Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1993 Oct 1;123(1):209–221. doi: 10.1083/jcb.123.1.209

Tissue polarity genes of Drosophila regulate the subcellular location for prehair initiation in pupal wing cells

PMCID: PMC2119819  PMID: 8408199

Abstract

The Drosophila wing is decorated with a regular array of distally pointing hairs. In the pupal wing, the hairs are formed from micro- villus like prehairs that contain large bundles of actin filaments. The distal orientation of the actin bundles reveals the proximal-distal polarity within the pupal wing epithelium. We have used F-actin staining to examine early stages of prehair development in both wild- type and mutant pupal wings. We have found a striking correlation between hair polarity and the subcellular location for assembly of the prehair. In a wild-type wing, all of the distally pointing hairs are derived from prehairs that are formed at the distal vertex of the hexagonally shaped pupal wing cells. Mutations in six tissue polarity genes result in abnormal hair polarity on the adult wing, and all also alter the subcellular location for prehair initiation. Based on their cellular phenotypes, we can place these six genes into three phenotypic groups. Double mutant analysis indicates that these phenotypic groups correspond to epistasis groups. This suggests that the tissue polarity genes function in or on a pathway that controls hair polarity by regulating the subcellular location for prehair formation.

Full Text

The Full Text of this article is available as a PDF (4.6 MB).

Selected References

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

  1. Adler P. N. The genetic control of tissue polarity in Drosophila. Bioessays. 1992 Nov;14(11):735–741. doi: 10.1002/bies.950141103. [DOI] [PubMed] [Google Scholar]
  2. Adler P. N., Vinson C., Park W. J., Conover S., Klein L. Molecular structure of frizzled, a Drosophila tissue polarity gene. Genetics. 1990 Oct;126(2):401–416. doi: 10.1093/genetics/126.2.401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bopp D., Bell L. R., Cline T. W., Schedl P. Developmental distribution of female-specific Sex-lethal proteins in Drosophila melanogaster. Genes Dev. 1991 Mar;5(3):403–415. doi: 10.1101/gad.5.3.403. [DOI] [PubMed] [Google Scholar]
  4. Garcia-Bellido A., Merriam J. R. Parameters of the wing imaginal disc development of Drosophila melanogaster. Dev Biol. 1971 Jan;24(1):61–87. doi: 10.1016/0012-1606(71)90047-9. [DOI] [PubMed] [Google Scholar]
  5. Gubb D., García-Bellido A. A genetic analysis of the determination of cuticular polarity during development in Drosophila melanogaster. J Embryol Exp Morphol. 1982 Apr;68:37–57. [PubMed] [Google Scholar]
  6. Hartwig J. H., Kwiatkowski D. J. Actin-binding proteins. Curr Opin Cell Biol. 1991 Feb;3(1):87–97. doi: 10.1016/0955-0674(91)90170-4. [DOI] [PubMed] [Google Scholar]
  7. Johnson R. L., Gundersen R., Lilly P., Pitt G. S., Pupillo M., Sun T. J., Vaughan R. A., Devreotes P. N. G-protein-linked signal transduction systems control development in Dictyostelium. Development. 1989;107 (Suppl):75–80. doi: 10.1242/dev.107.Supplement.75. [DOI] [PubMed] [Google Scholar]
  8. Lawrence P. A. Development and determination of hairs and bristles in the milkweed bug, Oncopeltus fasciatus (Lygaeidae, Hemiptera). J Cell Sci. 1966 Dec;1(4):475–498. doi: 10.1242/jcs.1.4.475. [DOI] [PubMed] [Google Scholar]
  9. McMahon A. P., Moon R. T. int-1--a proto-oncogene involved in cell signalling. Development. 1989;107 (Suppl):161–167. doi: 10.1242/dev.107.Supplement.161. [DOI] [PubMed] [Google Scholar]
  10. Mitchell H. K., Roach J., Petersen N. S. The morphogenesis of cell hairs on Drosophila wings. Dev Biol. 1983 Feb;95(2):387–398. doi: 10.1016/0012-1606(83)90040-4. [DOI] [PubMed] [Google Scholar]
  11. Perrimon N., Mahowald A. P. Multiple functions of segment polarity genes in Drosophila. Dev Biol. 1987 Feb;119(2):587–600. doi: 10.1016/0012-1606(87)90061-3. [DOI] [PubMed] [Google Scholar]
  12. Ready D. F., Hanson T. E., Benzer S. Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol. 1976 Oct 15;53(2):217–240. doi: 10.1016/0012-1606(76)90225-6. [DOI] [PubMed] [Google Scholar]
  13. Schubiger M., Palka J. Changing spatial patterns of DNA replication in the developing wing of Drosophila. Dev Biol. 1987 Sep;123(1):145–153. doi: 10.1016/0012-1606(87)90436-2. [DOI] [PubMed] [Google Scholar]
  14. Tilney L. G., Hatano S., Ishikawa H., Mooseker M. S. The polymerization of actin: its role in the generation of the acrosomal process of certain echinoderm sperm. J Cell Biol. 1973 Oct;59(1):109–126. doi: 10.1083/jcb.59.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Tucker J. B. Cytoskeletal coordination and intercellular signalling during metazoan embryogenesis. J Embryol Exp Morphol. 1981 Oct;65:1–25. [PubMed] [Google Scholar]
  16. Vinson C. R., Adler P. N. Directional non-cell autonomy and the transmission of polarity information by the frizzled gene of Drosophila. Nature. 1987 Oct 8;329(6139):549–551. doi: 10.1038/329549a0. [DOI] [PubMed] [Google Scholar]
  17. Vinson C. R., Conover S., Adler P. N. A Drosophila tissue polarity locus encodes a protein containing seven potential transmembrane domains. Nature. 1989 Mar 16;338(6212):263–264. doi: 10.1038/338263a0. [DOI] [PubMed] [Google Scholar]
  18. Wulf E., Deboben A., Bautz F. A., Faulstich H., Wieland T. Fluorescent phallotoxin, a tool for the visualization of cellular actin. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4498–4502. doi: 10.1073/pnas.76.9.4498. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES