Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1995 Feb;139(2):815–833. doi: 10.1093/genetics/139.2.815

Transvection in the Iab-5,6,7 Region of the Bithorax Complex of Drosophila: Homology Independent Interactions in Trans

R Hopmann 1, D Duncan 1, I Duncan 1
PMCID: PMC1206383  PMID: 7713434

Abstract

The Abdominal-B (Abd-B) gene of the bithorax complex (BX-C) of Drosophila controls the identities of the fifth through seventh abdominal segments and segments in the genitalia (more precisely, parasegments 10-14). Here we focus on iab-5, iab-6 and iab-7, regulatory regions of Abd-B that control expression in the fifth, sixth and seventh abdominal segments (parasegments 10-12). By analysis of partial BX-C deficiencies, we show that these regions are able to promote fifth and sixth abdominal segment identities in the absence of an Abd-B gene in cis. We establish that this ability does not result from cis-regulation of the adjacent abd-A or Ubx genes of the BX-C but rather occurs because the iab-5,6,7 region is able to interact with Abd-B in trans. We demonstrate that this interaction is proximity dependent and is, therefore, a case of what E. B. LEWIS has called transvection. Interactions of this type are presumably facilitated by the synapsis of homologues that occurs in somatic cells of Dipterans. Although transvection has been detected in a number of Drosophila genes, transvection of the iab-5,6,7 region is exceptional in two ways. First, interaction in trans with Abd-B does not require that homologues share homologous sequences within, or for some distance to either side of, the BX-C. This is the first case of transvection shown to be independent of local synapsis. A second unusual feature of iab-5,6,7 transvection is that it is remarkably difficult to disrupt by heterozygosity for chromosome rearrangements. The lack of requirement for local synapsis and the tenacity of trans-interaction argue that the iab-5,6,7 region can locate and interact with Abd-B over considerable distance. This is consistent with the normal role of iab-5,6,7, which must act over some 20-60 kb to influence its regulatory target in cis at the Abd-B promoter. Evidence is presented that trans-action of iab-5,6,7 requires, and may be mediated by, the region between distal iab-7 and Abd-B. Also, we show that iab-5,6,7 transvection is independent of the allelic state of zeste, a gene that influences several other cases of transvection. The long-range nature of interactions in trans between iab-5,6,7 and Abd-B suggests that similar interactions could operate effectively in organisms lacking extensive somatic pairing. Transvection may, therefore, be of more general significance than previously suspected.

Full Text

The Full Text of this article is available as a PDF (9.5 MB).

Selected References

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

  1. 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]
  2. Bender W., Weiffenbach B., Karch F., Peifer M. Domains of cis-interaction in the bithorax complex. Cold Spring Harb Symp Quant Biol. 1985;50:173–180. doi: 10.1101/sqb.1985.050.01.023. [DOI] [PubMed] [Google Scholar]
  3. Boulet A. M., Lloyd A., Sakonju S. Molecular definition of the morphogenetic and regulatory functions and the cis-regulatory elements of the Drosophila Abd-B homeotic gene. Development. 1991 Feb;111(2):393–405. doi: 10.1242/dev.111.2.393. [DOI] [PubMed] [Google Scholar]
  4. Brink R. A. Paramutation. Annu Rev Genet. 1973;7:129–152. doi: 10.1146/annurev.ge.07.120173.001021. [DOI] [PubMed] [Google Scholar]
  5. Busturia A., Casanova J., Sánchez-Herrero E., González R., Morata G. Genetic structure of the abd-A gene of Drosophila. Development. 1989 Nov;107(3):575–583. doi: 10.1242/dev.107.3.575. [DOI] [PubMed] [Google Scholar]
  6. Casanova J., Sánchez-Herrero E., Busturia A., Morata G. Double and triple mutant combinations of bithorax complex of Drosophila. EMBO J. 1987 Oct;6(10):3103–3109. doi: 10.1002/j.1460-2075.1987.tb02619.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Celniker S. E., Keelan D. J., Lewis E. B. The molecular genetics of the bithorax complex of Drosophila: characterization of the products of the Abdominal-B domain. Genes Dev. 1989 Sep;3(9):1424–1436. doi: 10.1101/gad.3.9.1424. [DOI] [PubMed] [Google Scholar]
  8. Celniker S. E., Sharma S., Keelan D. J., Lewis E. B. The molecular genetics of the bithorax complex of Drosophila: cis-regulation in the Abdominal-B domain. EMBO J. 1990 Dec;9(13):4277–4286. doi: 10.1002/j.1460-2075.1990.tb07876.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Condie J. M., Brower D. L. Allelic interactions at the engrailed locus of Drosophila: engrailed protein expression in imaginal discs. Dev Biol. 1989 Sep;135(1):31–42. doi: 10.1016/0012-1606(89)90155-3. [DOI] [PubMed] [Google Scholar]
  10. Crosby M. A., Lundquist E. A., Tautvydas R. M., Johnson J. J. The 3' regulatory region of the Abdominal-B gene: genetic analysis supports a model of reiterated and interchangeable regulatory elements. Genetics. 1993 Jul;134(3):809–824. doi: 10.1093/genetics/134.3.809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. Duncan I. The bithorax complex. Annu Rev Genet. 1987;21:285–319. doi: 10.1146/annurev.ge.21.120187.001441. [DOI] [PubMed] [Google Scholar]
  14. Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
  15. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  16. Galloni M., Gyurkovics H., Schedl P., Karch F. The bluetail transposon: evidence for independent cis-regulatory domains and domain boundaries in the bithorax complex. EMBO J. 1993 Mar;12(3):1087–1097. doi: 10.1002/j.1460-2075.1993.tb05750.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. 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]
  20. Hama C., Ali Z., Kornberg T. B. Region-specific recombination and expression are directed by portions of the Drosophila engrailed promoter. Genes Dev. 1990 Jul;4(7):1079–1093. doi: 10.1101/gad.4.7.1079. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Jijakli H., Ghysen A. Segmental determination in Drosophila central nervous system: analysis of the abdominal-A region of the bithorax complex. Int J Dev Biol. 1992 Mar;36(1):93–99. [PubMed] [Google Scholar]
  23. Judd B. H. Transvection: allelic cross talk. Cell. 1988 Jun 17;53(6):841–843. doi: 10.1016/s0092-8674(88)90209-7. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. Kassis J. A., VanSickle E. P., Sensabaugh S. M. A fragment of engrailed regulatory DNA can mediate transvection of the white gene in Drosophila. Genetics. 1991 Aug;128(4):751–761. doi: 10.1093/genetics/128.4.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Kellerman K. A., Mattson D. M., Duncan I. Mutations affecting the stability of the fushi tarazu protein of Drosophila. Genes Dev. 1990 Nov;4(11):1936–1950. doi: 10.1101/gad.4.11.1936. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. 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]
  31. Martinez-Arias A., Lawrence P. A. Parasegments and compartments in the Drosophila embryo. Nature. 1985 Feb 21;313(6004):639–642. doi: 10.1038/313639a0. [DOI] [PubMed] [Google Scholar]
  32. Paro R. Imprinting a determined state into the chromatin of Drosophila. Trends Genet. 1990 Dec;6(12):416–421. doi: 10.1016/0168-9525(90)90303-n. [DOI] [PubMed] [Google Scholar]
  33. Pattatucci A. M., Kaufman T. C. The homeotic gene Sex combs reduced of Drosophila melanogaster is differentially regulated in the embryonic and imaginal stages of development. Genetics. 1991 Oct;129(2):443–461. doi: 10.1093/genetics/129.2.443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Patterson G. I., Thorpe C. J., Chandler V. L. Paramutation, an allelic interaction, is associated with a stable and heritable reduction of transcription of the maize b regulatory gene. Genetics. 1993 Nov;135(3):881–894. doi: 10.1093/genetics/135.3.881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Santamaria P., García-Bellido A. Localization and growth pattern of the tergite Anlage of Drosophila. J Embryol Exp Morphol. 1972 Oct;28(2):397–417. [PubMed] [Google Scholar]
  36. Simon J., Peifer M., Bender W., O'Connor M. Regulatory elements of the bithorax complex that control expression along the anterior-posterior axis. EMBO J. 1990 Dec;9(12):3945–3956. doi: 10.1002/j.1460-2075.1990.tb07615.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Smolik-Utlaut S. M., Gelbart W. M. The effects of chromosomal rearrangements on the zeste-white interaction in Drosophila melanogaster. Genetics. 1987 Jun;116(2):285–298. doi: 10.1093/genetics/116.2.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. 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]
  39. 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]
  40. Sánchez-Herrero E. Control of the expression of the bithorax complex genes abdominal-A and abdominal-B by cis-regulatory regions in Drosophila embryos. Development. 1991 Feb;111(2):437–449. doi: 10.1242/dev.111.2.437. [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. Tartof K. D., Henikoff S. Trans-sensing effects from Drosophila to humans. Cell. 1991 Apr 19;65(2):201–203. doi: 10.1016/0092-8674(91)90153-p. [DOI] [PubMed] [Google Scholar]
  43. Tiong S. Y., Whittle J. R., Gribbin M. C. Chromosomal continuity in the abdominal region of the bithorax complex of Drosophila is not essential for its contribution to metameric identity. Development. 1987 Sep;101(1):135–142. doi: 10.1242/dev.101.1.135. [DOI] [PubMed] [Google Scholar]
  44. 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]
  45. 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 Genetics are provided here courtesy of Oxford University Press

RESOURCES