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Unintegrated ribosomal genes in diploid and polytene tissues of Drosophila melanogaster

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Abstract

We have examined DNA from polytene salivary glands and diploid brains and imaginal discs of male and female larvae having one or two nucleolus organizers. DNA having an estimated molecular weight of 5×109 or greater was obtained by sucrose gradient sedimentation of gently prepared lysates. Hybridization of the gradient fractions with 3H-ribosomal RNA reveals that 42% of the ribosomal genes are found in DNA of lower molecular weight (approximately 3×108 daltons) in the salivary glands of every genotype examined. In the brains and imaginai discs, by contrast, all of the ribosomal genes are found in the high molecular weight peak except in females with one nucleolus organizer where 42% are found in lower molecular weight DNA, as in the salivary gland. Thus unintegrated genes are not an exclusive feature of polytene tissue, but can occur in diploid tissue as well in at least one genotype.

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References

  • Ashburner, M.: Function and structure of polytene chromosomes during insect development. Advanc. Insect Physiol. 7, 1–96 (1970)

    Google Scholar 

  • Aupert, J.P., Ryter, A., Schaeffer, P.: Comportement de l'ADN des bactéries et des spores au cours d'un cycle sporal chez B. subtilis. Ann. Inst. Pasteur 115, 889–1007 (1968)

    Google Scholar 

  • Beermann, W.: Chromomeres and genes. In: Developmental studies on giant chromosomes (W. Beermann, ed.). Springer: Berlin-Heidelberg-New York: 1972

    Google Scholar 

  • Berendes, H.D., Beermann, W.: Biochemical activity of interphase chromosomes (polytene chromosomes). In: Handbook of molecular cytology (A. Lima-de-Faria, ed.), pp. 501–519. Amsterdam and New York: North Holland Publishing Co. 1969

    Google Scholar 

  • Blumenfeld, M., Forrest, H.: Differential under-replication of satellite DNAs during Drosophila development. Nature (Lond.) New Biol. 239, 170–172 (1972)

    Google Scholar 

  • Bohnert, H.J., Schiller, B., Böhme, L., Sauer, H.W.: Circular DNA and rolling circles in nucleolar rDNA from mitotic nuclei of Physarum polycephalum. Europ. J. Biochem. 57, 361–369 (1975)

    Google Scholar 

  • Bridges, C.B.: Salivary chromosome maps. J. Hered. 26, 60–64 (1935)

    Google Scholar 

  • Burgi, E., Hershey, A.D.: Sedimentation rate as a measure of molecular weight of DNA. Biophys. J. 3, 309–321 (1963)

    Google Scholar 

  • Cooper, K.W.: Cytogenetic analysis of major heterochromatic elements (especially Xh and Y) in Drosophila melanogaster, and the theory of “heterochromatin”. Chromosoma (Berl.) 10, 535–588 (1959)

    Google Scholar 

  • Derksen, J., Berendes, H.D.: Polytene chromosome structure at the submicroscopic level. II. Length distribution of DNA molecules from polytene chromosomes of Drosophila melanogaster and D. hydei. Chromosoma (Berl.) 31, 468–477 (1970)

    Google Scholar 

  • Eberle, H., Lark, K.G.: Chromosome replication in Bacillus subtilis cultures growing at different rates. Proc. nat. Acad. Sci. (Wash.) 57, 95–101 (1967)

    Google Scholar 

  • Endow, S.A., Gall, J.G.: Differential replication of satellite DNA in polyploid tissues of Drosophila virilis. Chromosoma (Berl.) 50, 175–192 (1975)

    Google Scholar 

  • Gall, J.G.: Free ribosomal RNA genes in the macronucleus of Tetrahymena. Proc. nat. Acad. Sci. (Wash.) 71, 3078–3081 (1974)

    Google Scholar 

  • Gall, J.G., Cohen, E.H., Polan, M.L.: Repetitive DNA sequences in Drosophila. Chromosoma (Berl.) 33, 319–344 (1971)

    Google Scholar 

  • Gall, J.G., Rochaix, J.D.: The amplified ribosomal DNA of Dytiscid beetles. Proc. nat. Acad. Sci. (Wash.) 71, 1819–1823 (1974)

    Google Scholar 

  • Glover, D.M., White, R.L., Finnegan, D.J., Hogness, D.S.: Characterization of six cloned DNAs from Drosophila melanogaster, including one that contains the genes for rRNA. Cell 5, 149–157 (1975)

    Google Scholar 

  • Harford, A.G.: Ribosomal gene magnification in Drosophila: A chromosomal change. Genetics 78, 887–896 (1974)

    Google Scholar 

  • Heitz, E.: Die somatische Heteropyknose bei Drosophila melanogaster und ihre genetische Bedeutung. Z. Zellforsch. 20, 237–287 (1934a)

    Google Scholar 

  • Heitz, E.: Über α- und β-Heterochromatin sowie Konstanz und Bau der Chromomeren bei Drosophila. Biol. Zbl. 54, 588–609 (1934b)

    Google Scholar 

  • Hennig, W., Meer, B.: Reduced polyteny of ribosomal RNA cistrons in giant chromosomes of Drosophila hydei. Nature (Lond.) New Biol. 233, 70–72 (1971)

    Google Scholar 

  • Hourcade, D., Dressler, D., Wolfson, J.: The amplification of ribosomal RNA genes involves a rolling circle intermediate. Proc. nat. Acad. Sci. (Wash.) 70, 2926–2930 (1973)

    Google Scholar 

  • Kavenoff, R.: Characterization of the Bacillus subtilis W23 genome by sedimentation. J. molec. Biol. 72, 801–806 (1972)

    Google Scholar 

  • Kavenoff, R., Zimm, B.: Chromosome-sized DNA molecules from Drosophila. Chromosoma (Berl.) 41, 1–27 (1973)

    Google Scholar 

  • Klotz, L.C., Zimm, B.H.: Size of DNA determined by viscoelastic measurements: Results on bacteriophages, Bacillus subtilis and Escherichia coli. J. molec. Biol. 72, 779–800 (1972)

    Google Scholar 

  • Laird, C.D.: DNA of Drosophila chromosomes. Ann. Rev. Genet. 7, 177–204 (1973)

    Google Scholar 

  • Miller, O.L., Jr., Beatty, B.R.: Extrachromosomal nucleolar genes in amphibian oocytes. Genetics 61, Suppl. 133–143 (1969)

    Google Scholar 

  • Mulder, M.P., Duijn, P. van, Gloor, H.J.: The replicative organization of DNA in polytene chromosomes of Drosophila hydei. Genetica's-Gravenhage 39, 385–428 (1968)

    Google Scholar 

  • Nicoletti, B., Lindsley, D.L.: Translocations between the X and Y chromosomes of Drosophila melanogaster. Genetics 45, 1705–1722 (1960)

    Google Scholar 

  • Peacock, W.J., Brutlag, D., Goldring, E., Appels, R., Hinton, C.W., Lindsley, D.L.: The organization of highly repeated DNA sequences in Drosophila melanogaster. Cold Spr. Harb. Symp. quant. Biol. 33, 405–416 (1973)

    Google Scholar 

  • Prescott, D.M., Bostock, C.J., Murti, K.G., Lauth, M.R., Gamow, E.: DNA of ciliated protozoa; I. Electron microscopic and sedimentation analyses of macronuclear and micronuclear DNA of Stylonychia mytilus. Chromosoma (Berl.) 34, 355–366 (1971)

    Google Scholar 

  • Ritossa, F.M., Atwood, K.C., Spiegelman, S.: A molecular explanation of the bobbed mutants of Drosophila as partial deficiencies of “ribosomal” DNA. Genetics 54, 819–834 (1966)

    Google Scholar 

  • Ritossa, F., Malva, C., Boncinelli, E., Graziani, F., Polito, L.: The first steps of magnification of DNA complementary to ribosomal RNA in Drosophila melanogaster. Proc. nat. Acad. Sci. (Wash.) 68, 1580–1584 (1971)

    Google Scholar 

  • Ritossa, F.M., Spiegelman, S.: Localization of DNA complementary to ribosomal RNA in the nucleolar organizer region of Drosophila melanogaster. Proc. nat. Acad. Sci. (Wash.) 53, 737–745 (1965)

    Google Scholar 

  • Robb, J.A.: Maintenance of imaginal discs of Drosophila melanogaster in chemically defined media. J. Cell Biol. 41, 876–885 (1969)

    Google Scholar 

  • Rochaix, J.D., Bird, A.P.: Circular ribosomal DNA and ribosomal DNA replication in somatic amphibian cells. Chromosoma (Berl.) 52, 317–327 (1975)

    Google Scholar 

  • Rochaix, J.D., Bird, A., Bakken, A.: Ribosomal RNA gene amplification by rolling circles. J. molec. Biol. 87, 473–487 (1974)

    Google Scholar 

  • Rudkin, G.T.: Nonreplicating DNA in Drosophila. Genetics 61, Suppl. 227–238 (1969)

    Google Scholar 

  • Schalet, A., Lefevre, G., Jr.: The localization of “ordinary” sex-linked genes in section 20 of the polytene X chromosome of Drosophila melanogaster. Chromosoma (Berl.) 44, 183–202 (1973)

    Google Scholar 

  • van der Schans, G.P., Aten, B.T., Blok, J.: Determination of molecular weight distribution of DNA by means of sedimentation in a sucrose gradient. Analyt. Biochem. 32, 14–30 (1969)

    Google Scholar 

  • Schweber, M.S.: The satellite bands of the DNA of Drosophila virilis. Chromosoma (Berl.) 44, 371–382 (1974)

    Google Scholar 

  • Spear, B.B.: The genes for ribosomal RNA in diploid and polytene chromosomes of Drosophila melanogaster. Chromosoma (Berl.) 48, 159–179 (1974)

    Google Scholar 

  • Spear, B.B., Gall, J.G.: Independent control of ribosomal gene replication in polytene chromosomes of Drosophila melanogaster. Proc. nat. Acad. Sci. (Wash.) 70, 1359–1363 (1973)

    Google Scholar 

  • Tartof, K.D.: Increasing the multiplicity of ribosomal RNA genes in Drosophila melanogaster. Science 171, 294–297 (1971)

    Google Scholar 

  • Tartof, K.D.: Regulation of ribosomal RNA gene multiplicity in Drosophila melanogaster. Genetics 73, 57–71 (1973)

    Google Scholar 

  • Vermeulen, C.W., Atwood, K.C.: The proportion of DNA complementary to ribosomal RNA in Drosophila melanogaster. Biochem. biophys. Res. Commun. 19, 221–226 (1965)

    Google Scholar 

  • Vogt, W.M., Braun, R.: The structure of ribosomal DNA in Physarum polycephalum. J. molec. Biol. (in press, 1976)

  • Wolstenholme, D.R., Dawid, I.G., Ristow, H.: An electron microscope study of DNA molecules from Chironomus tentans and Chironomus thummi. Genetics 60, 759–770 (1968)

    Google Scholar 

  • Yoshikawa, H.: Chromosomes in Bacillus subtilis spores and their segretation during germination. J. Bact. 95, 2282–2292 (1968)

    Google Scholar 

  • Zuchowski, C., Harford, A.G.: On the chromosomal integration of disproportionately replicated ribosomal genes in Drosophila melanogaster. Biophys. J. 16, 226a (1976)

  • Zuchowski, C., Harford, A.G.: Ribosomal genes not integrated into chromosomal DNA in Drosophila melanogaster. Chromosoma (Berl.) 58, 219–234 (1976)

    Google Scholar 

Download references

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  1. Division of Cell and Molecular Biology, State University of New York at Buffalo, 14214, Buffalo, N.Y., USA

    Christine I. Zuchowski & A. Gayler Harford

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  1. Christine I. Zuchowski
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  2. A. Gayler Harford
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Zuchowski, C.I., Harford, A.G. Unintegrated ribosomal genes in diploid and polytene tissues of Drosophila melanogaster . Chromosoma 58, 235–246 (1976). https://doi.org/10.1007/BF00292089

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  • DOI: https://doi.org/10.1007/BF00292089

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