Skip to main content
PMC home page
The EMBO Journal logoLink to The EMBO Journal
. 1992 Oct;11(10):3645–3652. doi: 10.1002/j.1460-2075.1992.tb05449.x

Trans regulation in the Ultrabithorax gene of Drosophila: alterations in the promoter enhance transvection.

A Martínez-Laborda 1, A González-Reyes 1, G Morata 1
PMCID: PMC556824  PMID: 1396564

Abstract

We report a genetic and molecular study of UbxMX6 and Ubx195rx1, two mutations in the Ultrabithorax (Ubx) locus which appear to have a strong effect on the activity of the homologous Ubx gene. These mutations show the characteristic embryonic and adult phenotypes of Ubx null alleles, and also fail to produce any detectable Ubx product. Yet, genetic and phenotypic analyses involving a large number of trans heterozygous combinations of UbxMX6 and Ubx195rx1 with different classes of Ubx mutations, indicate that they hyperactivate the homologous gene. This effect is induced on wildtype or mutant forms of Ubx, provided that the pairing in the bithorax region is normal, i.e. these mutations have a strong positive effect on transvection. We also show that, unlike all the other known cases of transvection in Ubx, this is not zeste-dependent. Southern analyses indicate that UbxMX6 is a 3.4 kb deletion, and Ubx195rx1 is an approximately 11 kb insertion of foreign DNA, both in the promoter region. We speculate that the region altered in the mutations may have a wildtype function to ensure cis-autonomy of the regulation of Ubx transcription.

Full text

PDF
3649

Images in this article

3647Image
on p.3647
3648Image
on p.3648
3650Image
on p.3650

Selected References

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

  1. Babu P., Selvakumar K. S., Bhosekar S. Studies on transvection at the bithorax complex in Drosophila melanogaster. Mol Gen Genet. 1987 Dec;210(3):557–563. doi: 10.1007/BF00327212. [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. Bender W. Homeotic gene products as growth factors. Cell. 1985 Dec;43(3 Pt 2):559–560. doi: 10.1016/0092-8674(85)90224-7. [DOI] [PubMed] [Google Scholar]
  4. Busturia A., Vernos I., Macias A., Casanova J., Morata G. Different forms of Ultrabithorax proteins generated by alternative splicing are functionally equivalent. EMBO J. 1990 Nov;9(11):3551–3555. doi: 10.1002/j.1460-2075.1990.tb07565.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Casanova J., Sánchez-Herrero E., Morata G. Contrabithorax and the control of spatial expression of the bithorax complex genes of Drosophila. J Embryol Exp Morphol. 1985 Dec;90:179–196. [PubMed] [Google Scholar]
  7. Casanova J., Sánchez-Herrero E., Morata G. Prothoracic transformation and functional structure of the Ultrabithorax gene of Drosophila. Cell. 1985 Sep;42(2):663–669. doi: 10.1016/0092-8674(85)90123-0. [DOI] [PubMed] [Google Scholar]
  8. Castelli-Gair J. E., Micol J. L., García-Bellido A. Transvection in the Drosophila Ultrabithorax gene: a Cbx1 mutant allele induces ectopic expression of a normal allele in trans. Genetics. 1990 Sep;126(1):177–184. doi: 10.1093/genetics/126.1.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dreesen T. D., Henikoff S., Loughney K. A pairing-sensitive element that mediates trans-inactivation is associated with the Drosophila brown gene. Genes Dev. 1991 Mar;5(3):331–340. doi: 10.1101/gad.5.3.331. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. 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]
  12. 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]
  13. Hayes P. H., Sato T., Denell R. E. Homoeosis in Drosophila: the ultrabithorax larval syndrome. Proc Natl Acad Sci U S A. 1984 Jan;81(2):545–549. doi: 10.1073/pnas.81.2.545. [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. 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]
  16. 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]
  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. Kerridge S., Morata G. Developmental effects of some newly induced Ultrabithorax alleles of Drosophila. J Embryol Exp Morphol. 1982 Apr;68:211–234. [PubMed] [Google Scholar]
  19. Lawrence P. A., Green S. M. Cell lineage in the developing retina of Drosophila. Dev Biol. 1979 Jul;71(1):142–152. doi: 10.1016/0012-1606(79)90088-5. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. 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]
  23. Macias A., Casanova J., Morata G. Expression and regulation of the abd-A gene of Drosophila. Development. 1990 Dec;110(4):1197–1207. doi: 10.1242/dev.110.4.1197. [DOI] [PubMed] [Google Scholar]
  24. Mathog D. Transvection in the Ultrabithorax domain of the bithorax complex of Drosophila melanogaster. Genetics. 1990 Jun;125(2):371–382. doi: 10.1093/genetics/125.2.371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Micol J. L., Castelli-Gair J. E., García-Bellido A. Genetic analysis of transvection effects involving cis-regulatory elements of the Drosophila Ultrabithorax gene. Genetics. 1990 Oct;126(2):365–373. doi: 10.1093/genetics/126.2.365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Micol J. L., García-Bellido A. Genetic analysis of "transvection" effects involving contrabithorax mutations in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1988 Feb;85(4):1146–1150. doi: 10.1073/pnas.85.4.1146. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Morata G. Analysis of gene expression during development in the homeotic mutant Contrabithorax of Drosophila melanogaster. J Embryol Exp Morphol. 1975 Aug;34(1):19–31. [PubMed] [Google Scholar]
  28. Morata G., Botas J., Kerridge S., Struhl G. Homeotic transformations of the abdominal segments of Drosophila caused by breaking or deleting a central portion of the bithorax complex. J Embryol Exp Morphol. 1983 Dec;78:319–341. [PubMed] [Google Scholar]
  29. Morata G., Kerridge S. Sequential functions of the bithorax complex of Drosophila. Nature. 1981 Apr 30;290(5809):778–781. doi: 10.1038/290778a0. [DOI] [PubMed] [Google Scholar]
  30. Müller H. P., Schaffner W. Transcriptional enhancers can act in trans. Trends Genet. 1990 Sep;6(9):300–304. doi: 10.1016/0168-9525(90)90236-y. [DOI] [PubMed] [Google Scholar]
  31. Müller J., Bienz M. Long range repression conferring boundaries of Ultrabithorax expression in the Drosophila embryo. EMBO J. 1991 Nov;10(11):3147–3155. doi: 10.1002/j.1460-2075.1991.tb04876.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. 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]
  34. Saari G., Bienz M. The structure of the Ultrabithorax promoter of Drosophila melanogaster. EMBO J. 1987 Jun;6(6):1775–1779. doi: 10.1002/j.1460-2075.1987.tb02430.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. 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]
  36. Struhl G. Genes controlling segmental specification in the Drosophila thorax. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7380–7384. doi: 10.1073/pnas.79.23.7380. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. 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]
  39. White R. A., Wilcox M. Protein products of the bithorax complex in Drosophila. Cell. 1984 Nov;39(1):163–171. doi: 10.1016/0092-8674(84)90202-2. [DOI] [PubMed] [Google Scholar]
  40. Wu C. T., Jones R. S., Lasko P. F., Gelbart W. M. Homeosis and the interaction of zeste and white in Drosophila. Mol Gen Genet. 1989 Sep;218(3):559–564. doi: 10.1007/BF00332424. [DOI] [PubMed] [Google Scholar]
  41. Zachar Z., Chapman C. H., Bingham P. M. On the molecular basis of transvection effects and the regulation of transcription. Cold Spring Harb Symp Quant Biol. 1985;50:337–346. doi: 10.1101/sqb.1985.050.01.043. [DOI] [PubMed] [Google Scholar]

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

RESOURCES