Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1994 Jul 5;91(14):6324–6328. doi: 10.1073/pnas.91.14.6324

Functional redundancy: the respective roles of the two sloppy paired genes in Drosophila segmentation.

K M Cadigan 1, U Grossniklaus 1, W J Gehring 1
PMCID: PMC44194  PMID: 8022780

Abstract

The sloppy paired (slp) locus consists of two genes, slp1 and slp2, both of which encode proteins containing a forkhead domain (a DNA-binding motif). Previous work has shown that a severe segmentation phenotype is obtained only when both slp genes are deleted. Here we examine the functional redundancy of the locus in more detail. The phenotypes of embryos containing various combinations of functional slp genes suggest that for early slp function, until gastrulation, only slp1 is required. At later times, there is still a greater requirement for slp1, but in many respects the two slp genes are completely redundant. Both slp genes produce similar phenotypes when ubiquitously expressed via a heat shock promoter. We propose that the slp proteins are biochemically equivalent and that the greater requirement for slp1 in some functions can be explained in large part by its earlier expression.

Full text

PDF
6327

Images in this article

6325Image
on p.6325
6325Image
on p.6325
6326Image
on p.6326
6326Image
on p.6326
6327Image
on p.6327

Selected References

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

  1. Baker N. E. Embryonic and imaginal requirements for wingless, a segment-polarity gene in Drosophila. Dev Biol. 1988 Jan;125(1):96–108. doi: 10.1016/0012-1606(88)90062-0. [DOI] [PubMed] [Google Scholar]
  2. Basson M. E., Thorsness M., Rine J. Saccharomyces cerevisiae contains two functional genes encoding 3-hydroxy-3-methylglutaryl-coenzyme A reductase. Proc Natl Acad Sci U S A. 1986 Aug;83(15):5563–5567. doi: 10.1073/pnas.83.15.5563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baumgartner S., Bopp D., Burri M., Noll M. Structure of two genes at the gooseberry locus related to the paired gene and their spatial expression during Drosophila embryogenesis. Genes Dev. 1987 Dec;1(10):1247–1267. doi: 10.1101/gad.1.10.1247. [DOI] [PubMed] [Google Scholar]
  4. Bejsovec A., Martinez Arias A. Roles of wingless in patterning the larval epidermis of Drosophila. Development. 1991 Oct;113(2):471–485. doi: 10.1242/dev.113.2.471. [DOI] [PubMed] [Google Scholar]
  5. Bellen H. J., O'Kane C. J., Wilson C., Grossniklaus U., Pearson R. K., Gehring W. J. P-element-mediated enhancer detection: a versatile method to study development in Drosophila. Genes Dev. 1989 Sep;3(9):1288–1300. doi: 10.1101/gad.3.9.1288. [DOI] [PubMed] [Google Scholar]
  6. Cadigan K. M., Grossniklaus U., Gehring W. J. Localized expression of sloppy paired protein maintains the polarity of Drosophila parasegments. Genes Dev. 1994 Apr 15;8(8):899–913. doi: 10.1101/gad.8.8.899. [DOI] [PubMed] [Google Scholar]
  7. Clark K. L., Halay E. D., Lai E., Burley S. K. Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5. Nature. 1993 Jul 29;364(6436):412–420. doi: 10.1038/364412a0. [DOI] [PubMed] [Google Scholar]
  8. Coleman K. G., Poole S. J., Weir M. P., Soeller W. C., Kornberg T. The invected gene of Drosophila: sequence analysis and expression studies reveal a close kinship to the engrailed gene. Genes Dev. 1987 Mar;1(1):19–28. doi: 10.1101/gad.1.1.19. [DOI] [PubMed] [Google Scholar]
  9. Coulter D. E., Wieschaus E. Gene activities and segmental patterning in Drosophila: analysis of odd-skipped and pair-rule double mutants. Genes Dev. 1988 Dec;2(12B):1812–1823. doi: 10.1101/gad.2.12b.1812. [DOI] [PubMed] [Google Scholar]
  10. Côté S., Preiss A., Haller J., Schuh R., Kienlin A., Seifert E., Jäckle H. The gooseberry-zipper region of Drosophila: five genes encode different spatially restricted transcripts in the embryo. EMBO J. 1987 Sep;6(9):2793–2801. doi: 10.1002/j.1460-2075.1987.tb02575.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fjose A., McGinnis W. J., Gehring W. J. Isolation of a homoeo box-containing gene from the engrailed region of Drosophila and the spatial distribution of its transcripts. Nature. 1985 Jan 24;313(6000):284–289. doi: 10.1038/313284a0. [DOI] [PubMed] [Google Scholar]
  12. Frasch M., Hoey T., Rushlow C., Doyle H., Levine M. Characterization and localization of the even-skipped protein of Drosophila. EMBO J. 1987 Mar;6(3):749–759. doi: 10.1002/j.1460-2075.1987.tb04817.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Goldstein L. S. Functional redundancy in mitotic force generation. J Cell Biol. 1993 Jan;120(1):1–3. doi: 10.1083/jcb.120.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Grossniklaus U., Pearson R. K., Gehring W. J. The Drosophila sloppy paired locus encodes two proteins involved in segmentation that show homology to mammalian transcription factors. Genes Dev. 1992 Jun;6(6):1030–1051. doi: 10.1101/gad.6.6.1030. [DOI] [PubMed] [Google Scholar]
  15. Gutjahr T., Patel N. H., Li X., Goodman C. S., Noll M. Analysis of the gooseberry locus in Drosophila embryos: gooseberry determines the cuticular pattern and activates gooseberry neuro. Development. 1993 May;118(1):21–31. doi: 10.1242/dev.118.1.21. [DOI] [PubMed] [Google Scholar]
  16. Heemskerk J., DiNardo S., Kostriken R., O'Farrell P. H. Multiple modes of engrailed regulation in the progression towards cell fate determination. Nature. 1991 Aug 1;352(6334):404–410. doi: 10.1038/352404a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Higashijima S., Michiue T., Emori Y., Saigo K. Subtype determination of Drosophila embryonic external sensory organs by redundant homeo box genes BarH1 and BarH2. Genes Dev. 1992 Jun;6(6):1005–1018. doi: 10.1101/gad.6.6.1005. [DOI] [PubMed] [Google Scholar]
  18. Karess R. E., Rubin G. M. Analysis of P transposable element functions in Drosophila. Cell. 1984 Aug;38(1):135–146. doi: 10.1016/0092-8674(84)90534-8. [DOI] [PubMed] [Google Scholar]
  19. Kataoka T., Powers S., McGill C., Fasano O., Strathern J., Broach J., Wigler M. Genetic analysis of yeast RAS1 and RAS2 genes. Cell. 1984 Jun;37(2):437–445. doi: 10.1016/0092-8674(84)90374-x. [DOI] [PubMed] [Google Scholar]
  20. Kornberg T. Engrailed: a gene controlling compartment and segment formation in Drosophila. Proc Natl Acad Sci U S A. 1981 Feb;78(2):1095–1099. doi: 10.1073/pnas.78.2.1095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Krause H. M., Klemenz R., Gehring W. J. Expression, modification, and localization of the fushi tarazu protein in Drosophila embryos. Genes Dev. 1988 Aug;2(8):1021–1036. doi: 10.1101/gad.2.8.1021. [DOI] [PubMed] [Google Scholar]
  22. Macdonald P. M., Ingham P., Struhl G. Isolation, structure, and expression of even-skipped: a second pair-rule gene of Drosophila containing a homeo box. Cell. 1986 Dec 5;47(5):721–734. doi: 10.1016/0092-8674(86)90515-5. [DOI] [PubMed] [Google Scholar]
  23. Mohler J. Requirements for hedgehog, a segmental polarity gene, in patterning larval and adult cuticle of Drosophila. Genetics. 1988 Dec;120(4):1061–1072. doi: 10.1093/genetics/120.4.1061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Noordermeer J., Johnston P., Rijsewijk F., Nusse R., Lawrence P. A. The consequences of ubiquitous expression of the wingless gene in the Drosophila embryo. Development. 1992 Nov;116(3):711–719. doi: 10.1242/dev.116.3.711. [DOI] [PubMed] [Google Scholar]
  25. Nüsslein-Volhard C., Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature. 1980 Oct 30;287(5785):795–801. doi: 10.1038/287795a0. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Oro A. E., Ong E. S., Margolis J. S., Posakony J. W., McKeown M., Evans R. M. The Drosophila gene knirps-related is a member of the steroid-receptor gene superfamily. Nature. 1988 Dec 1;336(6198):493–496. doi: 10.1038/336493a0. [DOI] [PubMed] [Google Scholar]
  28. Poole S. J., Kauvar L. M., Drees B., Kornberg T. The engrailed locus of Drosophila: structural analysis of an embryonic transcript. Cell. 1985 Jan;40(1):37–43. doi: 10.1016/0092-8674(85)90306-x. [DOI] [PubMed] [Google Scholar]
  29. Rijsewijk F., Schuermann M., Wagenaar E., Parren P., Weigel D., Nusse R. The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell. 1987 Aug 14;50(4):649–657. doi: 10.1016/0092-8674(87)90038-9. [DOI] [PubMed] [Google Scholar]
  30. Rothe M., Nauber U., Jäckle H. Three hormone receptor-like Drosophila genes encode an identical DNA-binding finger. EMBO J. 1989 Oct;8(10):3087–3094. doi: 10.1002/j.1460-2075.1989.tb08460.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rothe M., Pehl M., Taubert H., Jäckle H. Loss of gene function through rapid mitotic cycles in the Drosophila embryo. Nature. 1992 Sep 10;359(6391):156–159. doi: 10.1038/359156a0. [DOI] [PubMed] [Google Scholar]
  32. Rubin G. M., Spradling A. C. Genetic transformation of Drosophila with transposable element vectors. Science. 1982 Oct 22;218(4570):348–353. doi: 10.1126/science.6289436. [DOI] [PubMed] [Google Scholar]
  33. Tabata T., Eaton S., Kornberg T. B. The Drosophila hedgehog gene is expressed specifically in posterior compartment cells and is a target of engrailed regulation. Genes Dev. 1992 Dec;6(12B):2635–2645. doi: 10.1101/gad.6.12b.2635. [DOI] [PubMed] [Google Scholar]
  34. Tautz D., Pfeifle C. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma. 1989 Aug;98(2):81–85. doi: 10.1007/BF00291041. [DOI] [PubMed] [Google Scholar]
  35. Walldorf U., Gehring W. J. Empty spiracles, a gap gene containing a homeobox involved in Drosophila head development. EMBO J. 1992 Jun;11(6):2247–2259. doi: 10.1002/j.1460-2075.1992.tb05284.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Weigel D., Jäckle H. The fork head domain: a novel DNA binding motif of eukaryotic transcription factors? Cell. 1990 Nov 2;63(3):455–456. doi: 10.1016/0092-8674(90)90439-l. [DOI] [PubMed] [Google Scholar]
  37. 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]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES