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Repetitive DNA sequences in Drosophila

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Abstract

The satellite DNAs of Drosophila melanogaster and D. virilis have been examined by isopycnic centrifugation, thermal denaturation, and in situ molecular hybridization. The satellites melt over a narrow temperature range, reassociate rapidly after denaturation, and separate into strands of differing buoyant density in alkaline CsCl. In D. virilis and D. melanogaster the satellites constitute respectively 41% and 8% of the DNA isolated from diploid tissue. The satellites make up only a minute fraction of the DNA isolated from polytene tissue. Complementary RNA synthesized in vitro from the largest satellite of D. virilis hybridized to the centromeric heterochromatin of mitotic chromosomes, although binding to the Y chromosome was low. The same cRNA hybridized primarily to the α-heterochromatin in the chromocenter of salivary gland nuclei. The level of hybridization in diploid and polytene nuclei was similar, despite the great difference in total DNA content. The centrifugation and hybridization data imply that the α-heterochromatin either does not replicate or replicates only slightly during polytenization. Similar but less extensive data are presented for D. melanogaster. — In D. melanogaster cRNA synthesized from total DNA hybridized to the entire chromocenter (α- and β-heterochromatin) and less intensely to many bands on the chromosome arms. The X chromosome was more heavily labeled than the autosomes. In D. virilis the X chromosome showed a similar preferential binding of cRNA copied from main peak sequences.—It is concluded that the majority of repetitive sequences in D. virilis and D. melanogaster are located in the α- and β-heterochromatin. Repetitive sequences constitute only a small percentage of the euchromatin, but they are widely distributed in the chromosomes. During polytenization the α-heterochromatin probably does not replicate, but some or all of the repetitive sequences in the β-heterochromatin and the euchromatin do replicate.

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References

  • Beermann, W.: Riesenchromosomen. Protoplasmatologia, vol. VI/D. Wien:Springer 1962.

    Google Scholar 

  • Berendes, H. D., Keyl, H. G.: Distribution of DNA in heterochromatin and euchromatin of polytene nuclei of Drosophila hydei. Genetics 57, 1–13 (1967).

    Google Scholar 

  • Bodenstein, D.: The postembryonic development of Drosophila. In: Biology of Drosophila (M. Demerec, ed.), p. 275–367. New York: John Wiley 1950.

    Google Scholar 

  • Brown, D. D., Dawid, I. B.: Specific gene amplification in oocytes. Science 160, 272–280 (1968).

    Google Scholar 

  • Burgess, R. R.: A new method for the large scale purification of Escherichia coli deoxyribonucleic acid-dependent ribonucleic acid polymerase. J. biol. Chem. 244, 6160–6167 (1969).

    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 

  • Dickson, E., Boyd, J., Laird, C.: The informational content of polytene chromosome DNA from Drosophila hydei. J. molec. Biol. (in press, 1971).

  • Eckhardt, R. A.: Studies on the chromosomal distribution of repetitive nucleotide sequences in polytene chromosomes. J. Cell Biol. 47, 55a (1970).

    Google Scholar 

  • — Gall, J. G.: Satellite DNA associated with heterochromatin in Rhynchosciara. Chromosoma (Berl.) 32, 407–427 (1971).

    Google Scholar 

  • Evans, D., Birnstiel, M. L.: Localization of amplified ribosomal DNA in the oocyte of Xenopus laevis. Biochim. biophys. Acta (Amst.) 166, 274–276 (1968).

    Google Scholar 

  • Fansler, B., Travaglini, E., Loeb, L., Schultz, J.: Structure of Drosophila melanogaster dAT replicated in an in vitro system. Biochem. biophys. Res. Commun. 40, 1266–1272 (1970).

    Google Scholar 

  • Flamm, W. G., McCallum, M., Walker, P. M. B.: The isolation of complementary strands from a mouse DNA fraction. Proc. nat. Acad. Sci. (Wash.) 57, 1729–1734 (1967).

    Google Scholar 

  • Fujii, S.: Further studies on the salivary gland chromosomes of Drosophila virilis. Cytologia (Tokyo) 12, 435–459 (1942).

    Google Scholar 

  • Gall, J. G.: Differential synthesis of the genes for ribosomal RNA during Amphibian oogenesis. Proc. nat. Acad. Sci. (Wash.) 60, 553–560 (1968).

    Google Scholar 

  • — The genes for ribosomal RNA during oogenesis. Genetics (Suppl.) 61, 121–132 (1969).

    Google Scholar 

  • Gall, J. G., Pardue, M. L.: Nucleic acid hybridization in cytological preparations. In: Methods in enzymology XII C (L. Grossman and K. Moldave, eds.). New York: Academic Press, Inc. 1971.

    Google Scholar 

  • Gerbi, S.: Localization and characterization of the ribosomal RNA cistrons in Sciara coprophila. J. molec. Biol. (in press, 1971).

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

    Google Scholar 

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

    Google Scholar 

  • Hennig, W., Hennig, I., Stein, H.: Repeated sequences in the DNA of Drosophila, and their localization in giant chromosomes. Chromosoma (Berl.) 32, 31–63 (1970).

    Google Scholar 

  • Jones, K. W.: Chromosomal and nuclear location of mouse satellite DNA in individual cells. Nature (Lond.) 255, 912–915 (1970).

    Google Scholar 

  • — Robertson, F. W.: Localization of reiterated nucleotide sequences in Drosophila and mouse by in situ hybridisation of complementary RNA. Chromosoma (Berl.) 31, 331–345 (1970).

    Google Scholar 

  • Kaufmann, B. P.: Somatic mitoses of Drosophila melanogaster. J. Morph. 56, 125–155 (1934).

    Google Scholar 

  • Laird, C., McCarthy, B.: Magnitude of interspecific nucleotide sequence variability in Drosophila. Genetics 60, 303–322 (1968).

    Google Scholar 

  • — Molecular characterization of the Drosophila genome. Genetics 63, 865–882 (1969).

    Google Scholar 

  • Macgregor, H. C., Kezer, J.: The chromosomal localization of a heavy satellite DNA in the testis of Plethodon c. cinereus. Chromosoma (Berl.) 33, 167–182 (1971).

    Google Scholar 

  • Mandel, M., Marmur, J.: Use of ultraviolet absorbance-temperature profile for determining the guanine plus cytosine content of DNA. In: Methods in enzymology XII B (L. Grossman and K. Moldave, eds.). New York: Academic Press, Inc. 1968.

    Google Scholar 

  • — Schildkraut, C., Marmur, J.: Use of CsCl density gradient analysis for determining the guanine plus cytosine content of DNA. In: Methods in enzymology XII B (L. Grossman and K. Moldave, eds.). New York: Academic Press, Inc. 1968.

    Google Scholar 

  • Marmur, J., Doty, P.: Determination of the base composition of deoxyribonucleic acid from its thermal denaturation temperature. J. molec. Biol. 5, 109–118 (1962).

    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.: Translocations between the X and the Y chromosomes of Drosophila melanogaster. Genetics 45, 1705–1722 (1960).

    Google Scholar 

  • Pardue, M. L., Gall, J. G.: Molecular hybridization of radioactive DNA to the DNA of cytological preparations. Proc. nat. Acad. Sci. (Wash.) 64, 600–604 (1969).

    Google Scholar 

  • — Chromosomal localization of mouse satellite DNA. Science 168, 1356–1358 (1970).

    Google Scholar 

  • — Gerbi, S. A., Eckhardt, R. A., Gall, J. G.: Cytological localization of DNA complementary to ribosomal RNA in polytene chromosomes of Diptera. Chromosoma (Berl.) 29, 268–290 (1970).

    Google Scholar 

  • Perkowska, E., Macgregor, H. C., Birnstiel, M. L.: Gene amplification in the oocyte nucleus of mutant and wild-type Xenopus laevis. Nature (Lond.) 217, 649–650 (1968).

    Google Scholar 

  • Perreault, W., Kaufmann, B., Gay, H.: Similarity in base composition of heterochromatic and euchromatic DNA in Drosophila melanogaster. Genetics 60, 289–301 (1968).

    Google Scholar 

  • Pettit, B. J., Rasch, R. W., Rasch, E. M.: DNA synthesis in giant salivary chromosomes of Drosophila virilis prior to pupation. J. Cell Physiol. 69, 273–280 (1967).

    Google Scholar 

  • Pikó, L., Tyler, A., Vinograd, J.: Amount, location, priming capacity, circularity and other properties of cytoplasmic DNA in sea urchin eggs. Biol. Bull. 132, 68–90 (1967).

    Google Scholar 

  • Plaut, W.: On the replicative organization of DNA in the polytene chromosome of Drosophila melanogaster. J. molec. Biol. 7, 632–635 (1963).

    Google Scholar 

  • Prokofyeva-Belgovskaya, A. A.: The structure of the Y chromosome in the salivary glands of Drosophila melanogaster. Genetics 22, 94–103 (1937).

    Google Scholar 

  • Rae, P.: Chromosomal distribution of rapidly reannealing DNA in Drosophila melanogaster. Proc. nat. Acad. Sci. (Wash.) 67, 1018–1025 (1970).

    Google Scholar 

  • - Swift, H.: Rapidly reannealing DNA in the genome of Drosophila melanogaster. J. molec. Biol. (in press, 1971).

  • Ritossa, F., Atwood, K., Lindsley, D., Spiegelman, S.: On the chromosomal distribution of DNA complementary to ribosomal and soluble RNA. Nat. Cancer Inst. Monogr. 23, 449–472 (1966).

    Google Scholar 

  • — Scala, G.: Equilibrium variations in the redundancy of rDNA in Drosophila melanogaster. Genetics 61, (Suppl.), 305–317 (1969).

    Google Scholar 

  • — 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 

  • Rudkin, G. T.: The structure and function of heterochromatin. In: Genetics today (Proc. XI Int. Cong. Genetics), p. 359–374. The Hague: Pergamon Press 1964.

    Google Scholar 

  • —: Non replicating DNA in Drosophila. Genetics (Suppl.) 61, 227–238 (1969).

    Google Scholar 

  • Schurin, M., Marmur, J.: Differences in the DNA of adult and larval forms of D. virilis. Abstracts of First Annual Meeting, American Society for Cell Biology, p. 193 (1961).

  • Swift, H.: The histones of polytene chromosomes. In: The nucleohistones. (J. Bonner and P. Ts'o, eds.). San Francisco: Holden-Day 1964.

    Google Scholar 

  • - Rasch, E.: In: Alfert, M.: Composition and structure of giant chromosomes. Int. Rev. Cytol. 3, 131–175 (1954).

    Google Scholar 

  • Szybalski, W.: Use of cesium sulfate for equilibrium density gradient centrifugation. In: Methods in enzymology XII B (L. Grossman and K. Moldave, eds.). New York: Academic Press, Inc. 1968.

    Google Scholar 

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

    Google Scholar 

  • Travaglini, E., Petrovic, J., Schultz, J.: Two satellite cytoplasmic DNA's in Drosophila. J. Cell Biol. 39, 136a (1968).

    Google Scholar 

  • Tulchin, N., Mateyko, G. M., Kopac, M. J.: Drosophila salivary glands in vitro. J. Cell Biol. 34, 891–897 (1967).

    Google Scholar 

  • Vinograd, J., Morris, J., Davidson, N., Dove, W.: The buoyant behavior of viral and bacterial DNA in alkaline CsCl. Proc. nat. Acad. Sci. (Wash.) 49, 12–17 (1963).

    Google Scholar 

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Gall, J.G., Cohen, E.H. & Polan, M.L. Repetitive DNA sequences in Drosophila . Chromosoma 33, 319–344 (1971). https://doi.org/10.1007/BF00284948

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