Abstract
R1 and R2 are distantly related non-long terminal repeat retrotransposable elements each of which inserts into a specific site in the 28S rRNA genes of most insects. We have analyzed aspects of R1 and R2 abundance and sequence variation in 27 geographical isolates of Drosophila melanogaster. The fraction of 28S rRNA genes containing these elements varied greatly between strains, 17-67% for R1 elements and 2-28% for R2 elements. The total percentage of the rDNA repeats inserted ranged from 32 to 77%. The fraction of the rDNA repeats that contained both of these elements suggested that R1 and R2 exhibit neither an inhibition of nor preference for insertion into a 28S gene already containing the other type of element. Based on the conservation of restriction sites in the elements of all strains, and sequence analysis of individual elements from three strains, nucleotide divergence is very low for R1 and R2 elements within or between strains (<0.6%). This sequence uniformity is the expected result of the forces of concerted evolution (unequal crossovers and gene conversion) which act on the rRNA genes themselves. Evidence for the role of retrotransposition in the turnover of R1 and R2 was obtained by using naturally occurring 5' length polymorphisms of the elements as markers for independent transposition events. The pattern of these different length 5' truncations of R1 and R2 was found to be diverse and unique to most strains analyzed. Because recombination can only, with time, amplify or eliminate those length variants already present, the diversity found in each strain suggests that retrotransposition has played a critical role in maintaining these elements in the rDNA repeats of D. melanogaster.
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- Ayer S., Benyajati C. Conserved enhancer and silencer elements responsible for differential Adh transcription in Drosophila cell lines. Mol Cell Biol. 1990 Jul;10(7):3512–3523. doi: 10.1128/mcb.10.7.3512. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Browne M. J., Read C. A., Roiha H., Glover D. M. Site specific insertion of a type I rDNA element into a unique sequence in the Drosophila melanogaster genome. Nucleic Acids Res. 1984 Dec 11;12(23):9111–9122. doi: 10.1093/nar/12.23.9111. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Burke W. D., Calalang C. C., Eickbush T. H. The site-specific ribosomal insertion element type II of Bombyx mori (R2Bm) contains the coding sequence for a reverse transcriptase-like enzyme. Mol Cell Biol. 1987 Jun;7(6):2221–2230. doi: 10.1128/mcb.7.6.2221. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Charlesworth B., Langley C. H. The population genetics of Drosophila transposable elements. Annu Rev Genet. 1989;23:251–287. doi: 10.1146/annurev.ge.23.120189.001343. [DOI] [PubMed] [Google Scholar]
- Dawid I. B., Rebbert M. L. Nucleotide sequences at the boundaries between gene and insertion regions in the rDNA of Drosophilia melanogaster. Nucleic Acids Res. 1981 Oct 10;9(19):5011–5020. doi: 10.1093/nar/9.19.5011. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dawid I. B., Wellauer P. K., Long E. O. Ribosomal DNA in Drosophila melanogaster. I. Isolation and characterization of cloned fragments. J Mol Biol. 1978 Dec 25;126(4):749–768. doi: 10.1016/0022-2836(78)90018-9. [DOI] [PubMed] [Google Scholar]
- Dover G., Coen E. Springcleaning ribosomal DNA: a model for multigene evolution? Nature. 1981 Apr 30;290(5809):731–732. doi: 10.1038/290731a0. [DOI] [PubMed] [Google Scholar]
- Eickbush T. H., Robins B. Bombyx mori 28S ribosomal genes contain insertion elements similar to the Type I and II elements of Drosophila melanogaster. EMBO J. 1985 Sep;4(9):2281–2285. doi: 10.1002/j.1460-2075.1985.tb03927.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Endow S. A., Glover D. M. Differential replication of ribosomal gene repeats in polytene nuclei of Drosophila. Cell. 1979 Jul;17(3):597–605. doi: 10.1016/0092-8674(79)90267-8. [DOI] [PubMed] [Google Scholar]
- Fujiwara H., Ogura T., Takada N., Miyajima N., Ishikawa H., Maekawa H. Introns and their flanking sequences of Bombyx mori rDNA. Nucleic Acids Res. 1984 Sep 11;12(17):6861–6869. doi: 10.1093/nar/12.17.6861. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Glover D. M., Hogness D. S. A novel arrangement of the 18S and 28S sequences in a repeating unit of Drosophila melanogaster rDNA. Cell. 1977 Feb;10(2):167–176. doi: 10.1016/0092-8674(77)90212-4. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Kalumuck K. E., Wetzel F. L., Procunier J. D. Relative abundance of various rDNA repeat types in polytene nuclei of Drosophila melanogaster. Genome. 1990 Apr;33(2):240–246. doi: 10.1139/g90-038. [DOI] [PubMed] [Google Scholar]
- Kerrebrock A. W., Srivastava R., Gerbi S. A. Isolation and characterization of ribosomal DNA variants from Sciara coprophila. J Mol Biol. 1989 Nov 5;210(1):1–13. doi: 10.1016/0022-2836(89)90286-6. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- 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]
- Long E. O., Rebbert M. L., Dawid I. B. Structure and expression of ribosomal RNA genes of Drosophila melanogaster interrupted by type-2 insertions. Cold Spring Harb Symp Quant Biol. 1981;45(Pt 2):667–672. doi: 10.1101/sqb.1981.045.01.084. [DOI] [PubMed] [Google Scholar]
- 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]
- Peacock W. J., Appels R., Endow S., Glover D. Chromosomal distribution of the major insert in Drosophila melanogaster 28S rRNA genes. Genet Res. 1981 Apr;37(2):209–214. doi: 10.1017/s0016672300020176. [DOI] [PubMed] [Google Scholar]
- Pellegrini M., Manning J., Davidson N. Sequence arrangement of the rDNA of Drosophila melanogaster. Cell. 1977 Feb;10(2):213–214. doi: 10.1016/0092-8674(77)90215-x. [DOI] [PubMed] [Google Scholar]
- Rae P. M. Coding region deletions associated with the major form of rDNA interruption in Drosophila. Nucleic Acids Res. 1981 Oct 10;9(19):4997–5010. doi: 10.1093/nar/9.19.4997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rae P. M., Kohorn B. D., Wade R. P. The 10 kb Drosophila virilis 28S rDNA intervening sequence is flanked by a direct repeat of 14 base pairs of coding sequence. Nucleic Acids Res. 1980 Aug 25;8(16):3491–3504. doi: 10.1093/nar/8.16.3491. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
- Smith V. L., Beckingham K. The intron boundaries and flanking rRNA coding sequences of Calliphora erythrocephala rDNA. Nucleic Acids Res. 1984 Feb 10;12(3):1707–1724. doi: 10.1093/nar/12.3.1707. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tartof K. D., Dawid I. G. Similarities and differences in the structure of X and Y chromosome rRNA genes of Drosophila. Nature. 1976 Sep 2;263(5572):27–30. doi: 10.1038/263027a0. [DOI] [PubMed] [Google Scholar]
- Tautz D., Hancock J. M., Webb D. A., Tautz C., Dover G. A. Complete sequences of the rRNA genes of Drosophila melanogaster. Mol Biol Evol. 1988 Jul;5(4):366–376. doi: 10.1093/oxfordjournals.molbev.a040500. [DOI] [PubMed] [Google Scholar]
- 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]
- Wellauer P. K., Dawid I. B. Ribosomal DNA in Drosophila melanogaster. II. Heteroduplex mapping of cloned and uncloned rDNA. J Mol Biol. 1978 Dec 25;126(4):769–782. doi: 10.1016/0022-2836(78)90019-0. [DOI] [PubMed] [Google Scholar]
- Wellauer P. K., Dawid I. B., Tartof K. D. X and Y chromosomal ribosomal DNA of Drosophila: comparison of spacers and insertions. Cell. 1978 Jun;14(2):269–278. doi: 10.1016/0092-8674(78)90113-7. [DOI] [PubMed] [Google Scholar]
- Wellauer P. K., Dawid I. B. The structural organization of ribosomal DNA in Drosophila melanogaster. Cell. 1977 Feb;10(2):193–212. doi: 10.1016/0092-8674(77)90214-8. [DOI] [PubMed] [Google Scholar]
- White R. L., Hogness D. S. R loop mapping of the 18S and 28S sequences in the long and short repeating units of Drosophila melanogaster rDNA. Cell. 1977 Feb;10(2):177–192. doi: 10.1016/0092-8674(77)90213-6. [DOI] [PubMed] [Google Scholar]
- Xiong Y. E., Eickbush T. H. Functional expression of a sequence-specific endonuclease encoded by the retrotransposon R2Bm. Cell. 1988 Oct 21;55(2):235–246. doi: 10.1016/0092-8674(88)90046-3. [DOI] [PubMed] [Google Scholar]
- Xiong Y., Burke W. D., Jakubczak J. L., Eickbush T. H. Ribosomal DNA insertion elements R1Bm and R2Bm can transpose in a sequence specific manner to locations outside the 28S genes. Nucleic Acids Res. 1988 Nov 25;16(22):10561–10573. doi: 10.1093/nar/16.22.10561. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Xiong Y., Eickbush T. H. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 1990 Oct;9(10):3353–3362. doi: 10.1002/j.1460-2075.1990.tb07536.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Xiong Y., Eickbush T. H. Similarity of reverse transcriptase-like sequences of viruses, transposable elements, and mitochondrial introns. Mol Biol Evol. 1988 Nov;5(6):675–690. doi: 10.1093/oxfordjournals.molbev.a040521. [DOI] [PubMed] [Google Scholar]
- Xiong Y., Eickbush T. H. The site-specific ribosomal DNA insertion element R1Bm belongs to a class of non-long-terminal-repeat retrotransposons. Mol Cell Biol. 1988 Jan;8(1):114–123. doi: 10.1128/mcb.8.1.114. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]