Skip to main content
Genetics logoLink to Genetics
. 1987 Jun;116(2):225–232. doi: 10.1093/genetics/116.2.225

Evolution of the Ribosomal DNA Spacers of Drosophila melanogaster : Different Patterns of Variation on X and Y Chromosomes

Scott M Williams 1,2, Glenn R Furnier 1,2, Eric Fuog 1,2, Curtis Strobeck 1,2
PMCID: PMC1203133  PMID: 3038672

Abstract

Length variation of the ribosomal gene spacers of Drosophila melanogaster was studied. Analysis of 47 X chromosomal and 47 Y chromosomal linked rDNA arrays collected from five continents indicates that the arrays on the two chromosomes differ qualitatively. The Y-linked arrays from around the world share little or no similarity for either their overall length or the organization of their spacers. Most of the X-linked arrays do, however, share a major length spacer of 5.1 kb. In addition, those X-linked arrays that have a major 5.1-kb band have similar spacer organization as demonstrated by genomic DNA digestions with several restriction enzymes. These data strongly support the hypothesis that spacer length patterns on only X-linked genes are maintained primarily by natural selection.

Full Text

The Full Text of this article is available as a PDF (3.5 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arnheim N., Krystal M., Schmickel R., Wilson G., Ryder O., Zimmer E. Molecular evidence for genetic exchanges among ribosomal genes on nonhomologous chromosomes in man and apes. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7323–7327. doi: 10.1073/pnas.77.12.7323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arnheim N., Treco D., Taylor B., Eicher E. M. Distribution of ribosomal gene length variants among mouse chromosomes. Proc Natl Acad Sci U S A. 1982 Aug;79(15):4677–4680. doi: 10.1073/pnas.79.15.4677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Britten R. J., Kohne D. E. Repeated sequences in DNA. Hundreds of thousands of copies of DNA sequences have been incorporated into the genomes of higher organisms. Science. 1968 Aug 9;161(3841):529–540. doi: 10.1126/science.161.3841.529. [DOI] [PubMed] [Google Scholar]
  4. Buongiorno-Nardelli M., Amaldi F., Beccari E., Junakovic N. Size of ribosomal DNA repeating units in Xenopus laevis: limited individual heterogeneity and extensive population polymorphism. J Mol Biol. 1977 Feb 15;110(1):105–117. doi: 10.1016/s0022-2836(77)80101-0. [DOI] [PubMed] [Google Scholar]
  5. Busby S. J., Reeder R. H. Spacer sequences regulate transcription of ribosomal gene plasmids injected into Xenopus embryos. Cell. 1983 Oct;34(3):989–996. doi: 10.1016/0092-8674(83)90556-1. [DOI] [PubMed] [Google Scholar]
  6. Chikaraishi D. M., Buchanan L., Danna K. J., Harrington C. A. Genomic organization of rat rDNA. Nucleic Acids Res. 1983 Sep 24;11(18):6437–6452. doi: 10.1093/nar/11.18.6437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. DeSalle R., Slightom J., Zimmer E. The molecular through ecological genetics of abnormal abdomen. II. Ribosomal DNA polymorphism is associated with the abnormal abdomen syndrome in Drosophila mercatorum. Genetics. 1986 Apr;112(4):861–875. doi: 10.1093/genetics/112.4.861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dover G. Molecular drive: a cohesive mode of species evolution. Nature. 1982 Sep 9;299(5879):111–117. doi: 10.1038/299111a0. [DOI] [PubMed] [Google Scholar]
  9. Gonzalez I. L., Gorski J. L., Campen T. J., Dorney D. J., Erickson J. M., Sylvester J. E., Schmickel R. D. Variation among human 28S ribosomal RNA genes. Proc Natl Acad Sci U S A. 1985 Nov;82(22):7666–7670. doi: 10.1073/pnas.82.22.7666. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Indik Z. K., Tartof K. D. Long spacers among ribosomal genes of Drosophila melanogaster. Nature. 1980 Apr 3;284(5755):477–479. doi: 10.1038/284477a0. [DOI] [PubMed] [Google Scholar]
  11. Ish-Horowicz D., Pinchin S. M., Schedl P., Artavanis-Tsakonas S., Mirault M. E. Genetic and molecular analysis of the 87A7 and 87C1 heat-inducible loci of D. melanogaster. Cell. 1979 Dec;18(4):1351–1358. doi: 10.1016/0092-8674(79)90245-9. [DOI] [PubMed] [Google Scholar]
  12. Kimura M., Ohta T. Population genetics of multigene family with special reference to decrease of genetic correlation with distance between gene members on a chromosome. Proc Natl Acad Sci U S A. 1979 Aug;76(8):4001–4005. doi: 10.1073/pnas.76.8.4001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kohorn B. D., Rae P. M. Accurate transcription of truncated ribosomal DNA templates in a Drosophila cell-free system. Proc Natl Acad Sci U S A. 1982 Mar;79(5):1501–1505. doi: 10.1073/pnas.79.5.1501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Metzenberg R. L., Stevens J. N., Selker E. U., Morzycka-Wroblewska E. Identification and chromosomal distribution of 5S rRNA genes in Neurospora crassa. Proc Natl Acad Sci U S A. 1985 Apr;82(7):2067–2071. doi: 10.1073/pnas.82.7.2067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Reeder R. H. Enhancers and ribosomal gene spacers. Cell. 1984 Sep;38(2):349–351. doi: 10.1016/0092-8674(84)90489-6. [DOI] [PubMed] [Google Scholar]
  16. Reeder R. H., Roan J. G., Dunaway M. Spacer regulation of Xenopus ribosomal gene transcription: competition in oocytes. Cell. 1983 Dec;35(2 Pt 1):449–456. doi: 10.1016/0092-8674(83)90178-2. [DOI] [PubMed] [Google Scholar]
  17. Reeder R. H., Roan J. G. The mechanism of nucleolar dominance in Xenopus hybrids. Cell. 1984 Aug;38(1):38–44. doi: 10.1016/0092-8674(84)90524-5. [DOI] [PubMed] [Google Scholar]
  18. Wellauer P. K., Dawid I. B., Brown D. D., Reeder R. H. The molecular basis for length heterogeneity in ribosomal DNA from Xenopus laevis. J Mol Biol. 1976 Aug 25;105(4):461–486. doi: 10.1016/0022-2836(76)90229-1. [DOI] [PubMed] [Google Scholar]
  19. Williams S. M., DeSalle R., Strobeck C. Homogenization of geographical variants at the nontranscribed spacer of rDNA in Drosophila mercatorum. Mol Biol Evol. 1985 Jul;2(4):338–346. doi: 10.1093/oxfordjournals.molbev.a040355. [DOI] [PubMed] [Google Scholar]
  20. Yang-Yen H. F., Subrahmanyam C. S., Cassidy B., Rothblum L. I. Characterization of rat ribosomal DNA II. identification of the highly repetitive DNA in the 3' non-transcribed spacer. J Mol Biol. 1985 Aug 5;184(3):389–398. doi: 10.1016/0022-2836(85)90289-x. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES