#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

A Population Genetic Model for the Maintenance of R2 Retrotransposons in rRNA Gene Loci


R2 retrotransposable elements exclusively insert into the tandemly repeated rRNA genes, the rDNA loci, of their animal hosts. R2 elements form stable long-term associations with their host, in which all individuals in a population contain many potentially active copies, but only a fraction of these individuals show active R2 retrotransposition. Previous studies have found that R2 RNA transcripts are processed from a 28S co-transcript and that the likelihood of R2-inserted units being transcribed is dependent upon their distribution within the rDNA locus. Here we analyze the rDNA locus and R2 elements from nearly 100 R2-active and R2-inactive individuals from natural populations of Drosophila simulans. Along with previous findings concerning the structure and expression of the rDNA loci, these data were incorporated into computer simulations to model the crossover events that give rise to the concerted evolution of the rRNA genes. The simulations that best reproduce the population data assume that only about 40 rDNA units out of the over 200 total units are actively transcribed and that these transcribed units are clustered in a single region of the locus. In the model, the host establishes this transcription domain at each generation in the region with the fewest R2 insertions. Only if the host cannot avoid R2 insertions within this 40-unit domain are R2 elements active in that generation. The simulations also require that most crossover events in the locus occur in the transcription domain in order to explain the empirical observation that R2 elements are seldom duplicated by crossover events. Thus the key to the long-term stability of R2 elements is the stochastic nature of the crossover events within the rDNA locus, and the inevitable expansions and contractions that introduce and remove R2-inserted units from the transcriptionally active domain.


Vyšlo v časopise: A Population Genetic Model for the Maintenance of R2 Retrotransposons in rRNA Gene Loci. PLoS Genet 9(1): e32767. doi:10.1371/journal.pgen.1003179
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003179

Souhrn

R2 retrotransposable elements exclusively insert into the tandemly repeated rRNA genes, the rDNA loci, of their animal hosts. R2 elements form stable long-term associations with their host, in which all individuals in a population contain many potentially active copies, but only a fraction of these individuals show active R2 retrotransposition. Previous studies have found that R2 RNA transcripts are processed from a 28S co-transcript and that the likelihood of R2-inserted units being transcribed is dependent upon their distribution within the rDNA locus. Here we analyze the rDNA locus and R2 elements from nearly 100 R2-active and R2-inactive individuals from natural populations of Drosophila simulans. Along with previous findings concerning the structure and expression of the rDNA loci, these data were incorporated into computer simulations to model the crossover events that give rise to the concerted evolution of the rRNA genes. The simulations that best reproduce the population data assume that only about 40 rDNA units out of the over 200 total units are actively transcribed and that these transcribed units are clustered in a single region of the locus. In the model, the host establishes this transcription domain at each generation in the region with the fewest R2 insertions. Only if the host cannot avoid R2 insertions within this 40-unit domain are R2 elements active in that generation. The simulations also require that most crossover events in the locus occur in the transcription domain in order to explain the empirical observation that R2 elements are seldom duplicated by crossover events. Thus the key to the long-term stability of R2 elements is the stochastic nature of the crossover events within the rDNA locus, and the inevitable expansions and contractions that introduce and remove R2-inserted units from the transcriptionally active domain.


Zdroje

1. EickbushTH, EickbushDG (2007) Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics 175: 477–485.

2. ConconiA, WidmerRM, KollerT, SogoJM (1989) Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle. Cell 57: 753–761.

3. DammannR, LucchiniR, KollerT, SogoJM (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.

4. YeJ, EickbushTH (2006) Chromatin structure and transcription of the R1- and R2-inserted rRNA genes of Drosophila melanogaster. Mol Cell Biol 26: 8781–8790.

5. Eickbush TH (2002) R2 and Related Site-specific non-LTR Retrotransposons. pp. 813–835. In Mobile DNA II, N. Craig, R. Craigie, M. Gellert, and A Lambowitz, eds. American Society of Microbiology Press. Washington D.C.

6. KojimaKK, FujiawaraH (2005) Long-term inheritance of the 28S rDNA-specific retrotransposon R2. Mol Biol Evol 22: 2157–2165.

7. KojimaKK, KumaK, TohH, FujiwaraH (2006) Identification of rDNA-specific non-LTR retrotransposons in Cnidaria. Mol Biol Evol 23: 1984–1993.

8. LatheWD3rd, EickbushTH (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.

9. StageDE, EickbushTH (2009) Origin of nascent lineages and the mechanisms used to prime second-strand DNA synthesis in the R1 and R2 retrotransposons of Drosophila. Genome Biology 10: R49.

10. BurkeWD, MalikHS, LatheWC3rd, EickbushTH (1998) Are retrotransposons long-term hitchhikers? Nature 392: 141–142.

11. MalikHS, BurkeWD, EickbushTH (1999) The age and evolution of non-LTR retrotransposable elements. Mol Biol Evol 16: 793–805.

12. Perez-GonzalezCE, EickbushTH (2002) Rates of R1 and R2 retrotransposition and elimination from the rDNA locus of Drosophila melanogaster. Genetics 162: 799–811.

13. ZhangX, EickbushTH (2005) Characterization of active R2 retrotransposition in the rDNA locus of Drosophila simulans. Genetics 170: 195–205.

14. Ohta T (1980) Evolution and variation of multigene families. New York: Springer-Verlag.

15. OhtaT, DoverG (1983) Population genetics of multigene families that are dispersed into two or more chromosomes. Proc Natl Acad Sci U S A 80: 4079–4083.

16. LyckegaardEMS, ClarkAG (1991) Evolution of ribosomal RNA gene copy number on the sex chromosomes of Drosophila melanogaster. Mol Biol Evol 8: 458–474.

17. ZhangX, EickbushMT, EickbushTH (2008) Role of recombination in the long-term retention of transposable elements in rRNA gene loci. Genetics 180: 1617–1629.

18. EickbushDG, YeJ, ZhangX, BurkeWD, EickbushTH (2008) Epigenetic regulation of retrotransposons within the nucleolus of Drosophila. Mol Cell Biol 28: 645–26461.

19. EickbushDG, EickbushTH (2010) R2 retrotransposons encode a self-cleaving ribozyme for processing from an rRNA co-transcript. Mol Cell Biol 30: 3142–3150.

20. ZhouJ, EickbushTH (2009) The pattern of R2 retrotransposon activity in natural populations of Drosophila simulans reflects the dynamic nature of the rDNA locus. PLoS Genet 5: e1000386 doi:10.1371/journal.pgen.1000386.

21. LoheAR, RobertsPA (1990) An unusual Y chromosome of Drosophila simulans carrying amplified rDNA spacer without rRNA genes. Genetics 125: 399–406.

22. LuanDD, KormanMH, JakubczakJL, EickbushTH (1993) Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell 72: 595–605.

23. OstertagEM, KazazianHH (2001) Biology of mammalian L1 retrotransposons. Ann Rev Genet 35: 501–538.

24. AverbeckKT, EickbushTH (2005) Monitoring the mode and tempo of concerted evolution in the Drosophila melanogaster rDNA locus. Genetics 171: 1837–1846.

25. McKnightSL, MillerOL (1976) Ultrastructural patterns of RNA synthesis during early embryogenesis of Drosophila melanogaster. Cell 8: 305–319.

26. HawleyRS, MarcusCH (1989) Recombinational controls of rDNA redundancy in Drosophila. Ann Rev Genet 23: 87–120.

27. WilliamsSM, KennisonJA, RobbinsLG, StrobeckC (1989) Reciprocal recombination and the evolution of the ribosomal gene family of Drosophila melanogaster. Genetics 122: 617–624.

28. SchlottererC, TautzD (1994) Chromosomal homogeneity of Drosophila ribosomal DNA arrays suggests intrachromosomal exchange drives concerted evolution. Curr Biol 4: 777–783.

29. CharlesworthB, LangleyCH (1989) The population genetics of Drosophila transposable elements. Ann Rev Genet 23: 251–287.

30. CharlesworthB, SniegowskiP, StephanW (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371: 215–220.

31. Le RouzicA, BoutinTS, CapyP (2007) Long-term evolution of transposable elements. Proc Natl Acad Sci U S A 104: 19375–19380.

32. LeeYCG, LangleyCH (2010) Transposable elements in natural populations of Drosophila melanogaster. Phil Trans R Soc B 365: 1219–1228.

33. GentileK, BurkeWD, LatheWC, EickbushTH (2001) Stable and unstable lineages of the R1 retrotransposable element in the genus Drosophila. Mol Biol Evol 18: 235–245.

34. BurkeWD, EickbushDG, XiongY, JakubczakJ, EickbushTH (1993) Sequence relationship of retrotransposable elements R1 and R2 within and between divergent insect species. Mol Biol Evol 10: 163–185.

35. StageDE, EickbushTE (2010) Maintenance of multiple lineages of R1 and R2 retrotransposable elements in the ribosomal RNA gene loci of Nasonia. Insect Mol Biol 19 (suppl.1): 37–48.

36. FeschotteC (2008) Transposable elements and the evolution of regulatory networks. Nature Rev (Genetics) 9: 397–405.

37. GonzálezJ, KarasovTL, MesserPW, PetrovDA (2010) Genome-wide patterns of adaptation to temperature environments associated with transposable elements in Drosophila. PLoS Genet 6: e10000905 doi:10.1371/journal.pgen.1002932.

38. JamrichM, MillerOL (1984) The rare transcripts of interrupted rRNA genes in Drosophila melanogaster are processed or degraded during synthesis. EMBO J 3: 1541–1545.

39. ChooiWY (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.

40. MackayTFC, LymanRF, JacksonS, TerzianC, HillWG (1992) Polygenic mutation in Drosophila melanogaster: estimates from divergence among inbred strains. Evolution 46: 300–316.

41. AguileraA, Gomez-GonzalezB (2008) Genome instability: a mechanistic view of its causes and consequences. Nature Rev (Genetics) 9: 204–217.

42. PanJ, SasakiM, KniewelR, MurakamiH, Blitzblau, et al. (2011) A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144: 719–731.

43. AutonA, Fledel-AlonA, PfeiferS, VennO, SegurelL, et al. (2012) A fine-scale chimpanzee genetic map from population sequencing. Science 336: 193–198.

44. Voelket-MeimanK, KeilRL, RoederGS (1987) Recombination-stimulating sequences in yeast ribosomal DNA correspond to sequences regulating transcription by RNA polymerase I. Cell 48: 1071–1079.

45. Zhang X (2008) Dynamics of the rDNA locus and its retrotransposable elements. Ph.D. thesis, University of Rochester, Rochester, NY.

46. O'DonnellKA, BoekeJD (2007) Mighty Piwis defend the germline against genome intruders. Cell 129: 37–44.

47. BrenneckeJ, AravinAA, StarkA, DusM, KellisM, et al. (2007) Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128: 1089–1103.

48. AyerS, BenyajatiC (1990) Conserved enhancer and silencer elements responsible for differential Adh transcription in Drosophila cell lines. Mol Cell Biol 10: 3512–3523.

49. AdamsMD, CelnikerSE, HoltRA, EvansCA, GocayneJD, et al. (2000) The geneome sequence of Drosophila melanogaster. Science 287: 2185–2195.

50. EickbushDG, EickbushTH (1995) Vertical transmission of the retrotransposable elements R1 and R2 during the evolution of the Drosophila melanogaster species subgroup. Genetics 139: 671–684.

51. ZhangX, ZhouJ, EickbushTH (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.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2013 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#