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Interactions among modifiers of retrotransposon-induced alleles of the white locus of Drosophila melanogaster

Published online by Cambridge University Press:  14 April 2009

Leonard Rabinow
Affiliation:
The Biological Laboratories, Harvard University, 16 Divinity Ave., Cambridge, MA. 02138
James Birchler
Affiliation:
The Biological Laboratories, Harvard University, 16 Divinity Ave., Cambridge, MA. 02138
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Mutations in five loci that modify the phenotype of whiteapricot (wa), caused by the retrotransposon, copia, were examined in two-way combinations to determine whether their effects were additive or epistatic. All two-way combinations of mutations in these five loci, mottler of white (mw), suppressor of forked (su(f)), suppressor of white apricot (su(wa)), Enhancer of whiteapricot, (E(wa)) and Darkener of apricot (Doa), are additive in their effects on wa, implying that each second-site modifier locus affects a different process. Three other copia-induced mutations, HwUa, whd81b25 and ctns were also examined for responsiveness to mutations in these modifier loci. None clearly responded. Mutations associated with B104 insertions, including Gl, vgni, ctn and wric were also examined for responsiveness to mw mutations, which have specificity for this element as well. Both vgni and wric respond to mutations in mw. The former interaction demonstrates that mw is capable of interacting with B104 elements in loci other than white. The significance of the results with respect to the nature of second-site modifier loci is discussed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1990

References

Bender, W., Akam, M., Karch, F., Beachy, P. A., Peifer, M., Spierer, P., Lewis, E. B. & Hogness, D. S. (1983). Molecular genetics of the bithorax complex in Drosophila melanogaster. Science 221, 2329.CrossRefGoogle ScholarPubMed
Bingham, P. M. & Judd, B. H. (1981). Copy of the copia transposable element is very tightly linked to the wa allele at the white locus of D. melanogaster. Cell 25, 705711.CrossRefGoogle Scholar
Birchler, J. A. & Hiebert, J. C. (1989). Interaction of the Enhancer of white-apricot with transposable element alleles at the white locus in Drosophila melanogaster. Genetics 122, 129138.CrossRefGoogle ScholarPubMed
Birchler, J. A., Hiebert, J. C. & Rabinow, L. (1989). Interaction of the mottler of white with transposable element alleles at the white locus in Drosophila melanogaster. Genes and Development 3, 7384.CrossRefGoogle ScholarPubMed
Blochlinger, K., Bodmer, R., Jack, J., Jan, L. Y. & Jan, Y. N. (1988). Primary structure and expression of a product from cut, a locus involved in specifying sensory organ identity in Drosophila. Nature 333, 629635.CrossRefGoogle ScholarPubMed
Campuzano, S., Balcells, L., Villares, R., Carramolino, L., Garcia-Alonse, L. & Modolell, J. (1986). Excess function Hairy-wing mutations caused by gypsy and copia insertions within structural genes of the achaete-scute locus of Drosophila. Cell 44, 303312.CrossRefGoogle ScholarPubMed
Chang, D. Y., Wisely, B., Huang, S. M. & Voelker, R. A. (1986). Molecular cloning of suppressor of sable, a Drosophila melanogaster transposon-mediated suppressor. Molecular and Cellular Biology 6, 15201528.Google Scholar
Chou, T. B., Zachar, Z. & Bingham, P. M. (1987). Developmental expression of a regulatory gene is programmed at the level of splicing. EMBO Journal 6, 40954104.CrossRefGoogle ScholarPubMed
Clarke-Adams, C. D., Norris, D., Osley, M. A., Fassler, J. S. & Winston, F. (1988). Changes in histone gene dosage alter transcription in yeast. Genes and Development 2, 150159.CrossRefGoogle Scholar
Clarke-Adams, C. D. & Winston, F. (1987). The SPT6 gene is essential for growth and is required for δ-mediated transcription in Saccharomyces cerevisiae. Molecular and Cellular Biology 7, 679686.Google Scholar
Cullen, B. R., Lomedico, P. T. & Ju, G. (1984). Transcriptional interference in avian retroviruses – implications for the promoter insertion model of leukaemogenesis. Nature 307, 241245.CrossRefGoogle ScholarPubMed
Davis, P. S., Shen, M. W. & Judd, B. H. (1987). Asymmetrical pairings of transposons in and proximal to the white locus of Drosophila account for four classes of regularly occurring exchange products. Proceedings of the National Academy of Science, U.S.A. 84, 174178.CrossRefGoogle Scholar
Dorsett, D., Vigilanti, G. A., Rutledge, B. J. & Meselson, M. (1989). Alteration of hsp82 gene expression by the gypsy transposon and suppressor genes in Drosophila melanogaster. Genes and Development 3, 454468.CrossRefGoogle ScholarPubMed
Fassler, J. S. & Winston, F. (1988). Isolation and analysis of a novel class of suppressor of Ty insertion mutations in Saccharomyces cerevisiae. Genetics 118, 203212.CrossRefGoogle ScholarPubMed
Finnegan, D. J. & Fawcett, D. H. (1986). Transposable elements in Drosophila melanogaster, pp. 162 in Oxford Surveys on Eukaryotic Genes (ed. Maclean, N.). Oxford: Oxford University Press.Google Scholar
Flavell, A. J., Levis, R., Simon, M. A. & Rubin, G. M. (1981). The 5′ termini of RNAs encoded by the transposable element copia. Nucleic Acids Research 9, 62796291.CrossRefGoogle ScholarPubMed
Flavell, A. J., Ruby, S. W., Toole, J. J., Roberts, B. E. & Rubin, G. M. (1980). Translation and developmental regulation of RNA encoded by the eukaryotic transposable element copia. Proceedings of the National Academy of Science, U.S.A. 77, 71077111.CrossRefGoogle ScholarPubMed
Freund, R. & Meselson, M. (1984). LTR nucleotide sequence and specific insertion of the gypsy transposon. Proceedings of the National Academy of Science, U.S.A. 81, 44624464.CrossRefGoogle Scholar
Gehring, W. J. & Paro, R. (1980). Isolation of a hybrid plasmid with homologous sequences to a transposing element of Drosophila. Cell 19, 857904.CrossRefGoogle ScholarPubMed
Geyer, P. K., Green, M. M. & Corces, V. G. (1988). Mutant gene phenotypes mediated by a Drosophila melanogaster retrotransposon require sequences homologous to mammalian enhancers. Proceedings of the National Academy of Science, U.S.A. 85, 85938597.CrossRefGoogle ScholarPubMed
Geyer, P. K., Spana, C. & Corces, V. G. (1986). On the molecular mechanisms of gypsy-induced mutations at the yellow locus of Drosophila melanogaster. EMBO Journal 5, 26572662.CrossRefGoogle ScholarPubMed
Grandbastien, M. A., Spielmann, A. & Caboche, M. (1989). Tntl, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature 337, 376380.CrossRefGoogle Scholar
Green, M. M. (1959). Spatial and functional properties of pseudoalleles at the white locus in Drosophila melanogaster. Heredity 13, 303315.CrossRefGoogle Scholar
Jack, J. W. (1985). Molecular organization of the cut locus of Drosophila melanogaster. Cell 42, 869876.CrossRefGoogle ScholarPubMed
Johns, M. A., Mottinger, J. & Freeling, M. (1985). A low copy number, copia-like transposon in maize. EMBO Journal 4, 10931102.CrossRefGoogle ScholarPubMed
Kidd, S. & Young, M. W. (1986). Transposon dependent mutant phenotypes at the Notch locus of Drosophila. Nature 323, 8991.CrossRefGoogle ScholarPubMed
Levis, R., O'Hare, K. & Rubin, G. M. (1984). Effects of transposable element insertions on RNA encoded by the white gene of Drosophila. Cell 38, 471481.CrossRefGoogle Scholar
Levy, D. E., Lerner, R. A. & Wilson, M. C. (1982). A genetic locus regulates the expression of tissue-specific mRNAs from multiple transcription units. Proceedings of the National Academy of Science, U.S.A. 79, 58235827.CrossRefGoogle ScholarPubMed
Levy, D. E., Lerner, R. A. & Wilson, M. C. (1985). The GV-1 locus coordinately regulates the expression of multiple endogenous murine retroviruses. Cell 41, 289299.CrossRefGoogle ScholarPubMed
Lindsley, D. L. & Grell, E. H. (1968). Genetic Variations of Drosophila melanogaster. Carnegie Institute of Washington, Publication no. 627.Google Scholar
Mazo, A. M., Mizrokhi, L. J., Karavanov, A. A., Sedkov, Y. A., Krichevskaja, A. A. & Ilyin, Y. V. (1989). Suppression in Drosophila, su(Hw) and su(f) gene products interact with a region of gypsy (mdg4) regulating its transcriptional activity. EMBO Journal 8, 903911.CrossRefGoogle ScholarPubMed
Modolell, J., Bender, W. & Meselson, M. (1983). Drosophila melanogaster mutations suppressible by the suppressor of Hairy-wing are insertions of a 7·3 kilobase mobile element. Proceedings of the National Academy of Science, U.S.A. 80, 16781682.CrossRefGoogle ScholarPubMed
Morishita, K., Parker, D. S., Mucenski, M. L., Jenkins, N. A., Copeland, N. G. & Ihle, J. N. (1988). Retroviral activation of a novel gene encoding a zinc finger protein in IL-3-dependent myeloid leukemia cell lines. Cell 54, 831840.CrossRefGoogle ScholarPubMed
Morse, B., Rothberg, P. G., South, V. J., Spandorfer, J. M. & Astrin, S. M. (1988). Insertion mutagenesis by a Line-1 sequence in a human breast carcinoma. Nature 333, 8790.CrossRefGoogle Scholar
Mount, S. M. & Rubin, G. M. (1985). Complete nucleotide sequence of the Drosophila transposable element copia, homology between copia and retroviral proteins. Molecular and Cellular Biology 7, 16301638.Google Scholar
Mount, S. M., Green, M. M. & Rubin, G. M. (1988). Partial revertants of the transposable element-associated suppressible allele whiteapricot in Drosophila melanogaster. Genetics 118, 221234.CrossRefGoogle ScholarPubMed
Neigeborn, L., Celenza, J. L. & Carlson, M. (1987). SSN20 is an essential gene with mutant alleles that suppress defects in SUC2 transcription in Saccharomyces cerevisiae. Molecular and Cellular Biology 7, 672678.Google ScholarPubMed
Nusse, R. (1986). The activation of cellular oncogenes by retroviral insertion. Trends in Genetics 2, 244247.CrossRefGoogle Scholar
O'Hare, K., Levis, R. & Rubin, G. M. (1983). Transcription of the white locus in Drosophila melanogaster. Proceedings of the National Academy of Science, U.S.A. 80, 69176921.CrossRefGoogle ScholarPubMed
O'Hare, K., Murphy, C, Levis, R. & Rubin, G. M. (1984). DNA sequence of the white locus of Drosophila melanogaster. Journal of Molecular Biology 180, 437455.CrossRefGoogle ScholarPubMed
Parkhurst, S. M. & Corces, V. G. (1985). forked, gypsys and suppressors in Drosophila melanogaster. Cell 41, 429437.CrossRefGoogle Scholar
Parkhurst, S. M. & Corces, V. G. (1986 a). Interactions among the gypsy transposable element and the yellow and suppressor of Hairy-wing loci in Drosophila melanogaster. Molecular and Cellular Biology 6, 4753.Google ScholarPubMed
Parkhurst, S. M. & Corces, V. G. (1986 b). Mutations at the suppressor-of-forked locus increase the accumulation gypsy encoded transcripts in Drosophila melanogaster. Molecular and Cellular Biology 6, 22712274.Google ScholarPubMed
Parkhurst, S. M. & Corces, V. G. (1987). Developmental expression of Drosophila melanogaster retrovirus-like transposable elements. EMBO Journal 6, 419424.CrossRefGoogle ScholarPubMed
Parkhurst, S. M., Harrison, D. A., Remington, M. P., Spana, C., Kelley, R. L., Coyne, R. S. & Corces, V. G. (1988). The Drosophila su(Hw) gene, which controls the phenotypic effect of the gypsy transposable element, encodes a DNA-binding protein. Genes and Development 2, 12051215.CrossRefGoogle ScholarPubMed
Peifer, M. & Bender, W. (1988). Sequences of the gypsy transposon of Drosophila necessary for its effects on adjacent genes. Proceedings of the National Academy of Science, U.S.A. 85, 96509654.CrossRefGoogle ScholarPubMed
Pirrotta, V. & Brockl, C. (1984). Transcription of the Drosophila white locus and some of its mutants. EMBO Journal 3, 563568.CrossRefGoogle ScholarPubMed
Rabinow, L. & Birchler, J. A. (1989). A dosage-sensitive modifier of retrotransposon induced alleles of the Drosophila white locus. EMBO Journal 8, 879889.CrossRefGoogle ScholarPubMed
Rubin, G. R., Kidwell, M. G. & Bingham, P. M. (1982). The molecular basis of P-M hybrid dysgenesis, The nature of induced mutations. Cell 29, 987994.CrossRefGoogle ScholarPubMed
Rutledge, B. J., Mortin, M. A., Schwarz, E., Thierry-Mieg, D. & Meselson, M. (1988). Genetic interactions of modifier genes and modifiable alleles in Drosophila melanogaster. Genetics 119, 391397.CrossRefGoogle ScholarPubMed
Sang, H. M., Pelisson, A., Bucheton, A. & Finnegan, D. J. (1984). Molecular lesions associated with white gene mutations induced by I-R hybrid dysgenesis in Drosophila melanogaster. EMBO Journal 3, 30793085.CrossRefGoogle Scholar
Scherer, G., Tschudl, C., Perera, J., Delius, H. & Pirrotta, V. (1982). B104, a new dispersed repeated gene family in Drosophila melanogaster and its analogies with retroviruses. Journal of Molecular Biology 157, 435451.CrossRefGoogle ScholarPubMed
Schwartz, H. E., Lockett, T. J. & Young, M. W. (1982). Analysis of transcripts from two families of nomadic DNA. Journal of Molecular Biology 157, 4968.CrossRefGoogle ScholarPubMed
Searles, L. L. & Voelker, R. A. (1986). Molecular characterization of the Drosophila melanogaster vermilion locus and its suppressible alleles. Proceedings of the National Academy of Science, U.S.A. 83, 404408.CrossRefGoogle ScholarPubMed
Strand, D. J. & McDonald, J. F. (1989). Insertion of a copia element 5′ to the Drosophila melanogaster alcohol dehydrogenase gene (adh) is associated with altered developmental and tissue-specific patterns of expression. Genetics 121, 787794.CrossRefGoogle Scholar
Spana, C., Harrison, D. A. & Corces, V. G. (1988). The Drosophila malanogaster suppressor-of-Hairy-wing protein binds to specific sequences of the gypsy retrotransposon. Genes and Development 2, 14141423.CrossRefGoogle Scholar
Swaroop, A., Paco-Larson, M. L. & Garen, A. (1985). Molecular genetics of a transposon-induced dominant mutation in the Drosophila locus Glued. Proceedings of the National Academy of Science, U.S.A. 82, 17511755.CrossRefGoogle ScholarPubMed
Traina-Dorge, V. L., Carr, J. K., Bailey-Wilson, J. E., Elston, R. C, Taylor, B. A. & Cohen, J. C. (1985). Cellular genes in the mouse regulate in trans the expression of endogenous mouse mammary tumour viruses. Genetics 111, 597615.CrossRefGoogle Scholar
Voytas, D. F. & Ausubel, F. M. (1988). A copia-like transposable element family in Arabidopsis thaliana. Nature 336, 242244.CrossRefGoogle ScholarPubMed
Williams, J. A. & Bell, J. B. (1988). Molecular organization of the vestigial region in Drosophila melanogaster. EMBO Journal 7, 13551363.CrossRefGoogle ScholarPubMed
Winston, F., Chaleff, D. T., Valent, B. & Fink, G. R. (1984 a). Mutations affecting Ty-mediated expression of the HIS-4 gene of Saccharomyces cerevisiae. Genetics 107, 179197.CrossRefGoogle Scholar
Winston, F., Dollard, C, Malone, E. A., Clare, J., Kapakos, J. G., Farabough, P. & Minehart, P. L. (1987). Three genes are required for trans-activation of Ty transcription in yeast. Genetics 115, 649656.CrossRefGoogle ScholarPubMed
Winston, F., Durbin, K. J. & Fink, G. R. (1984 b). The SPT3 gene is required for normal transcription of Ty elements in S. cerevisiae. Cell 39, 675682.CrossRefGoogle ScholarPubMed
Zachar, Z. & Bingham, P. M. (1982). Regulation of white locus expression, The structure of mutant alleles at the white locus in Drosophila melanogaster. Cell 30, 529541.CrossRefGoogle ScholarPubMed
Zachar, Z., Chou, T. B. & Bingham, P. M. (1987). Evidence that a regulatory gene autoregulates splicing of its transcript. EMBO Journal 6, 41054111.CrossRefGoogle ScholarPubMed
Zachar, Z., Davison, D., Garza, D. & Bingham, P. M. (1985). A detailed developmental and structural study of the transcriptional effects of insertion of the copia transposon into the white locus of Drosophila melanogaster. Genetics 111, 495515.CrossRefGoogle ScholarPubMed