Skip to main content
PMC home page
The EMBO Journal logoLink to The EMBO Journal
. 1990 Dec;9(13):4277–4286. doi: 10.1002/j.1460-2075.1990.tb07876.x

The molecular genetics of the bithorax complex of Drosophila: cis-regulation in the Abdominal-B domain.

S E Celniker 1, S Sharma 1, D J Keelan 1, E B Lewis 1
PMCID: PMC552210  PMID: 2265608

Abstract

In Drosophila the Abdominal-B (Abd-B) domain of the bithorax complex (BX-C) spans over 100 kb and is responsible for specifying the identities of adult abdominal segments five (A5) to nine (A9), inclusive, and correspondingly, neuromeres 10-14 of the embryonic central nervous system. The domain consists of a region coding for two proteins, ABD-BI (54 kd) and ABD-BII (36 kd) and cis-regulatory regions extending from infra-abdominal-5 (iab-5) to iab-9, inclusive. We have used a monoclonal anti-ABD-B antibody to infer that mutants in iab-8 eliminate the expression of ABD-BI in neuromeres 10-13, inclusive, and that mutants in iab-9 eliminate expression of ABD-BII in neuromere 14. ABD-B expression is also analyzed in homozygotes for (i) loss-of-function mutants involving the iab-5, iab-6 and iab-7 regions, (ii) gain-of-function mutants Miscadastral pigmentation (Mcp) and Superabdominal (Sab), and (iii) a trans-regulator, Polycomb (Pc). ABD-B expression along the antero-posterior axis is colinear with the chromosomal order of the cis-regulatory regions. The behavior of rearrangement-associated iab-6 and iab-7 mutants suggests that the enhancer-like region, iab-5, and possibly also iab-6, may be shared between the abd-A and Abd-B domains. Such sharing is proposed as a factor that tends to keep gene complexes intact during evolution.

Full text

PDF
4278

Images in this article

4280Fig. 2.
on p.4280
4282Fig. 3.
on p.4282
4282Fig. 4.
on p.4282
4282Fig. 5.
on p.4282
4284Fig. 6.
on p.4284
4284Fig. 7.
on p.4284

Selected References

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

  1. Beachy P. A., Helfand S. L., Hogness D. S. Segmental distribution of bithorax complex proteins during Drosophila development. Nature. 1985 Feb 14;313(6003):545–551. doi: 10.1038/313545a0. [DOI] [PubMed] [Google Scholar]
  2. Bender W., Akam M., Karch F., Beachy P. A., Peifer M., Spierer P., Lewis E. B., Hogness D. S. Molecular Genetics of the Bithorax Complex in Drosophila melanogaster. Science. 1983 Jul 1;221(4605):23–29. doi: 10.1126/science.221.4605.23. [DOI] [PubMed] [Google Scholar]
  3. Casanova J., Sánchez-Herrero E., Morata G. Identification and characterization of a parasegment specific regulatory element of the abdominal-B gene of Drosophila. Cell. 1986 Nov 21;47(4):627–636. doi: 10.1016/0092-8674(86)90627-6. [DOI] [PubMed] [Google Scholar]
  4. Celniker S. E., Lewis E. B. Transabdominal, a dominant mutant of the Bithorax Complex, produces a sexually dimorphic segmental transformation in Drosophila. Genes Dev. 1987 Apr;1(2):111–123. doi: 10.1101/gad.1.2.111. [DOI] [PubMed] [Google Scholar]
  5. Cumberledge S., Zaratzian A., Sakonju S. Characterization of two RNAs transcribed from the cis-regulatory region of the abd-A domain within the Drosophila bithorax complex. Proc Natl Acad Sci U S A. 1990 May;87(9):3259–3263. doi: 10.1073/pnas.87.9.3259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. DeLorenzi M., Ali N., Saari G., Henry C., Wilcox M., Bienz M. Evidence that the Abdominal-B r element function is conferred by a trans-regulatory homeoprotein. EMBO J. 1988 Oct;7(10):3223–3231. doi: 10.1002/j.1460-2075.1988.tb03189.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Delorenzi M., Bienz M. Expression of Abdominal-B homeoproteins in Drosophila embryos. Development. 1990 Feb;108(2):323–329. doi: 10.1242/dev.108.2.323. [DOI] [PubMed] [Google Scholar]
  8. Desplan C., Theis J., O'Farrell P. H. The Drosophila developmental gene, engrailed, encodes a sequence-specific DNA binding activity. Nature. 1985 Dec 19;318(6047):630–635. doi: 10.1038/318630a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Duncan I. M. Polycomblike: a gene that appears to be required for the normal expression of the bithorax and antennapedia gene complexes of Drosophila melanogaster. Genetics. 1982 Sep;102(1):49–70. doi: 10.1093/genetics/102.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Duncan I. The bithorax complex. Annu Rev Genet. 1987;21:285–319. doi: 10.1146/annurev.ge.21.120187.001441. [DOI] [PubMed] [Google Scholar]
  12. Enver T., Raich N., Ebens A. J., Papayannopoulou T., Costantini F., Stamatoyannopoulos G. Developmental regulation of human fetal-to-adult globin gene switching in transgenic mice. Nature. 1990 Mar 22;344(6264):309–313. doi: 10.1038/344309a0. [DOI] [PubMed] [Google Scholar]
  13. Garber R. L., Kuroiwa A., Gehring W. J. Genomic and cDNA clones of the homeotic locus Antennapedia in Drosophila. EMBO J. 1983;2(11):2027–2036. doi: 10.1002/j.1460-2075.1983.tb01696.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hogness D. S., Lipshitz H. D., Beachy P. A., Peattie D. A., Saint R. B., Goldschmidt-Clermont M., Harte P. J., Gavis E. R., Helfand S. L. Regulation and products of the Ubx domain of the bithorax complex. Cold Spring Harb Symp Quant Biol. 1985;50:181–194. doi: 10.1101/sqb.1985.050.01.024. [DOI] [PubMed] [Google Scholar]
  15. Ingham P. W., Ish-Horowicz D., Howard K. R. Correlative changes in homoeotic and segmentation gene expression in Krüppel mutant embryos of Drosophila. EMBO J. 1986 Jul;5(7):1659–1665. doi: 10.1002/j.1460-2075.1986.tb04409.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Karch F., Bender W., Weiffenbach B. abdA expression in Drosophila embryos. Genes Dev. 1990 Sep;4(9):1573–1587. doi: 10.1101/gad.4.9.1573. [DOI] [PubMed] [Google Scholar]
  18. Karch F., Weiffenbach B., Peifer M., Bender W., Duncan I., Celniker S., Crosby M., Lewis E. B. The abdominal region of the bithorax complex. Cell. 1985 Nov;43(1):81–96. doi: 10.1016/0092-8674(85)90014-5. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Kornfeld K., Saint R. B., Beachy P. A., Harte P. J., Peattie D. A., Hogness D. S. Structure and expression of a family of Ultrabithorax mRNAs generated by alternative splicing and polyadenylation in Drosophila. Genes Dev. 1989 Feb;3(2):243–258. doi: 10.1101/gad.3.2.243. [DOI] [PubMed] [Google Scholar]
  21. Krasnow M. A., Saffman E. E., Kornfeld K., Hogness D. S. Transcriptional activation and repression by Ultrabithorax proteins in cultured Drosophila cells. Cell. 1989 Jun 16;57(6):1031–1043. doi: 10.1016/0092-8674(89)90341-3. [DOI] [PubMed] [Google Scholar]
  22. Kuziora M. A., McGinnis W. Different transcripts of the Drosophila Abd-B gene correlate with distinct genetic sub-functions. EMBO J. 1988 Oct;7(10):3233–3244. doi: 10.1002/j.1460-2075.1988.tb03190.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Laughon A., Scott M. P. Sequence of a Drosophila segmentation gene: protein structure homology with DNA-binding proteins. Nature. 1984 Jul 5;310(5972):25–31. doi: 10.1038/310025a0. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Lewis E. B. Regulation of the genes of the bithorax complex in Drosophila. Cold Spring Harb Symp Quant Biol. 1985;50:155–164. doi: 10.1101/sqb.1985.050.01.021. [DOI] [PubMed] [Google Scholar]
  26. Lipshitz H. D., Peattie D. A., Hogness D. S. Novel transcripts from the Ultrabithorax domain of the bithorax complex. Genes Dev. 1987 May;1(3):307–322. doi: 10.1101/gad.1.3.307. [DOI] [PubMed] [Google Scholar]
  27. Mann R. S., Hogness D. S. Functional dissection of Ultrabithorax proteins in D. melanogaster. Cell. 1990 Feb 23;60(4):597–610. doi: 10.1016/0092-8674(90)90663-y. [DOI] [PubMed] [Google Scholar]
  28. McGinnis W., Garber R. L., Wirz J., Kuroiwa A., Gehring W. J. A homologous protein-coding sequence in Drosophila homeotic genes and its conservation in other metazoans. Cell. 1984 Jun;37(2):403–408. doi: 10.1016/0092-8674(84)90370-2. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. O'Connor M. B., Binari R., Perkins L. A., Bender W. Alternative RNA products from the Ultrabithorax domain of the bithorax complex. EMBO J. 1988 Feb;7(2):435–445. doi: 10.1002/j.1460-2075.1988.tb02831.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Peifer M., Bender W. The anterobithorax and bithorax mutations of the bithorax complex. EMBO J. 1986 Sep;5(9):2293–2303. doi: 10.1002/j.1460-2075.1986.tb04497.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Regulski M., Harding K., Kostriken R., Karch F., Levine M., McGinnis W. Homeo box genes of the Antennapedia and bithorax complexes of Drosophila. Cell. 1985 Nov;43(1):71–80. doi: 10.1016/0092-8674(85)90013-3. [DOI] [PubMed] [Google Scholar]
  33. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. Scott M. P., Weiner A. J. Structural relationships among genes that control development: sequence homology between the Antennapedia, Ultrabithorax, and fushi tarazu loci of Drosophila. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4115–4119. doi: 10.1073/pnas.81.13.4115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Shepherd J. C., McGinnis W., Carrasco A. E., De Robertis E. M., Gehring W. J. Fly and frog homoeo domains show homologies with yeast mating type regulatory proteins. Nature. 1984 Jul 5;310(5972):70–71. doi: 10.1038/310070a0. [DOI] [PubMed] [Google Scholar]
  37. Struhl G. A gene product required for correct initiation of segmental determination in Drosophila. Nature. 1981 Sep 3;293(5827):36–41. doi: 10.1038/293036a0. [DOI] [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. Sánchez-Herrero E., Akam M. Spatially ordered transcription of regulatory DNA in the bithorax complex of Drosophila. Development. 1989 Oct;107(2):321–329. doi: 10.1242/dev.107.2.321. [DOI] [PubMed] [Google Scholar]
  40. Sánchez-Herrero E., Casanova J., Kerridge S., Morata G. Anatomy and function of the bithorax complex of Drosophila. Cold Spring Harb Symp Quant Biol. 1985;50:165–172. doi: 10.1101/sqb.1985.050.01.022. [DOI] [PubMed] [Google Scholar]
  41. Sánchez-Herrero E., Crosby M. A. The Abdominal-B gene of Drosophila melanogaster: overlapping transcripts exhibit two different spatial distributions. EMBO J. 1988 Jul;7(7):2163–2173. doi: 10.1002/j.1460-2075.1988.tb03055.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Sánchez-Herrero E., Vernós I., Marco R., Morata G. Genetic organization of Drosophila bithorax complex. Nature. 1985 Jan 10;313(5998):108–113. doi: 10.1038/313108a0. [DOI] [PubMed] [Google Scholar]
  43. Tiong S., Bone L. M., Whittle J. R. Recessive lethal mutations within the bithorax-complex in Drosophila. Mol Gen Genet. 1985;200(2):335–342. doi: 10.1007/BF00425445. [DOI] [PubMed] [Google Scholar]
  44. Tremml G., Bienz M. Homeotic gene expression in the visceral mesoderm of Drosophila embryos. EMBO J. 1989 Sep;8(9):2677–2685. doi: 10.1002/j.1460-2075.1989.tb08408.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. 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]
  46. 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]
  47. Zavortink M., Sakonju S. The morphogenetic and regulatory functions of the Drosophila Abdominal-B gene are encoded in overlapping RNAs transcribed from separate promoters. Genes Dev. 1989 Dec;3(12A):1969–1981. doi: 10.1101/gad.3.12a.1969. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES