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. 1995 Apr;139(4):1611–1621. doi: 10.1093/genetics/139.4.1611

Stability of Tandem Repeats in the Drosophila Melanogaster HSR-Omega Nuclear RNA

N C Hogan 1, F Slot 1, K L Traverse 1, J C Garbe 1, W G Bendena 1, M L Pardue 1
PMCID: PMC1206488  PMID: 7540581

Abstract

The Drosophila melanogaster Hsr-omega locus produces a nuclear RNA containing >5 kb of tandem repeat sequences. These repeats are unique to Hsr-omega and show concerted evolution similar to that seen with classical satellite DNAs. In D. melanogaster the monomer is ~280 bp. Sequences of 191/2 monomers differ by 8 +/- 5% (mean +/- SD), when all pairwise comparisons are considered. Differences are single nucleotide substitutions and 1-3 nucleotide deletions/insertions. Changes appear to be randomly distributed over the repeat unit. Outer repeats do not show the decrease in monomer homogeneity that might be expected if homogeneity is maintained by recombination. However, just outside the last complete repeat at each end, there are a few fragments of sequence similar to the monomer. The sequences in these flanking regions are not those predicted for sequences decaying in the absence of recombination. Instead, the fragmentation of the sequence homology suggests that flanking regions have undergone more severe disruptions, possibly during an insertion or amplification event. Hsr-omega alleles differing in the number of repeats are detected and appear to be stable over a few thousand generations; however, both increases and decreases in repeat numbers have been observed. The new alleles appear to be as stable as their predecessors. No alleles of less than ~5 kb nor more than ~16 kb of repeats were seen in any stocks examined. The evidence that there is a limit on the minimum number of repeats is consistent with the suggestion that these repeats are important in the function of the unusual Hsr-omega nuclear RNA.

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Selected References

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  1. Bendena W. G., Garbe J. C., Traverse K. L., Lakhotia S. C., Pardue M. L. Multiple inducers of the Drosophila heat shock locus 93D (hsr omega): inducer-specific patterns of the three transcripts. J Cell Biol. 1989 Jun;108(6):2017–2028. doi: 10.1083/jcb.108.6.2017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Biessmann H., Mason J. M. Progressive loss of DNA sequences from terminal chromosome deficiencies in Drosophila melanogaster. EMBO J. 1988 Apr;7(4):1081–1086. doi: 10.1002/j.1460-2075.1988.tb02916.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cabot E. L., Doshi P., Wu M. L., Wu C. I. Population genetics of tandem repeats in centromeric heterochromatin: unequal crossing over and chromosomal divergence at the Responder locus of Drosophila melanogaster. Genetics. 1993 Oct;135(2):477–487. doi: 10.1093/genetics/135.2.477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cluster P. D., Marinković D., Allard R. W., Ayala F. J. Correlations between development rates, enzyme activities, ribosomal DNA spacer-length phenotypes, and adaptation in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1987 Jan;84(2):610–614. doi: 10.1073/pnas.84.2.610. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Coen E. S., Thoday J. M., Dover G. Rate of turnover of structural variants in the rDNA gene family of Drosophila melanogaster. Nature. 1982 Feb 18;295(5850):564–568. doi: 10.1038/295564a0. [DOI] [PubMed] [Google Scholar]
  6. Danilevskaya O. N., Slot F., Traverse K. L., Hogan N. C., Pardue M. L. Drosophila telomere transposon HeT-A produces a transcript with tightly bound protein. Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6679–6682. doi: 10.1073/pnas.91.14.6679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Diaz M. O., Gall J. G. Giant readthrough transcription units at the histone loci on lampbrush chromosomes of the newt Notophthalmus. Chromosoma. 1985;92(4):243–253. doi: 10.1007/BF00329807. [DOI] [PubMed] [Google Scholar]
  9. Eckert R. L., Green H. Structure and evolution of the human involucrin gene. Cell. 1986 Aug 15;46(4):583–589. doi: 10.1016/0092-8674(86)90884-6. [DOI] [PubMed] [Google Scholar]
  10. Endow S. A., Komma D. J. One-step and stepwise magnification of a bobbed lethal chromosome in Drosophila melanogaster. Genetics. 1986 Oct;114(2):511–523. doi: 10.1093/genetics/114.2.511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Epstein L. M., Mahon K. A., Gall J. G. Transcription of a satellite DNA in the newt. J Cell Biol. 1986 Oct;103(4):1137–1144. doi: 10.1083/jcb.103.4.1137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Garbe J. C., Bendena W. G., Alfano M., Pardue M. L. A Drosophila heat shock locus with a rapidly diverging sequence but a conserved structure. J Biol Chem. 1986 Dec 25;261(36):16889–16894. [PubMed] [Google Scholar]
  13. Garbe J. C., Pardue M. L. Heat shock locus 93D of Drosophila melanogaster: a spliced RNA most strongly conserved in the intron sequence. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1812–1816. doi: 10.1073/pnas.83.6.1812. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hogan N. C., Traverse K. L., Sullivan D. E., Pardue M. L. The nucleus-limited Hsr-omega-n transcript is a polyadenylated RNA with a regulated intranuclear turnover. J Cell Biol. 1994 Apr;125(1):21–30. doi: 10.1083/jcb.125.1.21. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hög C., Daneholt B., Wieslander L. Terminal repeats in long repeat arrays are likely to reflect the early evolution of Balbiani ring genes. J Mol Biol. 1988 Apr 20;200(4):655–664. doi: 10.1016/0022-2836(88)90478-0. [DOI] [PubMed] [Google Scholar]
  16. Jeffreys A. J., Neumann R., Wilson V. Repeat unit sequence variation in minisatellites: a novel source of DNA polymorphism for studying variation and mutation by single molecule analysis. Cell. 1990 Feb 9;60(3):473–485. doi: 10.1016/0092-8674(90)90598-9. [DOI] [PubMed] [Google Scholar]
  17. Lindsley D. L., Sandler L. The genetic analysis of meiosis in female Drosophila melanogaster. Philos Trans R Soc Lond B Biol Sci. 1977 Mar 21;277(955):295–312. doi: 10.1098/rstb.1977.0019. [DOI] [PubMed] [Google Scholar]
  18. Maresca A., Singer M. F. Deca-satellite: a highly polymorphic satellite that joins alpha-satellite in the African green monkey genome. J Mol Biol. 1983 Mar 15;164(4):493–511. doi: 10.1016/0022-2836(83)90047-5. [DOI] [PubMed] [Google Scholar]
  19. Mohler J., Pardue M. L. Mutational Analysis of the Region Surrounding the 93d Heat Shock Locus of DROSOPHILA MELANOGASTER. Genetics. 1984 Feb;106(2):249–265. doi: 10.1093/genetics/106.2.249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Pardue M. L., Dawid I. B. Chromosomal locations of two DNA segments that flank ribosomal insertion-like sequences in Drosophila: flanking sequences are mobile elements. Chromosoma. 1981;83(1):29–43. doi: 10.1007/BF00286014. [DOI] [PubMed] [Google Scholar]
  21. Petes T. D. Unequal meiotic recombination within tandem arrays of yeast ribosomal DNA genes. Cell. 1980 Mar;19(3):765–774. doi: 10.1016/s0092-8674(80)80052-3. [DOI] [PubMed] [Google Scholar]
  22. Ryseck R. P., Walldorf U., Hoffmann T., Hovemann B. Heat shock loci 93D of Drosophila melanogaster and 48B of Drosophila hydei exhibit a common structural and transcriptional pattern. Nucleic Acids Res. 1987 Apr 24;15(8):3317–3333. doi: 10.1093/nar/15.8.3317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Smith G. P. Evolution of repeated DNA sequences by unequal crossover. Science. 1976 Feb 13;191(4227):528–535. doi: 10.1126/science.1251186. [DOI] [PubMed] [Google Scholar]
  24. Stephan W. Tandem-repetitive noncoding DNA: forms and forces. Mol Biol Evol. 1989 Mar;6(2):198–212. doi: 10.1093/oxfordjournals.molbev.a040542. [DOI] [PubMed] [Google Scholar]
  25. Strand M., Prolla T. A., Liskay R. M., Petes T. D. Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair. Nature. 1993 Sep 16;365(6443):274–276. doi: 10.1038/365274a0. [DOI] [PubMed] [Google Scholar]
  26. Tartof K. D. Unequal mitotic sister chromatid exchange and disproportionate replication as mechanisms regulating ribosomal RNA gene redundancy. Cold Spring Harb Symp Quant Biol. 1974;38:491–500. doi: 10.1101/sqb.1974.038.01.053. [DOI] [PubMed] [Google Scholar]
  27. Wolff R. K., Plaetke R., Jeffreys A. J., White R. Unequal crossingover between homologous chromosomes is not the major mechanism involved in the generation of new alleles at VNTR loci. Genomics. 1989 Aug;5(2):382–384. doi: 10.1016/0888-7543(89)90076-1. [DOI] [PubMed] [Google Scholar]
  28. Wu C. I., True J. R., Johnson N. Fitness reduction associated with the deletion of a satellite DNA array. Nature. 1989 Sep 21;341(6239):248–251. doi: 10.1038/341248a0. [DOI] [PubMed] [Google Scholar]

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