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. 2001 Aug;158(4):1557–1567. doi: 10.1093/genetics/158.4.1557

Dynamics of R1 and R2 elements in the rDNA locus of Drosophila simulans.

C E Pérez-González 1, T H Eickbush 1
PMCID: PMC1461747  PMID: 11514447

Abstract

The mobile elements R1 and R2 insert specifically into the rRNA gene locus (rDNA locus) of arthropods, a locus known to undergo concerted evolution, the recombinational processes that preserve the sequence homogeneity of all repeats. To monitor how rapidly individual R1 and R2 insertions are turned over in the rDNA locus by these processes, we have taken advantage of the many 5' truncation variants that are generated during the target-primed reverse transcription mechanism used by these non-LTR retrotransposons for their integration. A simple PCR assay was designed to reveal the pattern of the 5' variants present in the rDNA loci of individual X chromosomes in a population of Drosophila simulans. Each rDNA locus in this population was found to have a large, unique collection of 5' variants. Each variant was present at low copy number, usually one copy per chromosome, and was seldom distributed to other chromosomes in the population. The failure of these variants to spread to other units in the same rDNA locus suggests a strong recombinational bias against R1 and R2 that results in the individual copies of these elements being rapidly lost from the rDNA locus. This bias suggests a significantly higher frequency of R1 and R2 retrotransposition than we have previously suggested.

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Selected References

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

  1. Bowen T., Dover G. A. PCR amplification of intergenic spacers in the ribosomal DNA of Drosophila melanogaster reveals high levels of turnover in length and copy-number of spacers in geographically separated populations. Mol Ecol. 1995 Aug;4(4):419–427. doi: 10.1111/j.1365-294x.1995.tb00235.x. [DOI] [PubMed] [Google Scholar]
  2. Burke W. D., Eickbush D. G., Xiong Y., Jakubczak J., Eickbush T. H. Sequence relationship of retrotransposable elements R1 and R2 within and between divergent insect species. Mol Biol Evol. 1993 Jan;10(1):163–185. doi: 10.1093/oxfordjournals.molbev.a039990. [DOI] [PubMed] [Google Scholar]
  3. Burke W. D., Malik H. S., Jones J. P., Eickbush T. H. The domain structure and retrotransposition mechanism of R2 elements are conserved throughout arthropods. Mol Biol Evol. 1999 Apr;16(4):502–511. doi: 10.1093/oxfordjournals.molbev.a026132. [DOI] [PubMed] [Google Scholar]
  4. Burke W. D., Malik H. S., Lathe W. C., 3rd, Eickbush T. H. Are retrotransposons long-term hitchhikers? Nature. 1998 Mar 12;392(6672):141–142. doi: 10.1038/32330. [DOI] [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. Dvorák J., Jue D., Lassner M. Homogenization of tandemly repeated nucleotide sequences by distance-dependent nucleotide sequence conversion. Genetics. 1987 Jul;116(3):487–498. doi: 10.1093/genetics/116.3.487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Eickbush D. G., Eickbush T. H. Vertical transmission of the retrotransposable elements R1 and R2 during the evolution of the Drosophila melanogaster species subgroup. Genetics. 1995 Feb;139(2):671–684. doi: 10.1093/genetics/139.2.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Eickbush D. G., Lathe W. C., 3rd, Francino M. P., Eickbush T. H. R1 and R2 retrotransposable elements of Drosophila evolve at rates similar to those of nuclear genes. Genetics. 1995 Feb;139(2):685–695. doi: 10.1093/genetics/139.2.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Eickbush D. G., Luan D. D., Eickbush T. H. Integration of Bombyx mori R2 sequences into the 28S ribosomal RNA genes of Drosophila melanogaster. Mol Cell Biol. 2000 Jan;20(1):213–223. doi: 10.1128/mcb.20.1.213-223.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gentile K. L., Burke W. D., Eickbush T. H. Multiple lineages of R1 retrotransposable elements can coexist in the rDNA loci of Drosophila. Mol Biol Evol. 2001 Feb;18(2):235–245. doi: 10.1093/oxfordjournals.molbev.a003797. [DOI] [PubMed] [Google Scholar]
  11. George J. A., Burke W. D., Eickbush T. H. Analysis of the 5' junctions of R2 insertions with the 28S gene: implications for non-LTR retrotransposition. Genetics. 1996 Mar;142(3):853–863. doi: 10.1093/genetics/142.3.853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hawley R. S., Marcus C. H. Recombinational controls of rDNA redundancy in Drosophila. Annu Rev Genet. 1989;23:87–120. doi: 10.1146/annurev.ge.23.120189.000511. [DOI] [PubMed] [Google Scholar]
  13. Hillis D. M., Moritz C., Porter C. A., Baker R. J. Evidence for biased gene conversion in concerted evolution of ribosomal DNA. Science. 1991 Jan 18;251(4991):308–310. doi: 10.1126/science.1987647. [DOI] [PubMed] [Google Scholar]
  14. Holliday R. Gene conversion: a possible mechanism for eliminating selfish DNA. Basic Life Sci. 1982;20:259–264. doi: 10.1007/978-1-4613-3476-7_17. [DOI] [PubMed] [Google Scholar]
  15. Jakubczak J. L., Burke W. D., Eickbush T. H. Retrotransposable elements R1 and R2 interrupt the rRNA genes of most insects. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3295–3299. doi: 10.1073/pnas.88.8.3295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jakubczak J. L., Xiong Y., Eickbush T. H. Type I (R1) and type II (R2) ribosomal DNA insertions of Drosophila melanogaster are retrotransposable elements closely related to those of Bombyx mori. J Mol Biol. 1990 Mar 5;212(1):37–52. doi: 10.1016/0022-2836(90)90303-4. [DOI] [PubMed] [Google Scholar]
  17. Jakubczak J. L., Zenni M. K., Woodruff R. C., Eickbush T. H. Turnover of R1 (type I) and R2 (type II) retrotransposable elements in the ribosomal DNA of Drosophila melanogaster. Genetics. 1992 May;131(1):129–142. doi: 10.1093/genetics/131.1.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Jamrich M., Miller O. L., Jr The rare transcripts of interrupted rRNA genes in Drosophila melanogaster are processed or degraded during synthesis. EMBO J. 1984 Jul;3(7):1541–1545. doi: 10.1002/j.1460-2075.1984.tb02008.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kidd S. J., Glover D. M. A DNA segment from D. melanogaster which contains five tandemly repeating units homologous to the major rDNA insertion. Cell. 1980 Jan;19(1):103–119. doi: 10.1016/0092-8674(80)90392-x. [DOI] [PubMed] [Google Scholar]
  20. Kidd S. J., Glover D. M. Drosophila melanogaster ribosomal DNA containing type II insertions is variably transcribed in different strains and tissues. J Mol Biol. 1981 Oct 5;151(4):645–662. doi: 10.1016/0022-2836(81)90428-9. [DOI] [PubMed] [Google Scholar]
  21. Lathe W. C., 3rd, Burke W. D., Eickbush D. G., Eickbush T. H. Evolutionary stability of the R1 retrotransposable element in the genus Drosophila. Mol Biol Evol. 1995 Nov;12(6):1094–1105. doi: 10.1093/oxfordjournals.molbev.a040283. [DOI] [PubMed] [Google Scholar]
  22. Lathe W. C., 3rd, Eickbush T. H. A single lineage of r2 retrotransposable elements is an active, evolutionarily stable component of the Drosophila rDNA locus. Mol Biol Evol. 1997 Dec;14(12):1232–1241. doi: 10.1093/oxfordjournals.molbev.a025732. [DOI] [PubMed] [Google Scholar]
  23. Linares A. R., Bowen T., Dover G. A. Aspects of nonrandom turnover involved in the concerted evolution of intergenic spacers within the ribosomal DNA of Drosophila melanogaster. J Mol Evol. 1994 Aug;39(2):151–159. doi: 10.1007/BF00163804. [DOI] [PubMed] [Google Scholar]
  24. Lohe A. R., Roberts P. A. An unusual Y chromosome of Drosophila simulans carrying amplified rDNA spacer without rRNA genes. Genetics. 1990 Jun;125(2):399–406. doi: 10.1093/genetics/125.2.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Long E. O., Dawid I. B. Expression of ribosomal DNA insertions in Drosophila melanogaster. Cell. 1979 Dec;18(4):1185–1196. doi: 10.1016/0092-8674(79)90231-9. [DOI] [PubMed] [Google Scholar]
  26. Long E. O., Dawid I. B. Repeated genes in eukaryotes. Annu Rev Biochem. 1980;49:727–764. doi: 10.1146/annurev.bi.49.070180.003455. [DOI] [PubMed] [Google Scholar]
  27. Luan D. D., Korman M. H., Jakubczak J. L., Eickbush T. H. Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell. 1993 Feb 26;72(4):595–605. doi: 10.1016/0092-8674(93)90078-5. [DOI] [PubMed] [Google Scholar]
  28. Lyckegaard E. M., Clark A. G. Evolution of ribosomal RNA gene copy number on the sex chromosomes of Drosophila melanogaster. Mol Biol Evol. 1991 Jul;8(4):458–474. doi: 10.1093/oxfordjournals.molbev.a040664. [DOI] [PubMed] [Google Scholar]
  29. Malik H. S., Eickbush T. H. Retrotransposable elements R1 and R2 in the rDNA units of Drosophila mercatorum: abnormal abdomen revisited. Genetics. 1999 Feb;151(2):653–665. doi: 10.1093/genetics/151.2.653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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. 1992;85(3):223–229. doi: 10.1007/BF00132274. [DOI] [PubMed] [Google Scholar]
  31. Moran J. V., Holmes S. E., Naas T. P., DeBerardinis R. J., Boeke J. D., Kazazian H. H., Jr High frequency retrotransposition in cultured mammalian cells. Cell. 1996 Nov 29;87(5):917–927. doi: 10.1016/s0092-8674(00)81998-4. [DOI] [PubMed] [Google Scholar]
  32. Nuzhdin S. V., Mackay T. F. Direct determination of retrotransposon transposition rates in Drosophila melanogaster. Genet Res. 1994 Apr;63(2):139–144. doi: 10.1017/s0016672300032249. [DOI] [PubMed] [Google Scholar]
  33. Nuzhdin S. V., Mackay T. F. The genomic rate of transposable element movement in Drosophila melanogaster. Mol Biol Evol. 1995 Jan;12(1):180–181. doi: 10.1093/oxfordjournals.molbev.a040188. [DOI] [PubMed] [Google Scholar]
  34. Petrov D. A., Lozovskaya E. R., Hartl D. L. High intrinsic rate of DNA loss in Drosophila. Nature. 1996 Nov 28;384(6607):346–349. doi: 10.1038/384346a0. [DOI] [PubMed] [Google Scholar]
  35. Polanco C., González A. I., Dover G. A. Patterns of variation in the intergenic spacers of ribosomal DNA in Drosophila melanogaster support a model for genetic exchanges during X-Y pairing. Genetics. 2000 Jul;155(3):1221–1229. doi: 10.1093/genetics/155.3.1221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Polanco C., González A. I., de la Fuente, Dover G. A. Multigene family of ribosomal DNA in Drosophila melanogaster reveals contrasting patterns of homogenization for IGS and ITS spacer regions. A possible mechanism to resolve this paradox. Genetics. 1998 May;149(1):243–256. doi: 10.1093/genetics/149.1.243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Roiha H., Miller J. R., Woods L. C., Glover D. M. Arrangements and rearrangements of sequences flanking the two types of rDNA insertion in D. melanogaster. Nature. 1981 Apr 30;290(5809):749–753. doi: 10.1038/290749a0. [DOI] [PubMed] [Google Scholar]
  38. Schlötterer C., Tautz D. Chromosomal homogeneity of Drosophila ribosomal DNA arrays suggests intrachromosomal exchanges drive concerted evolution. Curr Biol. 1994 Sep 1;4(9):777–783. doi: 10.1016/s0960-9822(00)00175-5. [DOI] [PubMed] [Google Scholar]
  39. Szostak J. W., Wu R. Unequal crossing over in the ribosomal DNA of Saccharomyces cerevisiae. Nature. 1980 Apr 3;284(5755):426–430. doi: 10.1038/284426a0. [DOI] [PubMed] [Google Scholar]
  40. Templeton A. R., Hollocher H., Lawler S., Johnston J. S. Natural selection and ribosomal DNA in Drosophila. Genome. 1989;31(1):296–303. doi: 10.1139/g89-047. [DOI] [PubMed] [Google Scholar]
  41. Vincent A., Petes T. D. Mitotic and meiotic gene conversion of Ty elements and other insertions in Saccharomyces cerevisiae. Genetics. 1989 Aug;122(4):759–772. doi: 10.1093/genetics/122.4.759. [DOI] [PMC free article] [PubMed] [Google Scholar]

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