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Clustering of rDNA containing type 1 insertion sequence in the distal nucleolus organiser of Drosophila melanogaster: implications for the evolution of X and Y rDNA arrays

Published online by Cambridge University Press:  14 April 2009

P. R. England ,
H. W. Stokes  and
R. Frankham
P. R. England
Affiliation:
School of Biological Sciences, Macquarie University, N.S.W. 2109, Australia
H. W. Stokes
Affiliation:
School of Biological Sciences, Macquarie University, N.S.W. 2109, Australia
R. Frankham*
Affiliation:
School of Biological Sciences, Macquarie University, N.S.W. 2109, Australia
*
† Corresponding author.

Summary

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The ribosomal RNAs produced by the multigene families on the X and Y chromosomes of Drosophila melanogaster are very similar despite the apparent evolutionary isolation of the X and Y chromosomal rDNA. X–Y exchange through the rDNA is one mechanism that may promote co-evolution of the two gene clusters by transferring Y rDNA copies to the X chromosome. This hypothesis predicts that the proximal rDNA of X chromosomes will be Y-like. Consequently, rDNA variants found only on the X chromosome (such as those interrupted by type 1 insertions) should be significantly clustered in the distal X nucleolus organizer. Proximal and distal portions of the X chromosome nucleolus organizer were separated by recombination between the inverted chromosomes In(1)scv2 (breakpoint in the centre of the rDNA) and In(1)sc4Lsc8R (no rDNA). Molecular analyses of the resulting stocks demonstrated that rRNA genes containing type 1 insertions were predominantly located on the chromosome carrying the distal portion of the X rDNA, thus confirming a prediction of the X–Y exchange hypothesis for the co-evolution of X and Y chromosomal rDNA. Distal clustering is not predicted by the alternative hypotheses of selection or gene conversion.

Type
Research Article
Information
Genetics Research , Volume 51 , Issue 3 , June 1988 , pp. 209 - 215
Copyright
Copyright © Cambridge University Press 1988

References

Appels, R. & 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 sites. Genetical Research 39, 149–156.CrossRefGoogle ScholarPubMed
Baltimore, D. (1981). Gene conversion: some implications for immunoglobulin genes. Cell 24, 592–594.CrossRefGoogle ScholarPubMed
Boncinelli, E., Borghese, A., Graziani, F., La Mantia, G., Manzi, A., Mariani, C. & Simeone, A. (1983). Inheritance of the rDNA spacer in D. melanogaster. Molecular and General Genetics 189, 370–374.CrossRefGoogle Scholar
Coen, E. S. & Dover, G. A. (1983). Unequal exchanges and the coevolution of X and Y rDNA arrays in Drosophila melanogaster. Cell 33, 849–855.CrossRefGoogle ScholarPubMed
Coen, E. S., Strachan, T. & Dover, G. (1982). Dynamics of concerted evolution of ribosomal DNA and histone gene families in the melanogaster species subgroup of Drosophila. Journal of Molecular Biology 158, 17–35.Google Scholar
Coen, E. S., Thoday, J. M. & Dover, G. (1982) Rate of turnover of structural variants in the rDNA gene family of Drosophila melanogaster. Nature 295, 564–568.Google Scholar
Dawid, I. B. & Botchan, P. (1977). Sequences homologous to ribosomal insertions occur in the Drosophila genome outside the nucleolus organizer. Proceedings of the National Academy of Sciences, U.S.A. 74, 4233–4237.CrossRefGoogle ScholarPubMed
De Cicco, D. V. & Glover, D. M. (1983). Amplification of rDNA and Tl sequences in Drosophila males deficient in rDNA. Cell 32, 1217–1225.Google Scholar
Dutton, F. L. & Krider, H. M. (1984). Factors influencing the disproportionate replication of the ribosomal cistrons in Drosophila melanogaster. Genetics 107, 395–404.Google Scholar
Frankham, R. (1980). Origin of genetic variation in selection lines. In Selection Experiments in Laboratory and Domestic Animals (ed. Robertson, A.), pp. 56–68. Slough: Common-wealth Agricultural Bureaux.Google Scholar
Frankham, R., Briscoe, D. A. & Nurthen, R. K. (1978). Unequal crossing over at the rRNA locus as a source of quantitative genetic variation. Nature 272, 80–81.CrossRefGoogle ScholarPubMed
Frankham, R., Briscoe, D. A. & Nurthen, R. K. (1980). Unequal crossing over at the rRNA tandon as a source of quantitative genetic variation. Genetics 95, 727–742.CrossRefGoogle Scholar
Gerbi, S. A. (1985). Evolution of ribosomal DNA. In Molecular Evolutionary Genetics (ed. Maclntyre, R. J.), pp. 419–517. New York: Plenum Press.Google Scholar
Gillings, M. R., Frankham, R., Speirs, J. & Whalley, M. (1987). X–Y exchange and the coevolution of the X and Y rDNA arrays in Drosophila melanogaster. Genetics 116, 241–251.Google Scholar
Hawley, R. S., & Tartof, K. D. (1983). The ribosomal DNA of Drosophila melanogaster is organized differently from that of Drosophila hydei. Journal of Molecular Biology 163, 499–503.Google Scholar
Hilliker, A. J. & Appels, R. (1982). Pleiotropic effects associated with the deletion of heterochromatin surrounding rDNA on the X chromosome of Drosophila. Chromosoma 86, 469–490.CrossRefGoogle ScholarPubMed
Kalumuck, K. E. & Procunier, J. D. (1984). Non-selective amplification of ribosomal DNA repeat units in compensating genotypes of Drosophila melanogaster. Biochemical Genetics 22, 453–465.Google Scholar
Kidd, S. J. & Glover, D. M. (1980). A DNA segment from D. melanogaster which contains five tandemly repeating units homologous to the major rDNA insertion. Cell 19, 103–119.CrossRefGoogle Scholar
Lindsley, D. L., Appels, R. & Hilliker, A. J. (1982). The right breakpoint of In(1)scv2 subdivides the ribosomal DNA. Drosophila Information Service 59, 99–100.Google Scholar
Lindsley, D. L. & Grell, E. H. (1968). Genetic variations of Drosophila melanogaster. Carnegie Institute of Washington Publication No. 627.Google Scholar
Long, E. O., Rebbert, M. L. & Dawid, I. B. (1980). Structure and expression or ribosomal RNA genes of Drosophila melanogaster interrupted by type 2 insertions. Cold Spring Harbor Symposium on Quantitative Biology 45, 667–672.Google Scholar
Maddern, R. H. (1981). Exchange between the ribosomal RNA genes of the X and Y chromosomes of Drosophila melanogaster males. Genetical Research 38, 1–7.CrossRefGoogle ScholarPubMed
Maden, B. E. H. & Tartof, K. D. (1974). Nature of the ribosomal RNA transcribed from the X and Y chromosomes of Drosophila melanogaster. Journal of Molecular Biology 90, 51–64.Google Scholar
Pace, N. R., Olsen, G. J. & Woese, G. J. (1986). Ribosomal RNA phylogeny and the primary lines of evolutionary descent. Cell 45, 325–326.CrossRefGoogle ScholarPubMed
Palumbo, G., Endow, S. A. & Hawley, R. S. (1984). Reduction of wild type X chromosomes with the Ybb− chromosome of D. melanogaster. Genetical Research 43, 93–98.Google Scholar
Peacock, W. J., Appels, R., Endow, S. & Glover, D. (1981). Chromosomal distribution of the major insert in Drosophila melanogaster 28S rRNA genes. Genetical Research 37, 209–214.Google Scholar
Renkawitz-Pohl, R., Glatzer, K. H. & Kunz, W. (1981). Ribosomal RNA genes with an intervening sequence are clustered within the X-chromosomal ribosomal DNA of Drosophila hydei. Journal of Molecular Biology 148, 95–101.Google Scholar
Ritossa, F. (1976). The bobbed locus. In Genetics and Biology of Drosophila (ed. Ashburner, M. & Novitski, E.), pp. 801–846. London: Academic Press.Google Scholar
Roiha, H. & Glover, D. M. (1980). Characterisation of complete type II insertions in cloned segments of ribosomal DNA from Drosophila melanogaster. Journal of Molecular Biology 140, 341–355.CrossRefGoogle Scholar
Roiha, H., Miller, J. R., Woods, L. C. & Glover, D. M. (1981). Arrangements and rearrangements of sequences flanking the two types of rDNA insertion in D. melanogaster. Nature 290, 749–753.Google Scholar
Salzano, G. & Malva, C. (1984). Non-random loss of uninterrupted ribosomal DNA repeating units upon induction of a bobbed mutation. Journal of Molecular Biology 177, 189–200.Google Scholar
Sharp, Z. D., Gandhi, V. V. & Procunier, J. D. (1983). X chromosome nucleolus organizer mutants which alter major type I repeat multiplicity in Drosophila melanogaster. Molecular and General Genetics 190, 438–443.Google Scholar
Tartof, K. D. (1975). Redundant genes. Annual Review of Genetics 9, 355–385.Google Scholar
Tartof, K. D. & Dawid, I. B. (1976). Similarities and differences in the structure of X and Y chromosome rDNA genes of Drosophila. Nature 263, 27–30.Google Scholar
Terracol, R. & Prud'homme, N. (1986). Differential elimination of rDNA genes in bobbed mutants of Drosophila melanogaster. Molecular and Cellular Biology 6, 1023–1031.Google ScholarPubMed
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
Yagura, T., Yagura, M. & Muramatsu, M. (1979). Drosophila melanogaster has different ribosomal RNA sequences on X and Y chromosomes. Journal of Molecular Biology 133, 533–547.CrossRefGoogle ScholarPubMed