Scholar]
  23. Zaffran S., Astier M., Gratecos D., Sémériva M. The held out wings (how) Drosophila gene encodes a putative RNA-binding protein involved in the control of muscular and cardiac activity. Development. 1997 May;124(10):2087–2098. doi: 10.1242/dev.124.10.2087. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES