Summary
We examined P factor induced mutations of the Zw gene of Drosophila melanogaster in order to learn more about the site specificity of such mutations. Approximately 70000 chromosomes were screened using a powerful positive selection scheme. As only two mutants were discovered, Zw is a “cold spot” for transposable element insertion. One mutation involved a complex P element associated chromosomal rearrangement which was used to define the orientation of the gene with respect to the centromere of the X chromosome. The second mutation was either a simple, non-dysgenically induced point mutation or a very unstable insertion.
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Aquadro CF, Jennings RM, Bland MM, Laurie-Ahlberg CC, Langley CJ (1984) Patterns of naturally occurring DNA sequence variation, activity variation and linkage disequilibrium in the dopa decorboxylase region of Drosophila melanogaster. Genetics 107:S3
Bewley JC, Lucchesi JC (1975) Lethal effects of low and “null” activity alleles of 6-phosphogluconate dehydrogenase in Drosophila melanogaster. Genetics 79:451–466
Bingham PM, Levis R, Rubin GM (1981) Cloning of DNA sequences form the white locus of D. melanogaster by a novel and general method. Cell 25:693–704
Bingham PM, Kidwell MB, Rubin GM (1982) The molecular basis of P-M hybrid dysgenesis: the role of the P element, a P-strainspecific transposon family. Cell 29:995–1004
Blackman RK, Grimaila R, Macy M, Koehler D, Gelbar WM (1987) Mobilization of hobo elements residing within the decapentaplegic gene complex: suggestion of a new hybrid dysgenesis is system in Drosophila melanogaster. Cell 49:497–505
Bonner JJ, Pardue ML (1976) Ecdysone-stimulated RNA synthesis in imaginal discs of Drosophila melanogaster: assay by in situ hybridization. Chromosoma 58:87–99
Bregliano JC, Kidwell MG (1983) Hybrid dysgenesis determinants. In: Shapiro JA (ed) Mobile genetic elements. Academic Press, New York, pp 363–410
Chang D-Y, Wisely B, Huang S-M, Voelker RA (1986) Molecular cloning of suppressor of sable, a Drosophila melanogaster transposon-mediated suppressor. Mol Cell Biol 6:1520–1528
Davis PS, Shen MW, Judd BH (1987) Asymmetrical pairings of transposons in and proximal to the white locus of Drosophila account for four classes of regularly occurring exchange products. Proc Natl Acad Sci USA 84:174–178
Doring H-P, Freeling S, Hake S, Johns M, Kunze R, Merckelbach A, Salamini F, Starlinger P (1984) A Ds mutation of the AdhI gene in Zea Mays L. Mol Gen Genet 183:199–204
Eeken JCJ, Sobels FH (1986) The effect of X-irradiation and formaldehyde treatment of spermatogonia on the reversion of an unstable, P-element insertion mutation in Drosophila melanogaster. Mutat Res 175:61–65
Engels WR (1983) The P family of transposable elements in Drosophila. Annu Rev Genet 17:315–344
Engels WR (1984) A trans-acting product needed for P factor transposition in Drosophila. Science 226:1194–1196
Engels WR, Preston CR (1981) Identifying P factors in Drosophila by means of chromosome breakage hotspots. Cell 26:421–428
Enquist L, Sternberg N (1980) In vitro packaging of lambda Dam vectors and their use in cloning DNA fragments. Methods Enzymol 68:281–298
Feinberg AP, Vogelstein B (1983) A technique for radiolabelling DNA restriction endonuclease fragment to high specific activity. Anal Biochem 132:6–13
Finnegan DJ, Fawcett DH (1986) Transposable elements in Drosophila melanogaster. In: Maclean N (ed) Oxford surveys in eukaryotic genes, vol 3. Oxford University Press, London, pp 1–62
Frischauf A-M, Lehrach H, Poustka A, Murray N (1983) Lambda replacement vectors carrying polylinker sequences. J Mol Biol 170:827–842
Ganguly R, Ganguly N, Manning JE (1985) Isolation and characterization of the glucose-6-phosphate dehydrogenase gene of Drosophila melanogaster. Gene 35:91–101
Geer BW, Bowman JT, Simons JR (1974) The pentose shunt in wild-type and glucose-6-phosphate dehydrogenase deficient Drosophila melanogaster. J Exp Zool 187:77–86
Goldberg ML, Paro R, Gehring WJ (1982) Molecular cloning of the white locus region of Drosophila melanogaster using a large transposable element. EMBO J 1:93–98
Golubovskii MD, Voloshina MA, Zakharov IK, Yurchenko NN (1986) Interaction of mobile elements P and mog3 in Drosophila melanogaster: a genetic aspect. Genetika 22:2452–2458
Gvozdev VA, Gerasimova TI, Birstein VJ (1974) Inactivation of 6-phosphogluconate dehydrogenase structural gene of Drosophila melanogaster caused by translocation of heterochromatin. Mol Gen Genet 130:251–260
Gvozdev VA, Gostimsky TI, Gerasimova TI, Gubrovskaya EI, Braslavskaya O Yu (1975) Fine genetic structure of the 2D32F5 region of the X-chromosome of Drosophila melanogaster. Mol Gen Genet 141:269–275
Gvozdev VA, Gerasimova TI, Kogan GL, Rosovsky JM (1977) Investigations of the organization of genetic loci in Drosophila melanogaster: lethal mutations affecting 6-phosphogluconate dehydrogenase and their suppression. Mol Gen Genet 153:191–198
Hayward WA, Neel B, Astrin S (1981) Activation of cellular one genes by promoter insertion in ALV-induced lymphoid leukosis. Nature 290:475–479
Hohn B (1980) In vitro packaging of lambda and cosmid DNA. Methods Enzymol 68:299–309
Hughes MB, Lucchesi JC (1978) Dietary rescue of a lethal “null” activity allele of 6-phosphogluconate dehydrogenase in Drosophila melanogaster. Biochem Genet 16:469–475
Karn J, Brenner S, Barnett L, Cesareni G (1980) Novel bacteriophage lambda cloning vector. Proc Natl Acad Sci USA 77:5172–5176
Kidwell MG (1985) Hybrid dysgenesis in Drosophila melanogaster: nature and inheritance of P element regulation. Genetics 111:337–350
Kidwell MG, Sang HM (1986) Hybrid dysgenesis in Drosophila melanogaster: synthesis of RP strains by chromosomal contamination. Genet Res Camb 47:181–185
Langer-Safer PR, Levine M, Ward DC (1982) Immunological method for mapping genes on Drosophila polytene chromosomes. Proc Natl Acad Sci USA 79:4381–4385
Levis R, Collins M, Rubin GM (1982) FB elements are the common basis for the instability of the wDZL and we Drosophila mutations. Cell 30:551–565
Levis R, O'Hare K, Rubin GM (1984) Effects of transposable element insertions on RNA encoded by the white gene of Drosophila. Cell 38:471–481
Lindsley D, Grell E (1968) Genetic variations of Drosophila melanogaster. Carnegie Inst Wash Publ No. 627
Margulies L, Briscoe DI, Wallace SS (1986) The relationship between radiation-induced and transposon-induced genetic damage during Drosophila oogenesis. Mutat Res 162:55–68
Merriam JR (1968) FM7: first multiple seven. Drosophila Inf Serv 43:64
Nero D (1986) The pentose phosphate shunt in Drosophila melanogaster: studies on dysgenic mutants of glucose-6-phosphate dehydrogenase and the coordinate control of glucose-6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase. PhD Thesis, Cornell University, Ithaca, New York
Nicoletti B (1959) An efficient method for salivary-gland-chromosome preparations. Drosophila Inf Serv 33:181–182
O'Hare K, Rubin GM (1983) Structure of P transposable elements and their sites of insertion in the Drosophila melanogaster genome. Cell 34:25–35
O'Hare K, Murphy C, Levis R, Rubin GM (1984) DNA sequence of the white locus of Drosophila melanogaster. J Mol Biol 180:437–455
Parkhurst SM, Corces GV (1987) Developmental expression of Drosophila melanogaster retrovirus-like transposable elements. EMBO J 6:419–424
Rigby PWJ, Dieckmann M, Rhodes C, Berg P (1977) Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase. J Mol Biol 113:237–251
Rubin GM (1983) Dispersed repetitive DNAs in Drosophila. In: Shapiro JA (ed) Mobile genetic elements. Academic Press, New York, pp 324–362
Rubin GM, Kidwell MG, Bingham PM (1982) The molecular basis of P-M hybrid dysgenesis: the nature of induced mutations. Cell 29:987–994
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain termination inhibitors. Proc Natl Acad Sci USA 74:5463–5467
Searles KK, Jokerst RS, Bingham PM, Voelker RA, Greenleaf AL (1982) Molecular cloning of sequences from a Drosophila RNA polymerase II locus by P element transposon tagging. Cell 31:585–592
Shafer U (1986) Genes for male-specific transcripts in Drosophila melanogaster. Mol Gen Genet 202:219–225
Simmons JH, Lim JK (1980) Site specificity of mutations arising in dysgenic hybrids of Drosophila melanogaster. Proc Natl Acad Sci USA 77:6042–6046
Simon JA, Sutton CA, Lobell RB, Glaser RL, Lis JT (1985) Determinants of heat shock-induced chromosome puffing. Cell 40:805–817
Streck RD, MacGaffey JE, Beckendorf SK (1986) The structure of hobo transposable elements and their insertion sites. EMBO J 5:3615–3623
Tsubota S, Ashburner M, Schedl P (1985) P-element-induced control mutations at the τ gene of Drosophila melanogaster. Mol Cell Biol 5:2567–2574
Williamson VM, Young ET, Ciriacy M (1981) Transposable elements associated with constitutive expression of yeast alcohol dehydrogenase 11. Cell 23:605–614
Woodruff RC, Blount JL, Thompson JN (1987) Hybrid dysgenesis in D. melanogaster is not a general release mechanism for DNA transpositions. Science 237:1206–1208
Yannisch-Perron C, Vieira J, Messing J (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103–119
Yannopoulos G, Staematis N, Monastirioti M, Hatsopoulos P, Louis C (1987) Hobo is responsible for the induction of hybrid dysgenesis by strains of Drosophila melanogaster bearing the male recombination factor 23.5MRF. Cell 49:487–495
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Communicated by B.H. Judd
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Nero, D., Bowditch, N., Pickert, S. et al. A genetic and molecular analysis of P-induced mutations at the glucose-6-phosphate dehydrogenase locus in Drosophila melanogaster . Mol Gen Genet 219, 429–438 (1989). https://doi.org/10.1007/BF00259616
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DOI: https://doi.org/10.1007/BF00259616