The pattern of R2 retrotransposon activity in natural populations of Drosophila simulans reflects the dynamic nature of the rDNA locus

PLoS Genetics

Volumn 5, Issue 2, 2009, Pages

  Zhou, Jun ^a   Eickbush, Thomas H ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RIBOSOME DNA; RNA 28S;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DNA STRUCTURE; DROSOPHILA SIMULANS; FEMALE; GENE INSERTION; GENE LOCUS; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; MALE; NONHUMAN; OPEN READING FRAME; RETROPOSON; ANIMAL; DROSOPHILA; GENE DOSAGE; GENETICS;

ANIMALIA; DROSOPHILA SIMULANS;

ANIMAL POPULATION GROUPS; ANIMALS; DNA, RIBOSOMAL; DROSOPHILA; FEMALE; GENE DOSAGE; MALE; RETROELEMENTS; RNA, RIBOSOMAL, 28S; TRANSCRIPTION, GENETIC;

EID: 61449167094     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000386     Document Type: Article

References (43)

1. Charlesworth B, Langley CH (1989) The population genetics of Drosophila transposable elements. Annu Rev Genet 23: 251-287.
2. Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371: 215-220.
3. Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8: 272-285.
4. Vastenhouw NL, Plasterk RH (2004) RNAi protects the Caenorhabditis elegans germline against transposition. Trends Genet 20: 314-319.
5. Finnegan DJ (1992) Transposable elements. Curr Opin Genet Dev 2: 861-867.
6. Biemont C, Lemeunier F, Gautier C, Garcia Guerreiro M, Aulard S, et al. (1994) High rate of movement of one (mdg3) out of four transposable elements in a natural population of Drosophila melanogaster. C R Acad Sci III 317: 213-216.
7. Nuzhdin SV, Mackay TF (1995) The genomic rate of transposable element movement in Drosophila melanogaster. Mol Biol Evol 12: 180-181.
8. Prud'homme N, Gans M, Masson M, Terzian C, Bucheton A (1995) Flamenco, a gene controlling the gypsy retrovirus of Drosophila melanogaster. Genetics 139: 697-711.
9. Vieira C, Biemont C (1997) Transposition rate of the 412 retrotransposable element is independent of copy number in natural populations of Drosophila simulans. Mol Biol Evol 14: 185-188.
10. Perez-Gonzalez CE, Eickbush TH (2001) Dynamics of R1 and R2 elements in the rDNA locus of Drosophila simulans. Genetics 158: 1557-1567.
11. Desset S, Meignin C, Dastugue B, Vaury C (2003) COM, a heterochromatic locus governing the control of independent endogenous retroviruses from Drosophila melanogaster. Genetics 164: 501-509.
12. Eickbush TH, Eickbush DG (2007) Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics 175: 477-485.
13. Ganley AR, Kobayashi T (2007) Highly efficient concerted evolution in the ribosomal DNA repeats: total rDNA repeat variation revealed by whole-genome shotgun sequence data. Genome Res 17: 184-191.
14. Stage DE, Eickbush TH (2007) Sequence variation within the rRNA gene loci of 12 Drosophila species. Genome Res 17: 1888-1897.
15. Eickbush TH (2002) R2 and related site-specific non-long terminal repeat retrotransposons. In: Craig N, Craige R, Gellert M, Lambowitz A, eds. Mobile DNA II. Washington: ASM Press. pp 813-835.
16. Penton EH, Crease TJ (2004) Evolution of the transposable element Pokey in the ribosomal DNA of species in the subgenus Daphnia (Crustacea: Cladocera). Mol Biol Evol 21: 1727-1739.
17. Kojima KK, Fujiwara H (2005) Long-term inheritance of the 28S rDNA-specific retrotransposon R2. Mol Biol Evol 22: 2157-2165.
18. Burke WD, Malik HS, Lathe WC 3rd, Eickbush TH (1998) Are retrotransposons long-term hitchhikers? Nature 392: 141-142.
19. Malik HS, Burke WD, Eickbush TH (1999) The age and evolution of non-LTR retrotransposable elements. Mol Biol Evol 16: 793-805.
20. Jakubczak JL, Zenni MK, Woodruff RC, Eickbush TH (1992) Turnover of R1 (type I) and R2 (type II) retrotransposable elements in the ribosomal DNA of Drosophila melanogaster. Genetics 131: 129-142.
21. Lathe WD 3rd, Eickbush TH (1997) A single lineage of r2 retrotransposable elements is an active, evolutionarily stable component of the Drosophila rDNA locus. Mol Biol Evol 14: 1232-1241.
22. Lathe WC 3rd, Burke WD, Eickbush DG, Eickbush TH (1995) Evolutionary stability of the R1 retrotransposable element in the genus Drosophila. Mol Biol Evol 12: 1094-1105.
23. Zhang X, Eickbush MT, Eickbush TH (2008) Role of recombination in the long-term retention of transposable elements in rRNA gene loci. Genetics 180: 1617-1626.
24. Zhang X, Eickbush TH (2005) Characterization of active R2 retrotransposition in the rDNA locus of Drosophila simulans. Genetics 170: 195-205.
25. Zhang X, Zhou J, Eickbush TH (2008) Rapid R2 retrotransposition leads to the loss of previously inserted copies via large deletions of the rDNA locus. Mol Biol Evol 25: 229-237.
26. Eickbush DG, Ye J, Zhang X, Burke WD, Eickbush TH (2008) Epigenetic Regulation of Retrotransposons within the Nucleolus of Drosophila. Mol Cell Biol 28: 6452-6461.
27. Perez-Gonzalez CE, Eickbush TH (2002) Rates of R1 and R2 retrotransposition and elimination from the rDNA locus of Drosophila melanogaster. Genetics 162: 799-811.
28. George JA, Burke WD, Eickbush TH (1996) Analysis of the 5′ junctions of R2 insertions with the 28S gene: implications for non-LTR retrotransposition. Genetics 142: 853-863.
29. Averbeck KT, Eickbush TH (2005) Monitoring the mode and tempo of concerted evolution in the Drosophila melanogaster rDNA locus. Genetics 171: 1837-1846.
30. Burke WD, Eickbush DG, Xiong Y, Jakubczak J, Eickbush TH (1993) Sequence relationship of retrotransposable elements R1 and R2 within and between divergent insect species. Mol Biol Evol 10: 163-185.
31. Eickbush DG, Eickbush TH (1995) Vertical transmission of the retrotransposable elements R1 and R2 during the evolution of the Drosophila melanogaster species subgroup. Genetics 139: 671-684.
32. Long EO, Dawid IB (1979) Expression of ribosomal DNA insertions in of Drosophila melanogaster. Cell 18: 1185-1196.
33. Kidd SJ, Clover DM (1981) Drosophila melanogaster ribosomal DNA containing type II insertions is variably transcribed in different strains and tissues. J Mol Biol 151: 645-662.
34. George JA, Eickbush TH (1999) Conserved features at the 5 end of Drosophila R2 retrotransposable elements: implications for transcription and translation. Insect Mol Biol 8: 3-10.
35. Eickbush DG, Eickbush TH (2003) Transcription of endogenous and exogenous R2 elements in the rRNA gene locus of Drosophila melanogaster. Mol Cell Biol 23: 3825-3836.
36. Ye J, Eickbush TH (2006) Chromatin structure and transcription of the R1- and R2-inserted rRNA genes of Drosophila melanogaster. Mol Cell Biol 26: 8781-8790.
37. Dammann R, Lucchini R, Koller T, Sogo JM (1995) Transcription in the yeast rRNA gene locus: distribution of the active gene copies and chromatin structure of their flanking regulatory sequences. Mol Cell Biol 15: 5294-5303.
38. Conconi A, Widmer RM, Koller T, Sogo JM (1989) Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle. Cell 57: 753-761.
39. McKnight SL, Miller OL (1976) Ultrastructural patterns of RNA synthesis during early embryogenesis of Drosophila melanogaster. Cell 8: 305-319.
40. Chooi WY (1979) The occurrence of long transcription units among the X and Y ribosomal genes of Drosophila melanogaster: transcription of insertion sequences. Chromosoma 74: 57-74.
41. Jamrich M, Miller OL (1984) The rare transcripts of interrupted rRNA genes in Drosophila melanogaster are processed or degraded during synthesis. EMBO J 3: 1541-1545.
42. Pikaard CS (2000) Nucleolar dominance: uniparental gene silencing on a multi-megabase scale in genetic hybrids. Plant Mol Biol 43: 163-177.
43. Gloor GB, Preston CR, Jonhnson-Schlitz DM, Nassif NA, Phillis RW, et al. (1993) Type I repressors of P-element mobility. Genetics 135: 81-95.