#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Sequencing of Pooled DNA Samples (Pool-Seq) Uncovers Complex Dynamics of Transposable Element Insertions in


Transposable elements (TEs) are mobile genetic elements that parasitize genomes by semi-autonomously increasing their own copy number within the host genome. While TEs are important for genome evolution, appropriate methods for performing unbiased genome-wide surveys of TE variation in natural populations have been lacking. Here, we describe a novel and cost-effective approach for estimating population frequencies of TE insertions using paired-end Illumina reads from a pooled population sample. Importantly, the method treats insertions present in and absent from the reference genome identically, allowing unbiased TE population frequency estimates. We apply this method to data from a natural Drosophila melanogaster population from Portugal. Consistent with previous reports, we show that low recombining genomic regions harbor more TE insertions and maintain insertions at higher frequencies than do high recombining regions. We conservatively estimate that there are almost twice as many “novel” TE insertion sites as sites known from the reference sequence in our population sample (6,824 novel versus 3,639 reference sites, with on average a 31-fold coverage per insertion site). Different families of transposable elements show large differences in their insertion densities and population frequencies. Our analyses suggest that the history of TE activity significantly contributes to this pattern, with recently active families segregating at lower frequencies than those active in the more distant past. Finally, using our high-resolution TE abundance measurements, we identified 13 candidate positively selected TE insertions based on their high population frequencies and on low Tajima's D values in their neighborhoods.


Vyšlo v časopise: Sequencing of Pooled DNA Samples (Pool-Seq) Uncovers Complex Dynamics of Transposable Element Insertions in. PLoS Genet 8(1): e32767. doi:10.1371/journal.pgen.1002487
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002487

Souhrn

Transposable elements (TEs) are mobile genetic elements that parasitize genomes by semi-autonomously increasing their own copy number within the host genome. While TEs are important for genome evolution, appropriate methods for performing unbiased genome-wide surveys of TE variation in natural populations have been lacking. Here, we describe a novel and cost-effective approach for estimating population frequencies of TE insertions using paired-end Illumina reads from a pooled population sample. Importantly, the method treats insertions present in and absent from the reference genome identically, allowing unbiased TE population frequency estimates. We apply this method to data from a natural Drosophila melanogaster population from Portugal. Consistent with previous reports, we show that low recombining genomic regions harbor more TE insertions and maintain insertions at higher frequencies than do high recombining regions. We conservatively estimate that there are almost twice as many “novel” TE insertion sites as sites known from the reference sequence in our population sample (6,824 novel versus 3,639 reference sites, with on average a 31-fold coverage per insertion site). Different families of transposable elements show large differences in their insertion densities and population frequencies. Our analyses suggest that the history of TE activity significantly contributes to this pattern, with recently active families segregating at lower frequencies than those active in the more distant past. Finally, using our high-resolution TE abundance measurements, we identified 13 candidate positively selected TE insertions based on their high population frequencies and on low Tajima's D values in their neighborhoods.


Zdroje

1. WickerTSabotFHua-VanABennetzenJLCapyP 2007 A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8 973 982

2. MillerWJMcDonaldJFNouaudDAnxolabehereD 1999 Molecular domestication–more than a sporadic episode in evolution. Genetica 107 197 207

3. AminetzachYTMacphersonJMPetrovDA 2005 Pesticide resistance via transposition-mediated adaptive gene truncation in Drosophila. Science 309 764 767

4. DabornPJYenJLBogwitzMRLe GoffGFeilE 2002 A single p450 allele associated with insecticide resistance in Drosophila. Science 297 2253 2256

5. GonzalezJLenkovKLipatovMMacphersonJMPetrovDA 2008 High rate of recent transposable element-induced adaptation in Drosophila melanogaster. PLoS Biol 6 e251 doi:10.1371/journal.pbio.0060251

6. GonzalezJPetrovDA 2009 The adaptive role of transposable elements in the Drosophila genome. Gene 448 124 133

7. BiessmannHKasraviBJakesKBuiTIkenagaK 1993 The genomic organization of HeT-A retroposons in Drosophila melanogaster. Chromosoma 102 297 305

8. BiessmannHValgeirsdottirKLofskyAChinCGintherB 1992 HeT-A, a transposable element specifically involved in “healing” broken chromosome ends in Drosophila melanogaster. Mol Cell Biol 12 3910 3918

9. HouleDNuzhdinSV 2004 Mutation accumulation and the effect of copia insertions in Drosophila melanogaster. Genet Res 83 7 18

10. PapaceitMAvilaVAguadeMGarcia-DoradoA 2007 The dynamics of the roo transposable element in mutation-accumulation lines and segregating populations of Drosophila melanogaster. Genetics 177 511 522

11. Perez-GonzalezCEEickbushTH 2002 Rates of R1 and R2 retrotransposition and elimination from the rDNA locus of Drosophila melanogaster. Genetics 162 799 811

12. KidwellMGKidwellJFSvedJA 1977 Hybrid Dysgenesis in DROSOPHILA MELANOGASTER: A Syndrome of Aberrant Traits Including Mutation, Sterility and Male Recombination. Genetics 86 813 833

13. RubinGMKidwellMGBinghamPM 1982 The molecular basis of P-M hybrid dysgenesis: the nature of induced mutations. Cell 29 987 994

14. CooleyLKelleyRSpradlingA 1988 Insertional mutagenesis of the Drosophila genome with single P elements. Science 239 1121 1128

15. FinneganDJ 1992 Transposable elements. Curr Opin Genet Dev 2 861 867

16. PuigMCaceresMRuizA 2004 Silencing of a gene adjacent to the breakpoint of a widespread Drosophila inversion by a transposon-induced antisense RNA. Proc Natl Acad Sci U S A 101 9013 9018

17. SteinemannMSteinemannSLottspeichF 1993 How Y-Chromosomes Become Genetically Inert. Proceedings of the National Academy of Sciences of the United States of America 90 5737 5741

18. NuzhdinSV 1999 Sure facts, speculations, and open questions about the evolution of transposable element copy number. Genetica 107 129 137

19. BurtATriversR 2006 Genes in Conflict: The Biology of Selfish Genetic Elements: Harvard Univ. Pr

20. MontgomeryECharlesworthBLangleyCH 1987 A test for the role of natural selection in the stabilization of transposable element copy number in a population of Drosophila melanogaster. Genet Res 49 31 41

21. MontgomeryEAHuangSMLangleyCHJuddBH 1991 Chromosome rearrangement by ectopic recombination in Drosophila melanogaster: genome structure and evolution. Genetics 129 1085 1098

22. LangleyCHMontgomeryEHudsonRKaplanNCharlesworthB 1988 On the role of unequal exchange in the containment of transposable element copy number. Genet Res 52 223 235

23. AravinAAHannonGJBrenneckeJ 2007 The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318 761 764

24. HannonGJMaloneCD 2009 Small RNAs as Guardians of the Genome. Cell 136 656 668

25. MontgomeryEALangleyCH 1983 Transposable Elements in Mendelian Populations. II. Distribution of Three COPIA-like Elements in a Natural Population of DROSOPHILA MELANOGASTER. Genetics 104 473 483

26. CharlesworthBLangleyCH 1989 The Population-Genetics of Drosophila Transposable Elements. Annual Review of Genetics 23 251 287

27. BiemontC 1992 Population-Genetics of Transposable DNA Elements - a Drosophila Point-of-View. Genetica 86 67 84

28. LeeYCLangleyCH 2010 Transposable elements in natural populations of Drosophila melanogaster. Philos Trans R Soc Lond B Biol Sci 365 1219 1228

29. KaminkerJSBergmanCMKronmillerBCarlsonJSvirskasR 2002 The transposable elements of the Drosophila melanogaster euchromatin: a genomics perspective. Genome Biol 3 RESEARCH0084

30. BartolomeCMasideXCharlesworthB 2002 On the abundance and distribution of transposable elements in the genome of Drosophila melanogaster. Mol Biol Evol 19 926 937

31. HillWGRobertsonA 1966 The effect of linkage on limits to artificial selection. Genet Res 8 269 294

32. CharlesworthBBetancourtAJKaiserVBGordoI 2009 Genetic recombination and molecular evolution. Cold Spring Harb Symp Quant Biol 74 177 186

33. DolginESCharlesworthB 2008 The effects of recombination rate on the distribution and abundance of transposable elements. Genetics 178 2169 2177

34. PetrovDAAminetzachYTDavisJCBensassonDHirshAE 2003 Size matters: non-LTR retrotransposable elements and ectopic recombination in Drosophila. Mol Biol Evol 20 880 892

35. PetrovDAFiston-LavierASLipatovMLenkovKGonzalezJ 2010 Population genomics of transposable elements in Drosophila melanogaster. Mol Biol Evol 28 1633 1644

36. BowenNJMcDonaldJF 2001 Drosophila euchromatic LTR retrotransposons are much younger than the host species in which they reside. Genome Res 11 1527 1540

37. BergmanCMBensassonD 2007 Recent LTR retrotransposon insertion contrasts with waves of non-LTR insertion since speciation in Drosophila melanogaster. Proc Natl Acad Sci U S A 104 11340 11345

38. LeratEBurletNBiemontCVieiraC 2010 Comparative analysis of transposable elements in the melanogaster subgroup sequenced genomes. Gene 473 100 109

39. EanesWFWesleyCCharlesworthB 1992 Accumulation of P elements in minority inversions in natural populations of Drosophila melanogaster. Genet Res 59 1 9

40. BiemontCLemeunierFGarcia GuerreiroMPBrookfieldJFGautierC 1994 Population dynamics of the copia, mdg1, mdg3, gypsy, and P transposable elements in a natural population of Drosophila melanogaster. Genet Res 63 197 212

41. SniegowskiPDCharlesworthB 1994 Transposable element numbers in cosmopolitan inversions from a natural population of Drosophila melanogaster. Genetics 137 815 827

42. CharlesworthBLapidACanadaD 1992 The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. I. Element frequencies and distribution. Genet Res 60 103 114

43. CharlesworthBJarnePAssimacopoulosS 1994 The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. III. Element abundances in heterochromatin. Genet Res 64 183 197

44. MasideXBartolomeCAssimacopoulosSCharlesworthB 2001 Rates of movement and distribution of transposable elements in Drosophila melanogaster: in situ hybridization vs Southern blotting data. Genet Res 78 121 136

45. LipatovMLenkovKPetrovDABergmanCM 2005 Paucity of chimeric gene-transposable element transcripts in the Drosophila melanogaster genome. BMC Biol 3 24

46. BartolomeCMasideX 2004 The lack of recombination drives the fixation of transposable elements on the fourth chromosome of Drosophila melanogaster. Genet Res 83 91 100

47. BergeroRForrestACharlesworthD 2008 Active miniature transposons from a plant genome and its nonrecombining Y chromosome. Genetics 178 1085 1092

48. HazzouriKMMohajerADejakSIOttoSPWrightSI 2008 Contrasting patterns of transposable-element insertion polymorphism and nucleotide diversity in autotetraploid and allotetraploid Arabidopsis species. Genetics 179 581 592

49. HormozdiariFHajirasoulihaIDaoPHachFYorukogluD 2010 Next-generation VariationHunter: combinatorial algorithms for transposon insertion discovery. Bioinformatics 26 i350 357

50. DrysdaleR 2008 FlyBase : a database for the Drosophila research community. Methods Mol Biol 420 45 59

51. SacktonTBKulathinalRJBergmanCMQuinlanARDopmanEB 2009 Population genomic inferences from sparse high-throughput sequencing of two populations of Drosophila melanogaster. Genome Biol Evol 1 449 465

52. BergmanCMQuesnevilleHAnxolabehereDAshburnerM 2006 Recurrent insertion and duplication generate networks of transposable element sequences in the Drosophila melanogaster genome. Genome Biol 7 R112

53. JensenMACharlesworthBKreitmanM 2002 Patterns of genetic variation at a chromosome 4 locus of Drosophila melanogaster and D. simulans. Genetics 160 493 507

54. WangWThorntonKBerryALongM 2002 Nucleotide variation along the Drosophila melanogaster fourth chromosome. Science 295 134 137

55. JordanIKRogozinIBGlazkoGVKooninEV 2003 Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet 19 68 72

56. van de LagemaatLNLandryJRMagerDLMedstrandP 2003 Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. Trends Genet 19 530 536

57. MasideXAssimacopoulosSCharlesworthB 2005 Fixation of transposable elements in the Drosophila melanogaster genome. Genet Res 85 195 203

58. KapitonovVVJurkaJ 2003 Molecular paleontology of transposable elements in the Drosophila melanogaster genome. Proc Natl Acad Sci U S A 100 6569 6574

59. SinghNDPetrovDA 2004 Rapid sequence turnover at an intergenic locus in Drosophila. Mol Biol Evol 21 670 680

60. AdamsMDCelnikerSEHoltRAEvansCAGocayneJD 2000 The genome sequence of Drosophila melanogaster. Science 287 2185 2195

61. GoldmanASLichtenM 1996 The efficiency of meiotic recombination between dispersed sequences in Saccharomyces cerevisiae depends upon their chromosomal location. Genetics 144 43 55

62. BrenneckeJAravinAAStarkADusMKellisM 2007 Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128 1089 1103

63. BiemontCTsitroneAVieiraCHooglandC 1997 Transposable element distribution in Drosophila. Genetics 147 1997 1999

64. RizzonCMaraisGGouyMBiemontC 2002 Recombination rate and the distribution of transposable elements in the Drosophila melanogaster genome. Genome Research 12 400 407

65. CohenJ 1978 Partialed products are interactions; partial powers are curve components. Psychological Bulletin 85 858 866

66. AndersonJASongYSLangleyCH 2008 Molecular population genetics of Drosophila subtelomeric DNA. Genetics 178 477 487

67. PetrovDALozovskayaERHartlDL 1996 High intrinsic rate of DNA loss in Drosophila. Nature 384 346 349

68. PetrovDAHartlDL 1998 High rate of DNA loss in the Drosophila melanogaster and Drosophila virilis species groups. Mol Biol Evol 15 293 302

69. BlumenstielJPHartlDLLozovskyER 2002 Patterns of insertion and deletion in contrasting chromatin domains. Mol Biol Evol 19 2211 2225

70. BartolomeCBelloXMasideX 2009 Widespread evidence for horizontal transfer of transposable elements across Drosophila genomes. Genome Biol 10 R22

71. TajimaF 1989 Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123 585 595

72. BravermanJMHudsonRRKaplanNLLangleyCHStephanW 1995 The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics 140 783 796

73. KimYStephanW 2002 Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics 160 765 777

74. OdgersWAAquadroCFCoppinCWHealyMJOakeshottJG 2002 Nucleotide polymorphism in the Est6 promoter, which is widespread in derived populations of Drosophila melanogaster, changes the level of Esterase 6 expressed in the male ejaculatory duct. Genetics 162 785 797

75. LiH 2011 A new test for detecting recent positive selection that is free from the confounding impacts of demography. Mol Biol Evol 28 365 375

76. SmithJMHaighJ 1974 The hitch-hiking effect of a favourable gene. Genet Res 23 23 35

77. InnanHKimY 2004 Pattern of polymorphism after strong artificial selection in a domestication event. Proc Natl Acad Sci U S A 101 10667 10672

78. HermissonJPenningsPS 2005 Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169 2335 2352

79. Fiston-LavierASCarriganMPetrovDAGonzalezJ 2010 T-lex: a program for fast and accurate assessment of transposable element presence using next-generation sequencing data. Nucleic Acids Res 39 e36

80. AlkanCSajjadianSEichlerEE 2011 Limitations of next-generation genome sequence assembly. Nat Methods 8 61 65

81. HooglandCBiemontC 1996 Chromosomal distribution of transposable elements in Drosophila melanogaster: test of the ectopic recombination model for maintenance of insertion site number. Genetics 144 197 204

82. KidwellMG 1992 Horizontal transfer of P elements and other short inverted repeat transposons. Genetica 86 275 286

83. MaloneCDBrenneckeJDusMStarkAMcCombieWR 2009 Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 137 522 535

84. PandeyRVKoflerROrozco-terWengelPNolteVSchlottererC 2011 PoPoolation DB: a user-friendly web-based database for the retrieval of natural polymorphisms in Drosophila. BMC Genet 12 27

85. QuesnevilleHBergmanCMAndrieuOAutardDNouaudD 2005 Combined evidence annotation of transposable elements in genome sequences. PLoS Comput Biol 1 e22 doi:10.1371/journal.pcbi.0010022

86. SmitAFAHubleyRGreenP RepeatMasker

87. LiHDurbinR 2010 Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26 589 595

88. LiHHandsakerBWysokerAFennellTRuanJ 2009 The Sequence Alignment/Map format and SAMtools. Bioinformatics 25 2078 2079

89. KoflerROrozco-terWengelPDe MaioNPandeyRVNolteV 2011 PoPoolation: a toolbox for population genetic analysis of next generation sequencing data from pooled individuals. PLoS ONE 6 e15925 doi:10.1371/journal.pone.0015925

90. RobinsonJTThorvaldsdottirHWincklerWGuttmanMLanderES 2011 Integrative genomics viewer. Nat Biotechnol 29 24 26

91. BerrizGFKingODBryantBSanderCRothFP 2003 Characterizing gene sets with FuncAssociate. Bioinformatics 19 2502 2504

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2012 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

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#