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. 1985 Dec 16;4(13A):3489–3499. doi: 10.1002/j.1460-2075.1985.tb04108.x

Separable cis-acting control elements for expression of the white gene of Drosophila.

R Levis, T Hazelrigg, G M Rubin
PMCID: PMC554688  PMID: 3004962

Abstract

The white gene of Drosophila is required for the pigmentation of the eyes, ocelli, Malpighian tubules and testis sheath. We have examined the regulation of white expression in germ line transformants that carry the mRNA-coding sequences of white flanked by varying amounts of the sequences normally located adjacent to them. A segment with as little as 1.9 kb of 5'- and 2.1 kb of 3'-flanking DNA was expressed to give essentially wild-type pigmentation in all of these tissues and interacted in trans with the zeste-1 allele. In contrast, transformants having segments with 1.1 kb of 5'-flanking DNA had reduced levels of pigment in their eyes, no detectable pigment in their testes and did not interact with zeste-1. The eyes, Malpighian tubules and ocelli of transformants with as little as 0.4 kb of 5'-flanking DNA were pigmented and the eye pigmentation exhibited dosage compensation. We conclude that there are sequence elements present in the region from 1.1 to 1.9 kb upstream from the 5' end of the white transcript which are required for expression in the testes and interaction of white and zeste-1. The same or other elements in this region appear to augment the pigmentation of the eye.

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Selected References

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

  1. Baker B. S., Belote J. M. Sex determination and dosage compensation in Drosophila melanogaster. Annu Rev Genet. 1983;17:345–393. doi: 10.1146/annurev.ge.17.120183.002021. [DOI] [PubMed] [Google Scholar]
  2. Bingham P. M., Zachar Z. Evidence that two mutations, wDZL and z1, affecting synapsis-dependent genetic behavior of white are transcriptional regulatory mutations. Cell. 1985 Apr;40(4):819–825. doi: 10.1016/0092-8674(85)90341-1. [DOI] [PubMed] [Google Scholar]
  3. Birchmeier C., Schümperli D., Sconzo G., Birnstiel M. L. 3' editing of mRNAs: sequence requirements and involvement of a 60-nucleotide RNA in maturation of histone mRNA precursors. Proc Natl Acad Sci U S A. 1984 Feb;81(4):1057–1061. doi: 10.1073/pnas.81.4.1057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Birnstiel M. L., Busslinger M., Strub K. Transcription termination and 3' processing: the end is in site! Cell. 1985 Jun;41(2):349–359. doi: 10.1016/s0092-8674(85)80007-6. [DOI] [PubMed] [Google Scholar]
  5. Bourouis M., Richards G. Remote regulatory sequences of the Drosophila glue gene sgs3 as revealed by P-element transformation. Cell. 1985 Feb;40(2):349–357. doi: 10.1016/0092-8674(85)90149-7. [DOI] [PubMed] [Google Scholar]
  6. Daniels S. B., McCarron M., Love C., Chovnick A. Dysgenesis-induced instability of rosy locus transformation in Drosophila melanogaster: analysis of excision events and the selective recovery of control element deletions. Genetics. 1985 Jan;109(1):95–117. doi: 10.1093/genetics/109.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Davison D., Chapman C. H., Wedeen C., Bingham P. M. Genetic and physical studies of a portion of the white locus participating in transcriptional regulation and in synapsis-dependent interactions in Drosophila adult tissues. Genetics. 1985 Jul;110(3):479–494. doi: 10.1093/genetics/110.3.479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Demerec M, Slizynska H. Mottled White 258-18 of Drosophila Melanogaster. Genetics. 1937 Nov;22(6):641–649. doi: 10.1093/genetics/22.6.641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fjose A., Polito L. C., Weber U., Gehring W. J. Developmental expression of the white locus of Drosophila melanogaster. EMBO J. 1984 Sep;3(9):2087–2094. doi: 10.1002/j.1460-2075.1984.tb02095.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Garabedian M. J., Hung M. C., Wensink P. C. Independent control elements that determine yolk protein gene expression in alternative Drosophila tissues. Proc Natl Acad Sci U S A. 1985 Mar;82(5):1396–1400. doi: 10.1073/pnas.82.5.1396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gehring W. J., Klemenz R., Weber U., Kloter U. Functional analysis of the white gene of Drosophila by P-factor-mediated transformation. EMBO J. 1984 Sep;3(9):2077–2085. doi: 10.1002/j.1460-2075.1984.tb02094.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Gersh E S. Pigmentation in a Mottled White Eye Due to Position Effect in Drosophila Melanogaster. Genetics. 1952 May;37(3):322–338. doi: 10.1093/genetics/37.3.322. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Grosschedl R., Baltimore D. Cell-type specificity of immunoglobulin gene expression is regulated by at least three DNA sequence elements. Cell. 1985 Jul;41(3):885–897. doi: 10.1016/s0092-8674(85)80069-6. [DOI] [PubMed] [Google Scholar]
  15. Hazelrigg T., Levis R., Rubin G. M. Transformation of white locus DNA in drosophila: dosage compensation, zeste interaction, and position effects. Cell. 1984 Feb;36(2):469–481. doi: 10.1016/0092-8674(84)90240-x. [DOI] [PubMed] [Google Scholar]
  16. JUDD B. H. Formation of duplication-deficiency products by asymmetrical exchange within a complex locus of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1961 Apr 15;47:545–550. doi: 10.1073/pnas.47.4.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  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. 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]
  20. Levis R., Bingham P. M., Rubin G. M. Physical map of the white locus of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1982 Jan;79(2):564–568. doi: 10.1073/pnas.79.2.564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lifschytz E., Green M. M. The zeste-white interaction: induction and genetic analysis of a novel class of zeste alleles. EMBO J. 1984 May;3(5):999–1002. doi: 10.1002/j.1460-2075.1984.tb01919.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. McDevitt M. A., Imperiale M. J., Ali H., Nevins J. R. Requirement of a downstream sequence for generation of a poly(A) addition site. Cell. 1984 Jul;37(3):993–999. doi: 10.1016/0092-8674(84)90433-1. [DOI] [PubMed] [Google Scholar]
  23. O'Hare K., Murphy C., Levis R., Rubin G. M. DNA sequence of the white locus of Drosophila melanogaster. J Mol Biol. 1984 Dec 15;180(3):437–455. doi: 10.1016/0022-2836(84)90021-4. [DOI] [PubMed] [Google Scholar]
  24. O'Hare K., Rubin G. M. Structures of P transposable elements and their sites of insertion and excision in the Drosophila melanogaster genome. Cell. 1983 Aug;34(1):25–35. doi: 10.1016/0092-8674(83)90133-2. [DOI] [PubMed] [Google Scholar]
  25. O'hare K., Levis R., Rubin G. M. Transcription of the white locus in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1983 Nov;80(22):6917–6921. doi: 10.1073/pnas.80.22.6917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Pirrotta V., Bröckl C. Transcription of the Drosophila white locus and some of its mutants. EMBO J. 1984 Mar;3(3):563–568. doi: 10.1002/j.1460-2075.1984.tb01847.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Pirrotta V., Hadfield C., Pretorius G. H. Microdissection and cloning of the white locus and the 3B1-3C2 region of the Drosophila X chromosome. EMBO J. 1983;2(6):927–934. doi: 10.1002/j.1460-2075.1983.tb01523.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Pirrotta V., Steller H., Bozzetti M. P. Multiple upstream regulatory elements control the expression of the Drosophila white gene. EMBO J. 1985 Dec 16;4(13A):3501–3508. doi: 10.1002/j.1460-2075.1985.tb04109.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ready D. F., Hanson T. E., Benzer S. Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol. 1976 Oct 15;53(2):217–240. doi: 10.1016/0012-1606(76)90225-6. [DOI] [PubMed] [Google Scholar]
  30. Rubin G. M., Spradling A. C. Vectors for P element-mediated gene transfer in Drosophila. Nucleic Acids Res. 1983 Sep 24;11(18):6341–6351. doi: 10.1093/nar/11.18.6341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. SCHULTZ J. The relation of the heterochromatic chromosome regions to the nucleic acids of the cell. Cold Spring Harb Symp Quant Biol. 1956;21:307–328. doi: 10.1101/sqb.1956.021.01.025. [DOI] [PubMed] [Google Scholar]
  32. Spradling A. C., Rubin G. M. The effect of chromosomal position on the expression of the Drosophila xanthine dehydrogenase gene. Cell. 1983 Aug;34(1):47–57. doi: 10.1016/0092-8674(83)90135-6. [DOI] [PubMed] [Google Scholar]
  33. Spradling A. C., Rubin G. M. Transposition of cloned P elements into Drosophila germ line chromosomes. Science. 1982 Oct 22;218(4570):341–347. doi: 10.1126/science.6289435. [DOI] [PubMed] [Google Scholar]
  34. Zachar Z., Bingham P. M. Regulation of white locus expression: the structure of mutant alleles at the white locus of Drosophila melanogaster. Cell. 1982 Sep;30(2):529–541. doi: 10.1016/0092-8674(82)90250-1. [DOI] [PubMed] [Google Scholar]
  35. Zuker C. S., Cowman A. F., Rubin G. M. Isolation and structure of a rhodopsin gene from D. melanogaster. Cell. 1985 Apr;40(4):851–858. doi: 10.1016/0092-8674(85)90344-7. [DOI] [PubMed] [Google Scholar]
  36. van Breugel F. M. Cell clustering and pleiotropy in white-variegated eyes and Malphighian tubes of Drosophila hydei. Genetics. 1973 Oct;75(2):323–334. doi: 10.1093/genetics/75.2.323. [DOI] [PMC free article] [PubMed] [Google Scholar]

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