Abstract
We report here the genetical and X chromosome rDNA molecular study of two Drosophila melanogaster Oregon R lines. These lines differ extensively in the degree of resistance of the females both to the lethal effect of an increased temperature and to that of Bacillus thuringiensis beta-exotoxin, which is an inhibitor of the nucleolar RNA polymerase. The 3B line, whose females are resistant, came from an Oregon R population subjected over several generations to increased temperature, 28°C or over, while the other line is derived from the initial stock. Twofold variation was observed in the total number of ribosomal genes between the two lines. This variation applied to most ribosomal units, including the active ones. Variations among X chromosome rDNA content in a wild type population have thus been revealed using tests of resistance to the Bacillus thuringiensis beta-exotoxin. Additive variations in specific unit types between the two lines indicate that modifications to the rDNA content are not rare events.
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Appels, R, and Hilliker, A J. 1982. The cytogenetic boundaries of the rDNA region within heterochromatin of the X chromosome of Drosophila melanogaster and their relation to male meiotic pairing site. Genet Res Camb, 39, 149–156.
Beebee, T J C, and Bond, R P M. 1973. Effect of the exotoxin of Bacillus thuringiensis on normal and ecdysone stimulated ribonucleic acid polymerase activity in intact nuclei from the fat-body of Sarcophaga bullata larvae. BiochemJ, 136, 1–7.
Birnboim, H C, and Doly, J. 1979. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucl Acid Res, 1, 1513–1523.
Cooper, K W. 1959. Cytogenetic analysis of major hetero-chromatic elements (especially Xh and Y) in Drosophila melanogaster and the theory of ‘heterochromatin’. Chromosoma, 10, 535–588.
Dutton, F L, and Krider, M M. 1984. Ribosomal RNA cistrons of X chromosomes clonally derived from D. melanogaster laboratory populations: redundancy, organization and stability. Genetics, 107, 405–421.
Endow, S A, and Glover, D M. 1979. Differential replication of ribosomal repeats in polytene nuclei of Drosophila. Cell, 17, 597–605.
England, P R, Stokes, H W, and Fankham, R. 1988. Clustering of rDNA containing type 1 insertion sequence in the distal nucleolus organizer of Drosophila melanogaster: implications for the coevolution of X and Y rDNA arrays. Genet Res Camb, 51, 209–215.
Ephrussi, B, and Beadle, G V. 1936. A technique of transplantation for Drosophila. Am Nat, 70, 218–225.
Gillings, M R, Frankham, R, Speirs, J, and Whalley, M. 1987. X-Y exchange and the coevolution of the X and Y rDNA arrays in Drosophila melanogaster. Genetics, 116, 241–251.
Hawley, R S, and Marcus, C H. 1989. Recombinational controls of rDNA redundancy in Drosophila. Ann Rev Genet, 23, 87–120.
Hawley, R S, and Tartof, K D. 1985. A two-stage model for the control of rDNA magnification. Genetics, 109, 691–700.
Jakubczack, J L, Xiong, Y, and Eickbush, H. 1990. Type I (Rl) and type II (R2) ribosomal DNA insertions of Drosophila melanogaster are retrotransposable elements closely related to those of Bombyx mori. J Mol Biol, 212, 37–52.
Kidd, S J, and Glover, D M. 1981. Drosophila melanogaster ribosomal DNA containing type II insertions is variably transcribed in different strains and tissues. J Mol Biol, 151, 645–662.
Lecadet, M M, and Dedonder, R. 1971. Biogenesis of the crystalline inclusion of Bacillus thuringiensis during sporulation. Eur J Biochem, 23, 282–294.
Lindsley, D L, and Grell, E H. 1968. Genetics variations of Drosophila melanogaster. Carnegie Institute of Washington Publication, 627.
Locker, D, and Prud'Homme, N. 1973. Etude de plusieurs facteurs faisant varier la fréquence de réversion au locus bobbed chez Drosophila melanogaster. Mol Gen Genet, 124, 1119.
Long, E O, and Dawid, I B. 1979. Expression of ribosomal DNA insertions in Drosophila melanogaster. Cell, 18, 1185–1196.
Long, E O, and Dawid, I B. 1980. Repeated genes in Eucaryotes. Ann Rev Biochem, 49, 727–764.
Long, E O, Rebbert, M L, and Dawid, I B. 1980. Structure and expression of ribosomal RNA genes of Drosophila melanogaster interrupted by type 2 insertions. Cold Spring Harbor Symp Quant Biol, 45, 667–672.
McConnel, E, and Richards, A G. 1959. The production by Bacillus thuringiensis Berliner of a heat-stable substance toxic for insects. Can J Microbiol, 5, 161–168.
MacKedonski, V V, Hadjiolov, A A, and Sebesta, K. 1972. Preferential in vivo inhibition of ribosomal ribonucleic acid synthesis in mouse liver by exotoxin of Bacillus thuringiensis. FEBS Lett, 21, 211–214.
Marcus, C H, Zitron, A E, Wright, D A, and Hawley, R S. 1986. Autosomal modifiers of the bobbed phenotype are a major component of the rDNA magnification paradox in Drosophila melanogaster. Genetics, 113, 305–319.
Paumard, S, and Bourgin-Rosenberg, M. 1981. Utilisation du surnageant de cultures de Bacillus thuringiensis dans une étude in vivo du fonctionnement de l'organisateur nucléolaire chez Drosophila melanogaster. C R Acad Sci Paris, 293, 257–260.
Paumard-Rigal, S, and Rosenberg-Bourgin, M. 1990. High temperature of development and selection of Bacillus thuringiensis supernatant-resistant females in a Drosophila melanogaster Oregon R strain. Genetica, 81, 215–228.
Peacock, W J, Appels, R, Endow, S, and Glover, D. 1981. Chromosomal distribution of the major insert in Drosophila melanogaster 28 S rRNA genes. Genet Res Camb, 37, 209–214.
Ritossa, F M. 1972. Procedure for magnification of lethal deletions of genes for ribosomal RNA. Nature New biol, 240, 109–111.
Ritossa, F. 1976. The bobbed locus. In: Genetics and Biology of Drosophila Vol. 1b: Ashburner, M. and Novitski, E. (eds) Academic Press, London, pp. 801–846.
Ritossa, F M, Atwood, K C, and Spiegelman, S. 1966. A molecular explanation of the bobbed mutants of Drosophila as partial deficiencies of “ribosomal” DNA. Genetics, 54, 819–834.
Ritossa, F M, and Spiegelman, S. 1965. Localization of DNA complementary to ribosomal RNA in the nucleolus organizer region of Drosophila melanogaster. Proc Natl Acad Sci, USA, 53, 737–745.
Roiha, H, Miller, J R, Woods, L C, and Glover, D M. 1981. Arrangements and rearrangements of sequences flanking the two types of rDNA insertions in Drosophila melanogaster. Nature, 290, 749–753.
Rosenberg-Bourgin, M, Paumard, S, and Contesse, G. 1988a. Comparative study of molecular characteristics of X and Y nucleolar organizers of various lines of Drosophila melanogaster. Biol Cell, 62, 201–209.
Rosenberg-Bourgin, M, Paumard, S, Bracone, A, and Contesse, G. 1988b. Comparison between the molecular characteristics and the potential activity of X and Y nucleolar organizers from various Drosophila melanogaster laboratory lines. Biol Cell, 64, 3–11.
Salzano, G, and Malva, C. 1984. Non-random loss of uninterrupted ribosomal DNA repeating units upon induction of bobbed mutation. J Mol Biol, 177, 189–200.
Sharp, Z D, Ghandi, V V, and Procunier, J D. 1983. X chromosome nucleolus organiser mutants which alter major type I repeat multiplicity in Drosophila melanogaster. Mol Gen Genet, 190, 438–443.
Spear, B B. 1974. The genes for ribosomal RNA in diploid and polytene chromosomes of Drosophila melanogaster. Chromosoma, 48, 159–179.
Tartof, K D. 1971. Increasing the multiplicity of ribosomal RNA genes in Drosophila melanogaster. Science, 171, 294–297.
Tartof, K D. 1973a. Regulation of ribosomal RNA gene multiplicity in Drosophila melanogaster. Genetics, 73, 57–71.
Tartof, K D. 1973b. Unequal sister chromatid exchange and disproportionate replication as mechanisms regulating ribosomal RNA gene redundancy. Cold Spring Harbor Symp Quant Biol, 38, 491–500.
Tartof, K D. 1974. Unequal mitotic sister chromatid exchange as the mechanism of ribosomal gene magnification. Proc Natl Acad Sci, USA, 71, 1272–1276.
Tartof, K D, and Dawid, T B. 1976. Similarities and differences in the structure of X and Y chromosomes rRNA genes of Drosophila. Nature, 263, 27–30.
Terracol, R. 1987. Differential magnification of rDNA gene types in bobbed mutants of Drosophila melanogaster. Mol Gene Genet, 208, 168–176.
Terracol, R, and Prud'Homme, N. 1986. Differential elimination of rDNA genes in bobbed mutants of Drosophila melanogaster. Mol Cell Biol, 6, 1023–1031.
Wahl, G M, Stern, M, and Stark, G R. 1979. Efficient transfer of large DNA fragments from agarose gels to diazobenzyl-oxymethyl-paper and rapid hybridization by using dextran sulfate. Proc Natl Acad Sci, USA, 76, 3683–3687.
Wellauer, P K, Dawid, I B, and Tartof, K D. 1978. X and Y chromosomal ribosomal DNA of Drosophila melanogaster. Comparison of spacers and insertions. Cell, 14, 269–278.
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Paumard-Rigal, S., Rosenberg-Bourgin, M. Increase in the resistance to the Bacillus thuringiensis supernatant effect in a Drosophila melanogaster wild type Oregon R line. Heredity 69, 539–546 (1992). https://doi.org/10.1038/hdy.1992.169
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DOI: https://doi.org/10.1038/hdy.1992.169