Skip to main content
SpringerLink
Log in

Localization of ribosomal DNA insertion elements in polytene chromosomes of Drosophila simulans, Drosophila mauritiana and their interspecific hybrids

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

The locations of the ribosomal DNA (rDNA) insertion elements type I and type II along the polytene chromosomes of three Drosophila species of the melanogaster subgroup-D. simulans, D. mauritiana and D. melanogaster-have been compared. In situ hybridization has shown that the intragenomic distribution of type I as well as of type II insertions is different for these related species. In particular, we have revealed rDNA-free autosomal sites, containing type II element sequences within the D. simulans and D. mauritiana chromosomes. This finding confirms the ability of this type of insertion to transpose, as was demonstrated earlier for Bombyx mori. The appearance of the rDNA not associated with the nucleolar organizers, evident by additional nucleoli, occurred with species-specific frequency. At the same time, for all three species the pattern of such changes (an attachment of the nucleoti to varying sites of the chromosomes and the presence of ectopic contacts between them, a composition of the rDNA repeats in the nucleolar material not integrated at the nucleolar organizer) was similar. The number of additional nucleoti in the hybrid polytene nuclei corresponded to the value of the parental species exhibiting nucleolar replicative dominance.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ananiev, E. V., Barsky, V. E., Ilyin, Y. V. & Churikov, N. A., 1981. Localization of nucleoli in Drosophila melanogaster polytene chromosomes. Chromosoma 81: 619–628.

    Google Scholar 

  • Beckingham, K., 1982. Insect rDNA. In: Bush, H. & Rothblum, L. (eds). The cell nucleus, vol. 10. Academic Press, New York, pp. 205–269.

    Google Scholar 

  • Browne, M. J., Read, C. A., Roiha, H. & Glover, D. M., 1984. Site specific insertion of a type I rDNA element into a unique sequence in the Drosophila melanogaster genome. Nucl. Acids Res. 12: 9111–9121.

    Google Scholar 

  • Burke, W. D., Calalang, C. C. & Eickbush, T. H., 1987. The site-specific ribosomal insertion element type II of Bombyx mori (R2Bm) contains the coding sequence for a reverse transcriptase-like enzyme. Mol. and Cell. Biol. 7: 2221–2230.

    Google Scholar 

  • Dawid, I. B., Wellauer, P. K. & Long, O.E., 1978. Ribosomal DNA in Drosophila melanogaster. Isolation and characterization of cloned fragments. J. Mol. Biol. 126: 749–768.

    Google Scholar 

  • Durica, D. S. & Krider, H. M., 1977. Studies on the ribosomal RNA cistrons in iterspecific Drosophila hybrids. Dev. Biol. 55: 62–74.

    Google Scholar 

  • Eickbush, T. H. & Robins, B., 1985. Bombyx mori 28S genes contain insertion elements similar to the type I and type II elements of Drosophila melanogaster. EMBO J. 4: 2281–2285.

    Google Scholar 

  • Endow, S. A., 1980. On ribosomal gene compensation in Drosophila! Cell 22: 149–155.

    Google Scholar 

  • Endow, S. A., 1982. Polytenization of the ribosomal genes on the X and Y chromosomes of Drosophila melanogaster. Genetics 100: 375–385.

    Google Scholar 

  • Endow, S. A. & Glover, D. M., 1979. Differential replication of ribosomal gene repeats in polytene nuclei of Drosophila. Cell 17: 597–605.

    Google Scholar 

  • Fujiwara, H., Ogura, T., Takada, N., Miyajima, N., Ishikawa, H. & Maekawa, H., 1984. Introns and their flanking sequences of Bombyx mori rDNA. Nucli. Acids Res. 12: 6861–6869.

    Google Scholar 

  • Gall, J. G. & Pardue, M. L., 1971. Nucleic acids hybridization in cytological preparations. Methods Enzymol. 21: 470–480.

    Google Scholar 

  • Glover, D. M., 1977. Cloned segment of Drosophila melanogaster rDNA containing new types of sequence insertions. Proc. Natl. Acad. Sci. USA 74: 4932–4936.

    Google Scholar 

  • Glover, D. M., 1981. The rDNA of Drosophila melanogaster. Cell 26: 297–298.

    Google Scholar 

  • Goodrich-Young, C. & Krider, H. M., 1989. Nucleolar dominance and replicative dominance in Drosophila interspecific hybrids. Genetics 123: 349–358.

    Google Scholar 

  • Hennig, W. & Meer, B., 1971. Reduced polyteny of ribosomal RNA cistrons in giant chromosomes of Drosophila hydei. Nature New Biol. 233: 70–71.

    Google Scholar 

  • Hennig, W., Vogt, P., Jakob, G. & Siegmund, I., 1982. Nucleolus organizer regions in Drosophila species of the repleta group. Chromosoma 87: 279–292.

    Google Scholar 

  • Hilliker, A. J. & Appels, R., 1982. The cytogenetic boundaries of the rDNA region within heterochromatin of the X-chromosome of Drosophila melanogaster and their relation to male meiotic pairing sites. Genet. Res. (Cambr) 39: 149–156.

    Google Scholar 

  • Jakubezak, J. L., Xiong, Y. & Eickbush, T. H., 1990. Type (R1) and Type II (R2) ribosomal DNA insertions of Drosophila melanogaster are retrotransposable elements closely related to those in Bombyx mori. J. Mol. Biol. 212: 37–52.

    Google Scholar 

  • Kidd, S. J. & Glover, D. M., 1980. A DNA segment from Drosophila melanogaster which contains five tandemly repeating units homologous to the major rDNA insertions. Cell 19: 103–119.

    Google Scholar 

  • Kolchinsky, A. M., Vashakidze, R. P., Evgenev, M. B. & Mirzabekov, A. D., 1982. Cloning and study on Drosophila melanogaster ribosomal insertions. Mol. Biol. 16: 302–314.

    Google Scholar 

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

    Google Scholar 

  • Lemeunier, F., David, J. R., Tsacas, L. & Ashburner, M., 1986. The melanogaster species group. In: Ashburner, M. & Novitski, E., (eds). The genetics and biology of Drosophila, vol. 3e. Academic Press, London, New York, San Francisco, pp. 147–256.

    Google Scholar 

  • Lohe, A. R. & Roberts, P. A., 1990. An unusual Y chromosome of Drosophila simulans carrying amplified rDNA spacer without rRNA genes. Genetics 125: 399–406.

    Google Scholar 

  • Long, E. O. & Dawid, I. B., 1979. Expression of ribosomal DNA insertions in Drosophila melanogaster. Cell 18: 1185–1196.

    Google Scholar 

  • Mecheva, I. S. & Semionov, E. P., 1989. Comparison of the rDNA localization in three Drosophila sibling species (melanogaster subgroup). Compt. rend. Acad. bulg. Sci. 42: 105–108.

    Google Scholar 

  • Mecheva, I. S. & Semionov, E. P., 1990. rDNA replication in the interspecific hybrids of Drosophila. Compt. rend. Acad. bulg. Sci. 43: 89–91.

    Google Scholar 

  • Mecheva, I. S. & Semionov, E. P., 1991. Localization of ribosomal DNA in diploid and polytene nuclei of Drosophila simulans and Drosophila mauritiana. Dros. Inf. Serv. 70. In press.

  • Peacock, W. J., Appels, R., Endow, S. A. & Glover, D. M., 1981. Chromosomal distribution of the major insert in Drosophila melanogaster. Genet. Res. 37: 209–214.

    Google Scholar 

  • Ritossa, F. M. & Spiegelman, S., 1965. Localization of DNA complimentary to ribosomal RNA in the nucleolus organizer regions of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 53: 737–745.

    Google Scholar 

  • Roiha, H. & Glover, D. M., 1981. Duplicated rDNA sequences of variable lengths flanking the short type I insertions in the rDNA of Drosophila melanogaster. Nucl. Acids. Res. 9: 5521–5532.

    Google Scholar 

  • Roiha, H., Miller, J. R., Woods, L. C. & Glover, D. M., 1981. Arrangements and rearrangements of sequences flanking the two types of rDNA insertions in Drosophila melanogaster. Nature 290: 749–753.

    Google Scholar 

  • Roiha, H., Read, C. A., Browne, M. J. & Glover, D. M., 1983. Widely differing degrees of sequence conservation of the two types of rDNA insertion within the melanogaster species subgroup. EMBO J. 2: 721–726.

    Google Scholar 

  • Semionov, E. P. & Kirov, N. Kh., 1986. Increased number of nucleoli in the salivary gland cells of Drosophila melanogaster under conditions of rDNA dose compensation. Chromosoma 93: 477–482.

    Google Scholar 

  • Semionov, E. P., Smirnov, A. P. & Rodionov, A. V., 1978. Effect of EDTA on the conjugation of homologous polytene chromosomes and on ‘additional nucleolus formation’. Cytologia (USSR) 20: 411–414.

    Google Scholar 

  • Tartof, K. D., 1979. Evolution of transcribed and spacer sequences in the ribosomal RNA genes of Drosophila. Cell 17: 607–614.

    Google Scholar 

  • Tartof, K. D. & Dawid, I. B., 1976. Similarities and differences in the structure of X and Y chromosome rRNA genes of Drosophila. Nature 263: 27–30.

    Google Scholar 

  • Wellauer, P. K., Dawid, I. B. & Tartof, K. D., 1978. X and Y chromosomal ribosomal DNA of Drosophila: comparison of spacers and insertions. Cell 14: 269–278.

    Google Scholar 

  • Xiong, Y., Burke, W. D., Jakubchak, J. L. & Eickbush, T. H., 1988. Ribosomal DNA insertion elements R1Bm and R2Bm can transpose in a sequence-specific manner to locations outside the 28S gene. Nucl. Acids Res. 16: 10561–10573.

    Google Scholar 

  • Xiong, Y. & Eickbush, T. H., 1988a. Functional expression of a sequence-specific endonuclease encoded by the retrotransposon R2Bm. Cell 55: 235–246.

    Google Scholar 

  • Xiong, Y. & Eickbush, T. H., 1988b. The site-specific ribosomal DNA insertion element R1Bm belongs to a class of non-long-terminal-repeat retrotransposons. Mol. and Cell. Biol. 8: 114–123.

    Google Scholar 

  • Zuchowski, Ch. I. & Harford, A. G., 1977. Chromosomal rearrangements which affect the chromosomal integration of the ribosomal genes in Drosophila melanogaster. Cell 11: 383–388.

    Google Scholar 

Download references

Author information

Author notes

  1. I. S. Mecheva

    Present address: Department of Microbiology, MCV Station, Box 678, 23298-0678, Richmond, VA, USA

Authors and Affiliations

  1. Institute of Genetics, Bulgarian Academy of Sciences, 1113, Sofia, Bulgaria

    I. S. Mecheva

  2. Institute of Molecular Biology, Bulgarian Academy of Sciences, 1113, Sofia, Bulgaria

    E. P. Semionov

Authors
  1. I. S. Mecheva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. P. Semionov
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mecheva, I.S., Semionov, E.P. Localization of ribosomal DNA insertion elements in polytene chromosomes of Drosophila simulans, Drosophila mauritiana and their interspecific hybrids. Genetica 85, 223–229 (1992). https://doi.org/10.1007/BF00132274

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00132274

Key words

Search

Navigation