Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1991 Oct;129(2):443–461. doi: 10.1093/genetics/129.2.443

The Homeotic Gene Sex Combs Reduced of Drosophila Melanogaster Is Differentially Regulated in the Embryonic and Imaginal Stages of Development

A M Pattatucci 1, T C Kaufman 1
PMCID: PMC1204635  PMID: 1683847

Abstract

The Sex combs reduced (Scr) locus is unique among the genes contained within the Antennapedia complex (ANT-C) of Drosophila melanogaster in that it directs functions that are required for both cephalic and thoracic development in the embryo and the adult. Antibodies raised against protein encoded by Scr were used to follow the distribution of this gene product in embryos and imaginal discs of third instar larvae. Analysis of Scr protein accumulation in embryos hemizygous for breakpoint lesions mapping throughout the locus has allowed us to determine that sequences required for establishment of the Scr embryonic pattern are contained within a region of DNA that overlaps with the identified upstream regulatory region of the segmentation gene fushi tarazu (ftz). Gain-of-function mutations in Scr result in the presence of ectopic sex comb teeth on the first tarsal segment of mesothoracic and metathoracic legs of adult males. Heterozygous combinations of gain-of-function alleles with a wild-type Scr gene exhibit no evidence of ectopic protein localization in the second and third thoracic segments of embryos. However, mesothoracic and metathoracic leg imaginal discs can be shown to accumulate ectopically expressed Scr protein, implying a differential regulation of the Scr gene during these two periods of development. Additionally, we have found that the spatial pattern of Scr gene expression in imaginal tissues involved in the development of the adult thorax is governed in part by synapsis of homologous chromosomes in this region of the ANT-C. However, those imaginal discs that arise anteriorly to the prothorax do not appear to be sensitive to this form of gene regulation. Finally, we have demonstrated that the extent of Scr expression is influenced by mutations at the Polycomb (Pc) locus but not by mutant alleles of the zeste (z) gene. Taken together, our data suggests that Scr gene expression is differentially regulated both temporally and spatially in a manner that is sensitive to the structure of the locus.

Full Text

The Full Text of this article is available as a PDF (16.1 MB).

Selected References

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

  1. Akam M. The molecular basis for metameric pattern in the Drosophila embryo. Development. 1987 Sep;101(1):1–22. [PubMed] [Google Scholar]
  2. Denell R. E. Homoeosis in Drosophila. II. a Genetic Analysis of Polycomb. Genetics. 1978 Oct;90(2):277–289. doi: 10.1093/genetics/90.2.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Duncan I. Control of bithorax complex functions by the segmentation gene fushi tarazu of D. melanogaster. Cell. 1986 Oct 24;47(2):297–309. doi: 10.1016/0092-8674(86)90452-6. [DOI] [PubMed] [Google Scholar]
  4. Gehring W. J., Hiromi Y. Homeotic genes and the homeobox. Annu Rev Genet. 1986;20:147–173. doi: 10.1146/annurev.ge.20.120186.001051. [DOI] [PubMed] [Google Scholar]
  5. Gelbart W. M. Synapsis-dependent allelic complementation at the decapentaplegic gene complex in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1982 Apr;79(8):2636–2640. doi: 10.1073/pnas.79.8.2636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gelbart W. M., Wu C. T. Interactions of zeste mutations with loci exhibiting transvection effects in Drosophila melanogaster. Genetics. 1982 Oct;102(2):179–189. doi: 10.1093/genetics/102.2.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Geyer P. K., Green M. M., Corces V. G. Tissue-specific transcriptional enhancers may act in trans on the gene located in the homologous chromosome: the molecular basis of transvection in Drosophila. EMBO J. 1990 Jul;9(7):2247–2256. doi: 10.1002/j.1460-2075.1990.tb07395.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. González-Reyes A., Urquia N., Gehring W. J., Struhl G., Morata G. Are cross-regulatory interactions between homoeotic genes functionally significant? Nature. 1990 Mar 1;344(6261):78–80. doi: 10.1038/344078a0. [DOI] [PubMed] [Google Scholar]
  9. Hafen E., Levine M., Gehring W. J. Regulation of Antennapedia transcript distribution by the bithorax complex in Drosophila. Nature. 1984 Jan 19;307(5948):287–289. doi: 10.1038/307287a0. [DOI] [PubMed] [Google Scholar]
  10. Harding K., Levine M. Gap genes define the limits of antennapedia and bithorax gene expression during early development in Drosophila. EMBO J. 1988 Jan;7(1):205–214. doi: 10.1002/j.1460-2075.1988.tb02801.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Harding K., Wedeen C., McGinnis W., Levine M. Spatially regulated expression of homeotic genes in Drosophila. Science. 1985 Sep 20;229(4719):1236–1242. doi: 10.1126/science.3898362. [DOI] [PubMed] [Google Scholar]
  12. Henikoff S., Dreesen T. D. Trans-inactivation of the Drosophila brown gene: evidence for transcriptional repression and somatic pairing dependence. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6704–6708. doi: 10.1073/pnas.86.17.6704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ingham P. W., Martinez-Arias A. The correct activation of Antennapedia and bithorax complex genes requires the fushi tarazu gene. Nature. 1986 Dec 11;324(6097):592–597. doi: 10.1038/324592a0. [DOI] [PubMed] [Google Scholar]
  14. Jack J. W., Judd B. H. Allelic pairing and gene regulation: A model for the zeste-white interaction in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1368–1372. doi: 10.1073/pnas.76.3.1368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kaufman T. C., Lewis R., Wakimoto B. Cytogenetic Analysis of Chromosome 3 in DROSOPHILA MELANOGASTER: The Homoeotic Gene Complex in Polytene Chromosome Interval 84a-B. Genetics. 1980 Jan;94(1):115–133. doi: 10.1093/genetics/94.1.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kaufman T. C., Seeger M. A., Olsen G. Molecular and genetic organization of the antennapedia gene complex of Drosophila melanogaster. Adv Genet. 1990;27:309–362. doi: 10.1016/s0065-2660(08)60029-2. [DOI] [PubMed] [Google Scholar]
  17. Kaufman T. C., Tasaka S. E., Suzuki D. T. The interaction of two complex loci, zeste and bithorax in Drosophila melanogaster. Genetics. 1973 Oct;75(2):299–321. doi: 10.1093/genetics/75.2.299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kennison J. A., Tamkun J. W. Dosage-dependent modifiers of polycomb and antennapedia mutations in Drosophila. Proc Natl Acad Sci U S A. 1988 Nov;85(21):8136–8140. doi: 10.1073/pnas.85.21.8136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ko H. S., Fast P., McBride W., Staudt L. M. A human protein specific for the immunoglobulin octamer DNA motif contains a functional homeobox domain. Cell. 1988 Oct 7;55(1):135–144. doi: 10.1016/0092-8674(88)90016-5. [DOI] [PubMed] [Google Scholar]
  20. LeMotte P. K., Kuroiwa A., Fessler L. I., Gehring W. J. The homeotic gene Sex Combs Reduced of Drosophila: gene structure and embryonic expression. EMBO J. 1989 Jan;8(1):219–227. doi: 10.1002/j.1460-2075.1989.tb03367.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lewis E. B. A gene complex controlling segmentation in Drosophila. Nature. 1978 Dec 7;276(5688):565–570. doi: 10.1038/276565a0. [DOI] [PubMed] [Google Scholar]
  22. Lewis R. A., Wakimoto B. T., Denell R. E., Kaufman T. C. Genetic Analysis of the Antennapedia Gene Complex (Ant-C) and Adjacent Chromosomal Regions of DROSOPHILA MELANOGASTER. II. Polytene Chromosome Segments 84A-84B1,2. Genetics. 1980 Jun;95(2):383–397. doi: 10.1093/genetics/95.2.383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Little J. W., Byrd C. A., Brower D. L. Effect of abx, bx and pbx mutations on expression of homeotic genes in Drosophila larvae. Genetics. 1990 Apr;124(4):899–908. doi: 10.1093/genetics/124.4.899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mahaffey J. W., Diederich R. J., Kaufman T. C. Novel patterns of homeotic protein accumulation in the head of the Drosophila embryo. Development. 1989 Jan;105(1):167–174. doi: 10.1242/dev.105.1.167. [DOI] [PubMed] [Google Scholar]
  25. Mahaffey J. W., Kaufman T. C. Distribution of the Sex combs reduced gene products in Drosophila melanogaster. Genetics. 1987 Sep;117(1):51–60. doi: 10.1093/genetics/117.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Martinez-Arias A., Ingham P. W., Scott M. P., Akam M. E. The spatial and temporal deployment of Dfd and Scr transcripts throughout development of Drosophila. Development. 1987 Aug;100(4):673–683. doi: 10.1242/dev.100.4.673. [DOI] [PubMed] [Google Scholar]
  27. McGinnis W., Levine M. S., Hafen E., Kuroiwa A., Gehring W. J. A conserved DNA sequence in homoeotic genes of the Drosophila Antennapedia and bithorax complexes. 1984 Mar 29-Apr 4Nature. 308(5958):428–433. doi: 10.1038/308428a0. [DOI] [PubMed] [Google Scholar]
  28. Mirkovitch J., Gasser S. M., Laemmli U. K. Relation of chromosome structure and gene expression. Philos Trans R Soc Lond B Biol Sci. 1987 Dec 15;317(1187):563–574. doi: 10.1098/rstb.1987.0081. [DOI] [PubMed] [Google Scholar]
  29. Pattatucci A. M., Otteson D. C., Kaufman T. C. A functional and structural analysis of the Sex combs reduced locus of Drosophila melanogaster. Genetics. 1991 Oct;129(2):423–441. doi: 10.1093/genetics/129.2.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Phillips M. D., Shearn A. Mutations in polycombeotic, a Drosophila polycomb-group gene, cause a wide range of maternal and zygotic phenotypes. Genetics. 1990 May;125(1):91–101. doi: 10.1093/genetics/125.1.91. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Riley P. D., Carroll S. B., Scott M. P. The expression and regulation of Sex combs reduced protein in Drosophila embryos. Genes Dev. 1987 Sep;1(7):716–730. doi: 10.1101/gad.1.7.716. [DOI] [PubMed] [Google Scholar]
  32. Roberts P. A. Differences in synaptic affinity of chromosome arms of Drosophila melanogaster revealed by differential sensitivity to translocation heterozygosity. Genetics. 1972 Jul;71(3):401–415. doi: 10.1093/genetics/71.3.401. [DOI] [PubMed] [Google Scholar]
  33. Roberts P. A. Screening for x-ray-induced crossover suppressors in Drosophila melanogaster: prevalence and effectiveness of translocations. Genetics. 1970 Jul;65(3):429–448. doi: 10.1093/genetics/65.3.429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Scott M. P., O'Farrell P. H. Spatial programming of gene expression in early Drosophila embryogenesis. Annu Rev Cell Biol. 1986;2:49–80. doi: 10.1146/annurev.cb.02.110186.000405. [DOI] [PubMed] [Google Scholar]
  35. Scott M. P., Tamkun J. W., Hartzell G. W., 3rd The structure and function of the homeodomain. Biochim Biophys Acta. 1989 Jul 28;989(1):25–48. doi: 10.1016/0304-419x(89)90033-4. [DOI] [PubMed] [Google Scholar]
  36. Scott M. P., Weiner A. J., Hazelrigg T. I., Polisky B. A., Pirrotta V., Scalenghe F., Kaufman T. C. The molecular organization of the Antennapedia locus of Drosophila. Cell. 1983 Dec;35(3 Pt 2):763–776. doi: 10.1016/0092-8674(83)90109-5. [DOI] [PubMed] [Google Scholar]
  37. Struhl G., Akam M. Altered distributions of Ultrabithorax transcripts in extra sex combs mutant embryos of Drosophila. EMBO J. 1985 Dec 1;4(12):3259–3264. doi: 10.1002/j.1460-2075.1985.tb04075.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Struhl G., White R. A. Regulation of the Ultrabithorax gene of Drosophila by other bithorax complex genes. Cell. 1985 Dec;43(2 Pt 1):507–519. doi: 10.1016/0092-8674(85)90180-1. [DOI] [PubMed] [Google Scholar]
  39. Wakimoto B. T., Turner F. R., Kaufman T. C. Defects in embryogenesis in mutants associated with the antennapedia gene complex of Drosophila melanogaster. Dev Biol. 1984 Mar;102(1):147–172. doi: 10.1016/0012-1606(84)90182-9. [DOI] [PubMed] [Google Scholar]
  40. Wedeen C., Harding K., Levine M. Spatial regulation of Antennapedia and bithorax gene expression by the Polycomb locus in Drosophila. Cell. 1986 Mar 14;44(5):739–748. doi: 10.1016/0092-8674(86)90840-8. [DOI] [PubMed] [Google Scholar]
  41. White R. A., Lehmann R. A gap gene, hunchback, regulates the spatial expression of Ultrabithorax. Cell. 1986 Oct 24;47(2):311–321. doi: 10.1016/0092-8674(86)90453-8. [DOI] [PubMed] [Google Scholar]
  42. Wu C. T., Goldberg M. L. The Drosophila zeste gene and transvection. Trends Genet. 1989 Jun;5(6):189–194. doi: 10.1016/0168-9525(89)90074-7. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES