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. 1986 Dec 1;5(12):3343–3351. doi: 10.1002/j.1460-2075.1986.tb04649.x

Evidence that white-blood is a novel type of temperature-sensitive mutation resulting from temperature-dependent effects of a transposon insertion on formation of white transcripts.

P M Bingham, C H Chapman
PMCID: PMC1167332  PMID: 3028781

Abstract

We report results indicating that the temperature-sensitive white-blood (wbl) mutation has a novel molecular basis, involving the formation of RNA transcripts of the affected gene rather than the behavior of the polypeptide product. First, we show that the temperature-sensitive mutant phenotype of wbl correlates with (and presumably results from) a temperature-dependent effect on levels of the 2.6-kb polyadenylated white transcript. Second, DNA sequence analysis and other studies show that wbl is associated with the insertion into the second white intron of a previously uncharacterized retrotransposon (designated the blood transposon). We discuss the potential origins of the novel temperature-sensitive molecular phenotype of wbl and the prospects for exploiting wbl to engineer temperature-sensitive mutations in other genes.

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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. Benyajati C., Spoerel N., Haymerle H., Ashburner M. The messenger RNA for alcohol dehydrogenase in Drosophila melanogaster differs in its 5' end in different developmental stages. Cell. 1983 May;33(1):125–133. doi: 10.1016/0092-8674(83)90341-0. [DOI] [PubMed] [Google Scholar]
  3. Bingham P. M., Judd B. H. A copy of the copia transposable element is very tightly linked to the Wa allele at the white locus of D. melanogaster. Cell. 1981 Sep;25(3):705–711. doi: 10.1016/0092-8674(81)90177-x. [DOI] [PubMed] [Google Scholar]
  4. Bingham P. M., Kidwell M. G., Rubin G. M. The molecular basis of P-M hybrid dysgenesis: the role of the P element, a P-strain-specific transposon family. Cell. 1982 Jul;29(3):995–1004. doi: 10.1016/0092-8674(82)90463-9. [DOI] [PubMed] [Google Scholar]
  5. Bingham P. M., Levis R., Rubin G. M. Cloning of DNA sequences from the white locus of D. melanogaster by a novel and general method. Cell. 1981 Sep;25(3):693–704. doi: 10.1016/0092-8674(81)90176-8. [DOI] [PubMed] [Google Scholar]
  6. 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]
  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. Emerman M., Temin H. M. Genes with promoters in retrovirus vectors can be independently suppressed by an epigenetic mechanism. Cell. 1984 Dec;39(3 Pt 2):449–467. [PubMed] [Google Scholar]
  9. Emori Y., Shiba T., Kanaya S., Inouye S., Yuki S., Saigo K. The nucleotide sequences of copia and copia-related RNA in Drosophila virus-like particles. 1985 Jun 27-Jul 3Nature. 315(6022):773–776. doi: 10.1038/315773a0. [DOI] [PubMed] [Google Scholar]
  10. Ephrussi B, Herold J L. Studies of Eye Pigments of Drosophila II. Effect of Temperature on the Red and Brown Pigments in the Mutant Blood (w). Genetics. 1945 Jan;30(1):62–70. doi: 10.1093/genetics/30.1.62. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Frischauf A. M., Lehrach H., Poustka A., Murray N. Lambda replacement vectors carrying polylinker sequences. J Mol Biol. 1983 Nov 15;170(4):827–842. doi: 10.1016/s0022-2836(83)80190-9. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Hu N., Messing J. The making of strand-specific M13 probes. Gene. 1982 Mar;17(3):271–277. doi: 10.1016/0378-1119(82)90143-3. [DOI] [PubMed] [Google Scholar]
  14. Hyde R R. Two New Members of a Sex-Linked Multiple (Sex-Tuple) Allelomorph System. Genetics. 1916 Nov;1(6):535–580. doi: 10.1093/genetics/1.6.535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Inouye S., Saigo K., Yamada K., Kuchino Y. Identification and nucleotide sequence determination of a potential primer tRNA for reverse transcription of a Drosophila retrotransposon, 297. Nucleic Acids Res. 1986 Apr 11;14(7):3031–3043. doi: 10.1093/nar/14.7.3031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kidd S., Lockett T. J., Young M. W. The Notch locus of Drosophila melanogaster. Cell. 1983 Sep;34(2):421–433. doi: 10.1016/0092-8674(83)90376-8. [DOI] [PubMed] [Google Scholar]
  17. Kidd S., Young M. W. Transposon-dependent mutant phenotypes at the Notch locus of Drosophila. Nature. 1986 Sep 4;323(6083):89–91. doi: 10.1038/323089a0. [DOI] [PubMed] [Google Scholar]
  18. Levis R., O'Hare K., Rubin G. M. Effects of transposable element insertions on RNA encoded by the white gene of Drosophila. Cell. 1984 Sep;38(2):471–481. doi: 10.1016/0092-8674(84)90502-6. [DOI] [PubMed] [Google Scholar]
  19. Lindsley D. L., Sandler L., Baker B. S., Carpenter A. T., Denell R. E., Hall J. C., Jacobs P. A., Miklos G. L., Davis B. K., Gethmann R. C. Segmental aneuploidy and the genetic gross structure of the Drosophila genome. Genetics. 1972 May;71(1):157–184. doi: 10.1093/genetics/71.1.157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Marlor R. L., Parkhurst S. M., Corces V. G. The Drosophila melanogaster gypsy transposable element encodes putative gene products homologous to retroviral proteins. Mol Cell Biol. 1986 Apr;6(4):1129–1134. doi: 10.1128/mcb.6.4.1129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. O'Connell P. O., Rosbash M. Sequence, structure, and codon preference of the Drosophila ribosomal protein 49 gene. Nucleic Acids Res. 1984 Jul 11;12(13):5495–5513. doi: 10.1093/nar/12.13.5495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Parkhurst S. M., Corces V. G. Forked, gypsys, and suppressors in Drosophila. Cell. 1985 Jun;41(2):429–437. doi: 10.1016/s0092-8674(85)80016-7. [DOI] [PubMed] [Google Scholar]
  24. Parkhurst S. M., Corces V. G. Interactions among the gypsy transposable element and the yellow and the suppressor of hairy-wing loci in Drosophila melanogaster. Mol Cell Biol. 1986 Jan;6(1):47–53. doi: 10.1128/mcb.6.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. 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]
  27. Rubin G. M., Kidwell M. G., Bingham P. M. The molecular basis of P-M hybrid dysgenesis: the nature of induced mutations. Cell. 1982 Jul;29(3):987–994. doi: 10.1016/0092-8674(82)90462-7. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Schwartz H. E., Lockett T. J., Young M. W. Analysis of transcripts from two families of nomadic DNA. J Mol Biol. 1982 May 5;157(1):49–68. doi: 10.1016/0022-2836(82)90512-5. [DOI] [PubMed] [Google Scholar]
  30. Steller H., Pirrotta V. Expression of the Drosophila white gene under the control of the hsp70 heat shock promoter. EMBO J. 1985 Dec 30;4(13B):3765–3772. doi: 10.1002/j.1460-2075.1985.tb04146.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Swaroop A., Paco-Larson M. L., Garen A. Molecular genetics of a transposon-induced dominant mutation in the Drosophila locus Glued. Proc Natl Acad Sci U S A. 1985 Mar;82(6):1751–1755. doi: 10.1073/pnas.82.6.1751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Varmus H. E., Quintrell N., Ortiz S. Retroviruses as mutagens: insertion and excision of a nontransforming provirus alter expression of a resident transforming provirus. Cell. 1981 Jul;25(1):23–36. doi: 10.1016/0092-8674(81)90228-2. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. 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]
  35. Zachar Z., Davison D., Garza D., Bingham P. M. A detailed developmental and structural study of the transcriptional effects of insertion of the Copia transposon into the white locus of Drosophila melanogaster. Genetics. 1985 Nov;111(3):495–515. doi: 10.1093/genetics/111.3.495. [DOI] [PMC free article] [PubMed] [Google Scholar]

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