Skip to main content
Log in

Ribosomal genes not integrated into chromosomal DNA in Drosophila melanogaster

  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

DNA obtained by a gentle lysis procedure from adult Drosophila melanogaster was analyzed by sucrose gradient sedimentation. The major portion of the DNA has an estimated weight of at least 5–10×109 daltons. All of the ribosomal genes are present in this high molecular weight DNA in adult males with one nucleolus organizer or in adult females with two nucleolus organizers as shown by hybridizing fractions of the gradient with ribosomal RNA. In female adults with one nucleolus organizer instead of the usual two, 68% of the ribosomal genes are found in high molecular weight DNA and 32% are found in DNA of smaller size (∼3×108 daltons). We propose that these latter genes are not integrated into the DNA of the chromosome.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anagnostopoulos, C., Spizizen, J.: Requirements for transformation in Bacillus subtilis. J. Bact. 81, 741–746 (1961)

    Google Scholar 

  • Blamire, J., Cryer, D.R., Finkelstein, D.B., Marmur, J.: Sedimentation properties of yeast nuclear and mitochondrial DNA. J. molec. Biol. 67, 11–24 (1972)

    Google Scholar 

  • Bohnert, H.J., Schiller, B., Bohme, 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 

  • Boncinelli, E., Graziani, F., Polito, L., Malva, C., Ritossa, F.: rDNA magnification at the bobbed locus of the Y chromosome in Drosophila melanogaster. Cell Differentiation 1, 133–142 (1972)

    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 

  • Doane, W.W.: Drosophila. In: Methods in developmental biology (F.H. Wilt and N.K. Wessels, eds.), pp. 219–244 (1967)

  • Freifelder, D.: Molecular weights of coliphages and coliphage DNA: IV. Molecular weights of DNA from bacteriophage T4, T5, and T7 and the general problem of determination of M. J. molec. Biol. 54, 567–577 (1970)

    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., 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 

  • Graziani, F., Boncinelli, E., Malva, C., Gargano, S.: Mutual regulation of magnified bobbed loci in Drosophila melanogaster. Molec. gen. Genet. 134, 307–311 (1974)

    Google Scholar 

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

    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 

  • Krider, H.M., Levine, B.I.: Studies on the mutation abnormal oocyte and its interaction with the ribosomal DNA of Drosophila melanogaster. Genetics 81, 501–513 (1975)

    Google Scholar 

  • Levin, D., Hutchinson, F.: Neutral sucrose sedimentation of very large DNA from Bacillus subtilis: I. Effect of random double-strand breaks and centrifuge speed on sedimentation. J. molec. Biol. 75, 455–578 (1973)

    Google Scholar 

  • Lindsley, D.L., Grell, E.H.: Genetic variations of Drosophila melanogaster Carnegie Inst. Washington Publ. 627 (1968)

  • Marrakechi, M.: Etude d'un mutant bobbed ayant une quantité normale d'ADN ribosomal. Molec. gen. Genet. 135, 213–229 (1974)

    Google Scholar 

  • Marrakechi, M., Prud'homme, N.: A study of bobbed mutants induced by ethylmethane-sulfonate in Drosophila melanogaster. Biochem. biophys. Res. Commun. 43, 273–277 (1971)

    Google Scholar 

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

    Google Scholar 

  • Nomoto, M., Narahashi, Y.: A proteolytic enzyme of Streptomyces griseus: Purification of a protease of Streptomyces griseus. J. Biochem. 46, 653–667 (1959)

    Google Scholar 

  • Petes, T.D., Fangman, W.L.: Sedimentation properties of yeast chromosomal DNA. Proc. nat. Acad. Sci. (Wash.) 69, 1188–1191 (1972)

    Google Scholar 

  • Prescott, D., Murti, K.G.: Chromosome structure in ciliated protozoans. Cold Spr. Harb. Symp. quant. Biol. 38, 609–618 (1973)

    Google Scholar 

  • Procunier, J.D., Williamson, J.H.: Temperature-sensitive bobbed mutants in Drosophila melanogaster. Develop. Biol. 39, 198–209 (1974)

    Google Scholar 

  • Ritossa, F.M.: Unstable redundancy of genes for ribosomal RNA. Proc. nat. Acad. Sci. (Wash.) 60, 509–516 (1968a)

    Google Scholar 

  • Ritossa, F.M.: Nonoperative DNA complementary to ribosomal RNA. Proc. nat. Acad. Sci. (Wash.) 59, 1124–1131 (1968b)

    Google Scholar 

  • Ritossa, F.: Crossing-over between X and Y chromosomes during ribosomal DNA magnification in Drosophila melanogaster. Proc. nat. Acad. Sci. (Wash.) 70, 1950–1954 (1973)

    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 nucleolus organizer region of Drosophila melanogaster. Proc. nat. Acad. Sci. (Wash.) 53, 737–745 (1965)

    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.P., Bakken, A.H.: Ribosomal RNA gene ampliciation by rolling circles. J. molec. Biol. 87, 473–487 (1974)

    Google Scholar 

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

    Google Scholar 

  • Shermoen, A.W., Kiefer, B.I.: Regulation in rDNA-deficient Drosophila melanogaster. Cell 4, 275–280 (1975)

    Google Scholar 

  • Sibatani, A.: Difference in the proportion of DNA specific to ribosomal RNA between adults and larvae of Drosophila melanogaster. Molec. gen. Genet. 114, 177–180 (1971)

    Google Scholar 

  • Snusted, D.P., Dean, D.S.: Genetics experiments with bacterial viruses. San Francisco: W.H. Freeman and Co. 1971

    Google Scholar 

  • Spear, B.B., Gall, J.G.: Independent control of ribosomal gene replication in polytene chromosomes of D. 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 

  • Tartof, K.D.: Unequal mitotic sister chromatid exchange as the mechanism of ribosomal RNA gene magnification. Proc. nat. Acad. Sci. (Wash.) 71, 1272–1276 (1974)

    Google Scholar 

  • Tartof, K.D., Perry, R.P.: The 5S RNA genes of Drosophila melanogaster. J. molec. Biol. 51, 171–183 (1970)

    Google Scholar 

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

  • Williamson, J.H., Procunier, J.D.: Disproportionately-replicated, nonfunctional rDNA in compound chromosomes of Drosophila melanogaster. Molec. gen. Genet. 139, 33–37 (1975)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zuchowski, C.I., Harford, A.G. Ribosomal genes not integrated into chromosomal DNA in Drosophila melanogaster . Chromosoma 58, 219–234 (1976). https://doi.org/10.1007/BF00292088

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00292088

Keywords

Navigation