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Analysis of Transposon Interruptions Suggests Selection for L1 Elements on the X Chromosome


It has been hypothesised that the massive accumulation of L1 transposable elements on the X chromosome is due to their function in X inactivation, and that the accumulation of Alu elements near genes is adaptive. We tested the possible selective advantage of these two transposable element (TE) families with a novel method, interruption analysis. In mammalian genomes, a large number of TEs interrupt other TEs due to the high overall abundance and age of repeats, and these interruptions can be used to test whether TEs are selectively neutral. Interruptions of TEs, which are beneficial for the host, are expected to be deleterious and underrepresented compared with neutral ones. We found that L1 elements in the regions of the X chromosome that contain the majority of the inactivated genes are significantly less frequently interrupted than on the autosomes, while L1s near genes that escape inactivation are interrupted with higher frequency, supporting the hypothesis that L1s on the X chromosome play a role in its inactivation. In addition, we show that TEs are less frequently interrupted in introns than in intergenic regions, probably due to selection against the expansion of introns, but the insertion pattern of Alus is comparable to other repeats.


Vyšlo v časopise: Analysis of Transposon Interruptions Suggests Selection for L1 Elements on the X Chromosome. PLoS Genet 4(8): e32767. doi:10.1371/journal.pgen.1000172
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1000172

Souhrn

It has been hypothesised that the massive accumulation of L1 transposable elements on the X chromosome is due to their function in X inactivation, and that the accumulation of Alu elements near genes is adaptive. We tested the possible selective advantage of these two transposable element (TE) families with a novel method, interruption analysis. In mammalian genomes, a large number of TEs interrupt other TEs due to the high overall abundance and age of repeats, and these interruptions can be used to test whether TEs are selectively neutral. Interruptions of TEs, which are beneficial for the host, are expected to be deleterious and underrepresented compared with neutral ones. We found that L1 elements in the regions of the X chromosome that contain the majority of the inactivated genes are significantly less frequently interrupted than on the autosomes, while L1s near genes that escape inactivation are interrupted with higher frequency, supporting the hypothesis that L1s on the X chromosome play a role in its inactivation. In addition, we show that TEs are less frequently interrupted in introns than in intergenic regions, probably due to selection against the expansion of introns, but the insertion pattern of Alus is comparable to other repeats.


Zdroje

1. MedstrandP

van de LagemaatLN

DunnCA

LandryJR

SvenbackD

2005 Impact of transposable elements on the evolution of mammalian gene regulation. Cytogenetic and Genome Research 110 342 352

2. van de LagemaatLN

LandryJR

MagerDL

MedstrandP

2003 Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. Trends in Genetics 19 530 536

3. FeschotteC

PrithamEJ

2007 DNA transposons and the evolution of eukaryotic genomes. Annual Review of Genetics 41 331 368

4. JurkaJ

KapitonovVV

KohanyO

JurkaMV

2007 Repetitive Sequences in Complex Genomes: Structure and Evolution. Annu Rev Genomics Hum Genet

5. BejeranoG

SiepelAC

KentWJ

HausslerD

2005 Computational screening of conserved genomic DNA in search of functional noncoding elements. Nature Methods 2 535 545

6. LoweCB

BejeranoG

HausslerD

2007 Thousands of human mobile element fragments undergo strong purifying selection near developmental genes. Proc Natl Acad Sci U S A 104 8005 8010

7. JordanIK

RogozinIB

GlazkoGV

KooninEV

2003 Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends in Genetics 19 68 72

8. Marino-RamirezL

LewisKC

LandsmanD

JordanIK

2005 Transposable elements donate lineage-specific regulatory sequences to host genomes. Cytogenetic and Genome Research 110 333 341

9. BirneyE

StamatoyannopoulosJA

DuttaA

GuigoR

GingerasTR

2007 Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447 799 816

10. MarguliesEH

CooperGM

AsimenosG

ThomasDJ

DeweyCN

2007 Analyses of deep mammalian sequence alignments and constraint predictions for 1% of the human genome. Genome Res 17 760 774

11. SimonsC

PheasantM

MakuninIV

MattickJS

2006 Transposon-free regions in mammalian genomes. Genome Research 16 164 172

12. LyonMF

1998 X-chromosome inactivation: a repeat hypothesis. Cytogenetics and Cell Genetics 80 133 137

13. PavlicekA

JabbariK

PacesJ

PacesV

HejnarJ

2001 Similar integration but different stability of Alus and LINEs in the human genome. Gene 276 39 45

14. IHGSC 2001 Initial sequencing and analysis of the human genome. Nature 409 860 921

15. MarguliesEH

MaduroVVB

ThomasPJ

TomkinsJP

AmemiyaCT

2005 Comparative sequencing provides insights about the structure and conservation of marsupial and monotreme genomes. Proceedings of the National Academy of Sciences of the United States of America 102 3354 3359

16. BergmanCM

QuesnevilleH

AnxolabehereD

AshburnerM

2006 Recurrent insertion and duplication generate networks of transposable element sequences in the Drosophila melanogaster genome. Genome Biology 7

17. KriegsJO

MatzkeA

ChurakovG

KuritzinA

MayrG

2007 Waves of genomic hitchhikers shed light on the evolution of gamebirds (Aves : Galliformes). Bmc Evolutionary Biology 7

18. ChurakovG

SmitAFA

BrosiusJ

SchmitzB

2005 A novel abundant family of retroposed elements (DAS-SINEs) in the nine-banded armadillo (Dasypus novemcinctus). Molecular Biology and Evolution 22 886 893

19. PaceJK

FeschotteC

2007 The evolutionary history of human DNA transposons: Evidence for intense activity in the primate lineage. Genome Research 17 422 432

20. GiordanoJ

GeY

GelfandY

AbrusanG

BensonG

2007 Evolutionary history of mammalian transposons determined by genome-wide defragmentation. PLoS Computational Biology 3 e137

21. ArndtPF

HwaT

PetrovDA

2005 Substantial regional variation in substitution rates in the human genome: Importance of GC content, gene density, and telomere-specific effects. Journal of Molecular Evolution 60 748 U728

22. WebsterMT

AxelssonE

EllegrenH

2006 Strong regional biases in nucleotide substitution in the chicken genome. Molecular Biology and Evolution 23 1203 1216

23. ICGSC 2004 Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432 695 716

24. AxelssonE

WebsterMT

SmithNGC

BurtDW

EllegrenH

2005 Comparison of the chicken and turkey genomes reveals a higher rate of nucleotide divergence on microchromosomes than macrochromosomes. Genome Research 15 120 125

25. RossMT

GrafhamDV

CoffeyAJ

SchererS

McLayK

2005 The DNA sequence of the human X chromosome. Nature 434 325 337

26. HandleyLL

CeplitisH

EllegrenH

2004 Evolutionary strata on the chicken Z chromosome: Implications for sex chromosome evolution. Genetics 167 367 376

27. PlathK

Mlynarczyk-EvansS

NusinowDA

PanningB

2002 Xist RNA and the mechanism of X chromosome inactivation. Annual Review of Genetics 36 233 278

28. ChowJC

YenZ

ZiescheSM

BrownCJ

2005 Silencing of the mammalian X chromosome. Annual Review of Genomics and Human Genetics 6 69 92

29. DuretL

ChureauC

SamainS

WeissenbachJ

AvnerP

2006 The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene. Science 312 1653 1655

30. MikkelsenTS

WakefieldMJ

AkenB

AmemiyaCT

ChangJL

2007 Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences. Nature 447 167 U161

31. BrownCJ

HendrichBD

RupertJL

LafreniereRG

XingY

1992 The Human Xist Gene - Analysis of a 17 Kb Inactive X-Specific Rna That Contains Conserved Repeats and Is Highly Localized within the Nucleus. Cell 71 527 542

32. ChureauC

PrissetteM

BourdetA

BarbeV

CattolicoL

2002 Comparative sequence analysis of the X-inactivation center region in mouse, human, and bovine. Genome Research 12 894 908

33. CarrelL

WillardHF

2005 X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434 400 404

34. BaileyJA

CarrelL

ChakravartiA

EichlerEE

2000 Molecular evidence for a relationship between LINE-1 elements and X chromosome inactivation: The Lyon repeat hypothesis. Proceedings of the National Academy of Sciences of the United States of America 97 6634 6639

35. CarrelL

ParkC

TyekuchevaS

DunnJ

ChiaromonteF

2006 Genomic environment predicts expression patterns on the human inactive X chromosome. Plos Genetics 2 1477 1486

36. WangZ

WillardHF

MukherjeeS

FureyTS

2006 Evidence of influence of genomic DNA sequence on human X chromosome inactivation. Plos Computational Biology 2 979 988

37. JurkaJ

2004 Evolutionary impact of human Alu repetitive elements. Current Opinion in Genetics & Development 14 603 608

38. DewannieuxM

EsnaultC

HeidmannT

2003 LINE-mediated retrotransposition of marked Alu sequences. Nature Genetics 35 41 48

39. PolakP

DomanyE

2006 Alu elements contain many binding sites for transcription factors and may play a role in regulation of developmental processes. BMC Genomics 7

40. HaslerJ

StrubK

2006 Alu elements as regulators of gene expression. Nucleic Acids Research 34 5491 5497

41. BoissinotS

DavisJ

EntezamA

PetrovD

FuranoAV

2006 Fitness cost of LINE-1 (L1) activity in humans. Proceedings of the National Academy of Sciences of the United States of America 103 9590 9594

42. JurkaJ

KrnjajicM

KapitonovVV

StengerJE

KokhanyyO

2002 Active Alu elements are passed primarily through paternal germlines. Theoretical Population Biology 61 519 530

43. NgK

PullirschD

LeebM

WutzA

2007 Xist and the order of silencing. Embo Reports 8 34 39

44. LyonMF

2003 The lyon and the LINE hypothesis. Seminars in Cell & Developmental Biology 14 313 318

45. AbrusanG

KrambeckHJ

2006 The distribution of L1 and Alu retroelements in relation to GC content on human sex chromosomes is consistent with the ectopic recombination model. Journal of Molecular Evolution 63 484 492

46. SenSK

HanKD

WangJX

LeeJ

WangH

2006 Human genomic deletions mediated by recombination between Alu elements. American Journal of Human Genetics 79 41 53

47. BrookfieldJFY

2001 Selection on Alu sequences? Current Biology 11 R900 R901

48. HackenbergM

Bernaola-GalvanP

CarpenaP

OliverJL

2005 The biased distribution of alus in human isochores might be driven by recombination. Journal of Molecular Evolution 60 365 377

49. MontgomeryEA

HuangSM

LangleyCH

JuddBH

1991 Chromosome Rearrangement by Ectopic Recombination in Drosophila-Melanogaster - Genome Structure and Evolution. Genetics 129 1085 1098

50. HanK

LeeJ

MeyerTJ

WangJ

SenSK

2007 Alu recombination-mediated structural deletions in the chimpanzee genome. Plos Genetics 3 1939 1949

51. SymerDE

ConnellyC

SzakST

CaputoEM

CostGJ

2002 Human L1 retrotransposition is associated with genetic instability in vivo. Cell 110 327 338

52. GilbertN

Lutz-PriggeS

MoranJV

2002 Genomic deletions created upon LINE-1 retrotransposition. Cell 110 315 325

53. Lev-MaorG

SorekR

ShomronN

AstG

2003 The birth of an alternatively spliced exon: 3′ splice-site selection in Alu exons. Science 300 1288 1291

54. SelaN

MerschB

Gal-MarkN

Lev-MaorG

Hotz-WagenblattA

2007 Comparative analysis of transposed element insertion within human and mouse genomes reveals Alu's unique role in shaping the human transcriptome. Genome Biology 8

55. Gal-MarkN

SchwartzS

AstG

2008 Alternative splicing of Alu exons - two arms are better than one. Nucleic Acids Research 36 2012 2023

56. SmitAFA

1999 Interspersed repeats and other mementos of transposable elements in mammalian genomes. Current Opinion in Genetics & Development 9 657 663

57. UrrutiaAO

HurstLD

2003 The signature of selection mediated by expression on human genes. Genome Res 13 2260 2264

58. Castillo-DavisCI

MekhedovSL

HartlDL

KooninEV

KondrashovFA

2002 Selection for short introns in highly expressed genes. Nat Genet 31 415 418

59. ConleyAB

MillerWJ

JordanIK

2008 Human cis natural antisense transcripts initiated by transposable elements. Trends Genet 24 53 56

60. PetrovDA

AminetzachYT

DavisJC

BensassonD

HirshAE

2003 Size matters: Non-LTR retrotransposable elements and ectopic recombination in Drosophila. Molecular Biology and Evolution 20 880 892

61. MGSC 2002 Initial sequencing and comparative analysis of the mouse genome. Nature 420 520 562

62. PetrovDA

SangsterTA

JohnstonJS

HartlDL

ShawKL

2000 Evidence for DNA loss as a determinant of genome size. Science 287 1060 1062

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