Nucleosomes Shape DNA Polymorphism and Divergence


In eukaryotic cells, the majority of DNA is packaged in nucleosomes comprised of ∼147 bp of DNA wound tightly around the highly conserved histone octamer. Nucleosomal DNA from diverse organisms shows an anti-correlated ∼10 bp periodicity of AT-rich and GC-rich dinucleotides. These sequence features influence DNA bending and shape, facilitating structural interactions. We asked whether natural selection mediated through the periodic sequence preferences of nucleosomes shapes the evolution of non-protein-coding regions of D. melanogaster by examining the inter- and intra-species genomic variation relative to these fundamental chromatin building blocks. The sequence changes across nucleosome-bound regions on the melanogaster lineage mirror the observed nucleosome dinucleotide periodicities. Importantly, we show that the frequencies of polymorphisms in natural populations vary across these regions, paralleling divergence, with higher frequencies of preferred alleles. These patterns are most evident for intronic regions and indicate that non-protein coding regions are evolving toward sequences that facilitate the canonical association with the histone core. This result is consistent with the hypothesis that interactions between DNA and the core have systematic impacts on function that are subject to natural selection and are not solely due to mutational bias. These ubiquitous interactions with the histone core partially account for the evolutionary constraint observed in unannotated genomic regions, and may drive broad changes in base composition.


Vyšlo v časopise: Nucleosomes Shape DNA Polymorphism and Divergence. PLoS Genet 10(7): e32767. doi:10.1371/journal.pgen.1004457
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pgen.1004457

Souhrn

In eukaryotic cells, the majority of DNA is packaged in nucleosomes comprised of ∼147 bp of DNA wound tightly around the highly conserved histone octamer. Nucleosomal DNA from diverse organisms shows an anti-correlated ∼10 bp periodicity of AT-rich and GC-rich dinucleotides. These sequence features influence DNA bending and shape, facilitating structural interactions. We asked whether natural selection mediated through the periodic sequence preferences of nucleosomes shapes the evolution of non-protein-coding regions of D. melanogaster by examining the inter- and intra-species genomic variation relative to these fundamental chromatin building blocks. The sequence changes across nucleosome-bound regions on the melanogaster lineage mirror the observed nucleosome dinucleotide periodicities. Importantly, we show that the frequencies of polymorphisms in natural populations vary across these regions, paralleling divergence, with higher frequencies of preferred alleles. These patterns are most evident for intronic regions and indicate that non-protein coding regions are evolving toward sequences that facilitate the canonical association with the histone core. This result is consistent with the hypothesis that interactions between DNA and the core have systematic impacts on function that are subject to natural selection and are not solely due to mutational bias. These ubiquitous interactions with the histone core partially account for the evolutionary constraint observed in unannotated genomic regions, and may drive broad changes in base composition.


Zdroje

1. LeeW, TilloD, BrayN, MorseRH, DavisRW, et al. (2007) A high-resolution atlas of nucleosome occupancy in yeast. Nat Genet 39: 1235–1244.

2. PhamCD, HeX, SchnitzlerGR (2010) Divergent human remodeling complexes remove nucleosomes from strong positioning sequences. Nucleic Acids Res 38: 400–413.

3. MoshkinYM, ChalkleyGE, KanTW, ReddyBA, OzgurZ, et al. (2012) Remodelers organize cellular chromatin by counteracting intrinsic histone-DNA sequence preferences in a class-specific manner. Mol Cell Biol 32: 675–688.

4. LowaryPT, WidomJ (1998) New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J Mol Biol 276: 19–42.

5. ThastromA, LowaryPT, WidlundHR, CaoH, KubistaM, et al. (1999) Sequence motifs and free energies of selected natural and non-natural nucleosome positioning DNA sequences. J Mol Biol 288: 213–229.

6. KaplanN, MooreI, Fondufe-MittendorfY, GossettAJ, TilloD, et al. (2010) Nucleosome sequence preferences influence in vivo nucleosome organization. Nat Struct Mol Biol 17: 918–920 author reply 920–912.

7. KaplanN, MooreIK, Fondufe-MittendorfY, GossettAJ, TilloD, et al. (2009) The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458: 362–366.

8. Radman-LivajaM, RandoOJ (2010) Nucleosome positioning: how is it established, and why does it matter? Dev Biol 339: 258–266.

9. WidomJ (2001) Role of DNA sequence in nucleosome stability and dynamics. Q Rev Biophys 34: 269–324.

10. SegalE, Fondufe-MittendorfY, ChenL, ThastromA, FieldY, et al. (2006) A genomic code for nucleosome positioning. Nature 442: 772–778.

11. MavrichTN, JiangC, IoshikhesIP, LiX, VentersBJ, et al. (2008) Nucleosome organization in the Drosophila genome. Nature 453: 358–362.

12. IoshikhesIP, AlbertI, ZantonSJ, PughBF (2006) Nucleosome positions predicted through comparative genomics. Nat Genet 38: 1210–1215.

13. GaffneyDJ, McVickerG, PaiAA, Fondufe-MittendorfYN, LewellenN, et al. (2012) Controls of nucleosome positioning in the human genome. PLoS Genet 8: e1003036.

14. SatchwellSC, DrewHR, TraversAA (1986) Sequence periodicities in chicken nucleosome core DNA. J Mol Biol 191: 659–675.

15. AnselmiC, BocchinfusoG, De SantisP, SavinoM, ScipioniA (1999) Dual role of DNA intrinsic curvature and flexibility in determining nucleosome stability. J Mol Biol 286: 1293–1301.

16. DrewHR, TraversAA (1985) DNA bending and its relation to nucleosome positioning. J Mol Biol 186: 773–790.

17. ShraderTE, CrothersDM (1989) Artificial nucleosome positioning sequences. Proc Natl Acad Sci U S A 86: 7418–7422.

18. RohsR, WestSM, SosinskyA, LiuP, MannRS, et al. (2009) The role of DNA shape in protein-DNA recognition. Nature 461: 1248–1253.

19. WestSM, RohsR, MannRS, HonigB (2010) Electrostatic interactions between arginines and the minor groove in the nucleosome. J Biomol Struct Dyn 27: 861–866.

20. JiangC, PughBF (2009) Nucleosome positioning and gene regulation: advances through genomics. Nat Rev Genet 10: 161–172.

21. ZhangY, MoqtaderiZ, RattnerBP, EuskirchenG, SnyderM, et al. (2009) Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo. Nat Struct Mol Biol 16: 847–852.

22. ValouevA, JohnsonSM, BoydSD, SmithCL, FireAZ, et al. (2011) Determinants of nucleosome organization in primary human cells. Nature 474: 516–520.

23. BrogaardK, XiL, WangJP, WidomJ (2012) A map of nucleosome positions in yeast at base-pair resolution. Nature 486: 496–501.

24. ZhangZ, WippoCJ, WalM, WardE, KorberP, et al. (2011) A packing mechanism for nucleosome organization reconstituted across a eukaryotic genome. Science 332: 977–980.

25. FieldY, KaplanN, Fondufe-MittendorfY, MooreIK, SharonE, et al. (2008) Distinct modes of regulation by chromatin encoded through nucleosome positioning signals. PLoS Comput Biol 4: e1000216.

26. TilloD, HughesTR (2009) G+C content dominates intrinsic nucleosome occupancy. BMC Bioinformatics 10: 442.

27. SekingerEA, MoqtaderiZ, StruhlK (2005) Intrinsic histone-DNA interactions and low nucleosome density are important for preferential accessibility of promoter regions in yeast. Mol Cell 18: 735–748.

28. AlbertI, MavrichTN, TomshoLP, QiJ, ZantonSJ, et al. (2007) Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature 446: 572–576.

29. CuiF, ColeHA, ClarkDJ, ZhurkinVB (2012) Transcriptional activation of yeast genes disrupts intragenic nucleosome phasing. Nucleic Acids Res 40: 10753–10764.

30. BowmanGD (2010) Mechanisms of ATP-dependent nucleosome sliding. Curr Opin Struct Biol 20: 73–81.

31. WrightS (1931) Evolution in Mendelian Populations. Genetics 16: 97–159.

32. BulmerM (1991) The selection-mutation-drift theory of synonymous codon usage. Genetics 129: 897–907.

33. HartlDL, MoriyamaEN, SawyerSA (1994) Selection intensity for codon bias. Genetics 138: 227–234.

34. AkashiH (1994) Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics 136: 927–935.

35. AkashiH (1996) Molecular evolution between Drosophila melanogaster and D. simulans: reduced codon bias, faster rates of amino acid substitution, and larger proteins in D. melanogaster. Genetics 144: 1297–1307.

36. SasakiS, MelloCC, ShimadaA, NakataniY, HashimotoS-I, et al. (2009) Chromatin-associated periodicity in genetic variation downstream of transcriptional start sites. Science (New York, NY) 323: 401–404.

37. TolstorukovMY, VolfovskyN, StephensRM, ParkPJ (2011) Impact of chromatin structure on sequence variability in the human genome. Nature Structural & Molecular Biology 18: 510–515.

38. PrendergastJ, SempleC (2011) Widespread signatures of recent selection linked to nucleosome positioning in the human lineage. Genome Research 21: 1777–1877.

39. WashietlS, MachneR, GoldmanN (2008) Evolutionary footprints of nucleosome positions in yeast. Trends Genet 24: 583–587.

40. BabbittGA, CotterCR (2011) Functional conservation of nucleosome formation selectively biases presumably neutral molecular variation in yeast genomes. Genome Biol Evol 3: 15–22.

41. BabbittGA, KimY (2008) Inferring Natural Selection on Fine-Scale Chromatin Organization in Yeast. Molecular Biology and Evolution 25: 1714–1727.

42. BabbittGA, TolstorukovMY, KimY (2010) The molecular evolution of nucleosome positioning through sequence-dependent deformation of the DNA polymer. J Biomol Struct Dyn 27: 765–780.

43. WarneckeT, BatadaNN, HurstLD (2008) The impact of the nucleosome code on protein-coding sequence evolution in yeast. PLoS Genet 4: e1000250.

44. ChenX, ChenZ, ChenH, SuZ, YangJ, et al. (2012) Nucleosomes suppress spontaneous mutations base-specifically in eukaryotes. Science 335: 1235–1238.

45. JavaidS, ManoharM, PunjaN, MooneyA, OttesenJJ, et al. (2009) Nucleosome remodeling by hMSH2-hMSH6. Mol Cell 36: 1086–1094.

46. LiF, TianL, GuL, LiGM (2009) Evidence that nucleosomes inhibit mismatch repair in eukaryotic cells. J Biol Chem 284: 33056–33061.

47. HinzJM, RodriguezY, SmerdonMJ (2010) Rotational dynamics of DNA on the nucleosome surface markedly impact accessibility to a DNA repair enzyme. Proc Natl Acad Sci U S A 107: 4646–4651.

48. RodriguezY, SmerdonMJ (2013) The structural location of DNA lesions in nucleosome core particles determines accessibility by base excision repair enzymes. J Biol Chem 288: 13863–13875.

49. WangJ, ZhuangJ, IyerS, LinX, WhitfieldTW, et al. (2012) Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome Res 22: 1798–1812.

50. PeckhamHE, ThurmanRE, FuY, StamatoyannopoulosJA, NobleWS, et al. (2007) Nucleosome positioning signals in genomic DNA. Genome Res 17: 1170–1177.

51. AllanJ, FraserRM, Owen-HughesT, Keszenman-PereyraD (2012) Micrococcal nuclease does not substantially bias nucleosome mapping. J Mol Biol 417: 152–164.

52. PohYP, TingCT, FuHW, LangleyCH, BegunDJ (2012) Population Genomic Analysis of Base Composition Evolution in Drosophila melanogaster. Genome Biol Evol 4: 1245–1255.

53. MoriyamaEN, PowellJR (1996) Intraspecific nuclear DNA variation in Drosophila. Mol Biol Evol 13: 261–277.

54. KeightleyPD, TrivediU, ThomsonM, OliverF, KumarS, et al. (2009) Analysis of the genome sequences of three Drosophila melanogaster spontaneous mutation accumulation lines. Genome Res 19: 1195–1201.

55. DaveyCA, SargentDF, LugerK, MaederAW, RichmondTJ (2002) Solvent Mediated Interactions in the Structure of the Nucleosome Core Particle at 1.9 a Resolution. Journal of Molecular Biology 319: 1097–1113.

56. ChuaEY, VasudevanD, DaveyGE, WuB, DaveyCA (2012) The mechanics behind DNA sequence-dependent properties of the nucleosome. Nucleic Acids Res 40: 6338–6352.

57. IkemuraT (1982) Correlation between the abundance of yeast transfer RNAs and the occurrence of the respective codons in protein genes. Differences in synonymous codon choice patterns of yeast and Escherichia coli with reference to the abundance of isoaccepting transfer RNAs. J Mol Biol 158: 573–597.

58. DuretL (2002) Evolution of synonymous codon usage in metazoans. Curr Opin Genet Dev 12: 640–649.

59. TajimaF (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.

60. WatersonGA (1974) The Sampling Theory of Selectively Neutral Alleles. Advances in Applied Probability 6: 463–488.

61. McVeanGAT, CharlesworthB (1999) A Population Genetic Model for the Evolution of Synonymous Codon Usage: Patterns and Predictions. Genetics Research 74: 145–158.

62. SawyerSA, HartlDL (1992) Population genetics of polymorphism and divergence. Genetics 132: 1161–1176.

63. WrightS (1938) The Distribution of Gene Frequencies Under Irreversible Mutation. Proc Natl Acad Sci U S A 24: 253–259.

64. WallJD, PrzeworskiM (2000) When did the human population size start increasing? Genetics 155: 1865–1874.

65. LangleyCH, StevensK, CardenoC, LeeYC, SchriderDR, et al. (2012) Genomic Variation in Natural Populations of Drosophila melanogaster. Genetics 192: 533–598.

66. HernandezRD, WilliamsonSH, BustamanteCD (2007) Context dependence, ancestral misidentification, and spurious signatures of natural selection. Mol Biol Evol 24: 1792–1800.

67. HalliganDL, KeightleyPD (2006) Ubiquitous selective constraints in the Drosophila genome revealed by a genome-wide interspecies comparison. Genome Res 16: 875–884.

68. CasillasS, BarbadillaA, BergmanCM (2007) Purifying selection maintains highly conserved noncoding sequences in Drosophila. Mol Biol Evol 24: 2222–2234.

69. CharlesworthB (2012) The effects of deleterious mutations on evolution at linked sites. Genetics 190: 5–22.

70. BravermanJM, HudsonRR, KaplanNL, LangleyCH, StephanW (1995) The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics 140: 783–796.

71. PoolJE, Corbett-DetigRB, SuginoRP, StevensKA, CardenoCM, et al. (2012) Population Genomics of Sub-Saharan Drosophila melanogaster: African Diversity and Non-African Admixture. PLoS Genet 8: e1003080.

72. BegunDJ, WhitleyP (2002) Molecular population genetics of Xdh and the evolution of base composition in Drosophila. Genetics 162: 1725–1735.

73. SchopfB, BregenhornS, QuivyJP, KadyrovFA, AlmouzniG, et al. (2012) Interplay between mismatch repair and chromatin assembly. Proc Natl Acad Sci U S A 109: 1895–1900.

74. GaillardH, FitzgeraldDJ, SmithCL, PetersonCL, RichmondTJ, et al. (2003) Chromatin remodeling activities act on UV-damaged nucleosomes and modulate DNA damage accessibility to photolyase. J Biol Chem 278: 17655–17663.

75. JagannathanI, PepenellaS, HayesJJ (2011) Activity of FEN1 endonuclease on nucleosome substrates is dependent upon DNA sequence but not flap orientation. J Biol Chem 286: 17521–17529.

76. YeY, StahleyMR, XuJ, FriedmanJI, SunY, et al. (2012) Enzymatic excision of uracil residues in nucleosomes depends on the local DNA structure and dynamics. Biochemistry 51: 6028–6038.

77. LykoF, RamsahoyeBH, JaenischR (2000) DNA methylation in Drosophila melanogaster. Nature 408: 538–540.

78. HwangDG, GreenP (2004) Bayesian Markov chain Monte Carlo sequence analysis reveals varying neutral substitution patterns in mammalian evolution. Proc Natl Acad Sci U S A 101: 13994–14001.

79. NagylakiT (1983) Evolution of a large population under gene conversion. Proc Natl Acad Sci U S A 80: 5941–5945.

80. BirdsellJA (2002) Integrating genomics, bioinformatics, and classical genetics to study the effects of recombination on genome evolution. Mol Biol Evol 19: 1181–1197.

81. GaltierN, BazinE, BierneN (2006) GC-biased segregation of noncoding polymorphisms in Drosophila. Genetics 172: 221–228.

82. LiQ, WrangeO (1995) Accessibility of a glucocorticoid response element in a nucleosome depends on its rotational positioning. Mol Cell Biol 15: 4375–4384.

83. TilgnerH, NikolaouC, AlthammerS, SammethM, BeatoM, et al. (2009) Nucleosome positioning as a determinant of exon recognition. Nat Struct Mol Biol 16: 996–1001.

84. KwakH, FudaNJ, CoreLJ, LisJT (2013) Precise maps of RNA polymerase reveal how promoters direct initiation and pausing. Science 339: 950–953.

85. LiXY, MacArthurS, BourgonR, NixD, PollardDA, et al. (2008) Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm. PLoS Biol 6: e27.

86. CelnikerSE, WheelerDA, KronmillerB, CarlsonJW, HalpernA, et al. (2002) Finishing a whole-genome shotgun: release 3 of the Drosophila melanogaster euchromatic genome sequence. Genome Biol 3: RESEARCH0079.

87. RiddleNC, MinodaA, KharchenkoPV, AlekseyenkoAA, SchwartzYB, et al. (2011) Plasticity in patterns of histone modifications and chromosomal proteins in Drosophila heterochromatin. Genome Research 21: 147–163.

88. R Development Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing

89. Schrödinger L The PyMOL Molecular Graphics System, Version 1.5.0.4

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