Genome-Wide Nucleosome Positioning Is Orchestrated by Genomic Regions Associated with DNase I Hypersensitivity in Rice
The fundamental unit of chromatin is the nucleosome, which consists of 147 bp of DNA wrapped around a histone octamer containing four core histones (H3, H4, H2A, and H2B). Nucleosome positioning in the genome affects the DNA accessibility for regulatory proteins, and thus is critical for gene expression and regulation. Genomic regions associated with regulatory proteins are associated with a pronounced sensitivity to DNase I digestion, and are thus called DNase I hypersensitive sites (DHSs). It is well known that only a subset of nucleosomes are reproducibly positioned in eukaryotic genomes. However, it is less clear what factors determine genome-wide nucleosome positioning, especially in intergenic regions. We mapped both nucleosome positioning and DHS datasets across the rice genome. We discovered that DHSs located in a variety of contexts, both genic and intergenic, were flanked by strongly phased nucleosome arrays. We confirmed the same association of DHSs with phased nucleosomes in the human genome. We conclude that genomic loci associated with a diverse set of regulatory proteins are major determinants of nucleosome phasing, and this is true in both genic and intergenic regions.
Vyšlo v časopise:
Genome-Wide Nucleosome Positioning Is Orchestrated by Genomic Regions Associated with DNase I Hypersensitivity in Rice. PLoS Genet 10(5): e32767. doi:10.1371/journal.pgen.1004378
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004378
Souhrn
The fundamental unit of chromatin is the nucleosome, which consists of 147 bp of DNA wrapped around a histone octamer containing four core histones (H3, H4, H2A, and H2B). Nucleosome positioning in the genome affects the DNA accessibility for regulatory proteins, and thus is critical for gene expression and regulation. Genomic regions associated with regulatory proteins are associated with a pronounced sensitivity to DNase I digestion, and are thus called DNase I hypersensitive sites (DHSs). It is well known that only a subset of nucleosomes are reproducibly positioned in eukaryotic genomes. However, it is less clear what factors determine genome-wide nucleosome positioning, especially in intergenic regions. We mapped both nucleosome positioning and DHS datasets across the rice genome. We discovered that DHSs located in a variety of contexts, both genic and intergenic, were flanked by strongly phased nucleosome arrays. We confirmed the same association of DHSs with phased nucleosomes in the human genome. We conclude that genomic loci associated with a diverse set of regulatory proteins are major determinants of nucleosome phasing, and this is true in both genic and intergenic regions.
Zdroje
1. LugerK, MaderAW, RichmondRK, SargentDF, RichmondTJ (1997) Crystal structure of the nucleosome core particle at 2.8 angstrom resolution. Nature 389: 251–260.
2. BellO, TiwariVK, ThomaNH, SchubelerD (2011) Determinants and dynamics of genome accessibility. Nat Rev Genet 12: 554–564.
3. MavrichTN, IoshikhesIP, VentersBJ, JiangC, TomshoLP, et al. (2008) A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res 18: 1073–1083.
4. LockeG, TolkunovD, MoqtaderiZ, StruhlK, MorozovAV (2010) High-throughput sequencing reveals a simple model of nucleosome energetics. Proc Natl Acad Sci USA 107: 20998–21003.
5. ValouevA, JohnsonSM, BoydSD, SmithCL, FireAZ, et al. (2011) Determinants of nucleosome organization in primary human cells. Nature 474: 516–520.
6. StruhlK, SegalE (2013) Determinants of nucleosome positioning. Nat Struct Mol Biol 20: 267–273.
7. KaplanN, MooreIK, Fondufe-MittendorfY, GossettAJ, TilloD, et al. (2009) The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458: 362–366.
8. 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.
9. SegalE, Fondufe-MittendorfY, ChenLY, ThastromA, FieldY, et al. (2006) A genomic code for nucleosome positioning. Nature 442: 772–778.
10. GaffneyDJ, McVickerG, PaiAA, Fondufe-MittendorfYN, LewellenN, et al. (2012) Controls of nucleosome positioning in the human genome. PLoS Genet 8: e1003036.
11. YuanGC, LiuYJ, DionMF, SlackMD, WuLF, et al. (2005) Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309: 626–630.
12. MavrichTN, JiangCZ, IoshikhesIP, LiXY, VentersBJ, et al. (2008) Nucleosome organization in the Drosophila genome. Nature 453: 358–362.
13. SchonesDE, CuiKR, CuddapahS, RohTY, BarskiA, et al. (2008) Dynamic regulation of nucleosome positioning in the human genome. Cell 132: 887–898.
14. SasakiS, MelloCC, ShimadaA, NakataniY, HashimotoSI, et al. (2009) Chromatin-associated periodicity in genetic variation downstream of transcriptional start sites. Science 323: 401–404.
15. HughesAL, JinY, RandoOJ, StruhlK (2012) A functional evolutionary approach to identify determinants of nucleosome positioning: A unifying model for establishing the genome-wide pattern. Mol Cell 48: 5–15.
16. MatsumotoT, WuJZ, KanamoriH, KatayoseY, FujisawaM, et al. (2005) The map-based sequence of the rice genome. Nature 436: 793–800.
17. LiXY, WangXF, HeK, MaYQ, SuN, et al. (2008) High-resolution mapping of epigenetic modifications of the rice genome uncovers interplay between DNA methylation, histone methylation, and gene expression. Plant Cell 20: 259–276.
18. WangL, XieWB, ChenY, TangWJ, YangJY, et al. (2010) A dynamic gene expression atlas covering the entire life cycle of rice. Plant J 61: 752–766.
19. FengSH, CokusSJ, ZhangXY, ChenPY, BostickM, et al. (2010) Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci USA 107: 8689–8694.
20. HeGM, ZhuXP, EllingAA, ChenLB, WangXF, et al. (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell 22: 17–33.
21. YanHH, KikuchiS, NeumannP, ZhangWL, WuYF, et al. (2010) Genome-wide mapping of cytosine methylation revealed dynamic DNA methylation patterns associated with genes and centromeres in rice. Plant J 63: 353–365.
22. ZemachA, McDanielIE, SilvaP, ZilbermanD (2010) Genome-Wide Evolutionary Analysis of Eukaryotic DNA Methylation. Science 328: 916–919.
23. ThurmanRE, RynesE, HumbertR, VierstraJ, MauranoMT, et al. (2012) The accessible chromatin landscape of the human genome. Nature 489: 75–82.
24. ZhangWL, WuYF, SchnableJC, ZengZX, FreelingM, et al. (2012) High-resolution mapping of open chromatin in the rice genome. Genome Res 22: 151–162.
25. JiaoYQ, WangYH, XueDW, WangJ, YanMX, et al. (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42: 541–U536.
26. LuZF, YuH, XiongGS, WangJ, JiaoYQ, et al. (2013) Genome-wide binding analysis of the transcription activator IDEAL PLANT ARCHITECTURE1 reveals a complex network regulating rice plant architecture. Plant Cell 25: 3743–3759.
27. JinCY, ZangCZ, WeiG, CuiKR, PengWQ, et al. (2009) H3.3/H2A.Z double variant-containing nucleosomes mark 'nucleosome-free regions' of active promoters and other regulatory regions. Nat Genet 41: 941–945.
28. HenikoffS, HenikoffJG, SakaiA, LoebGB, AhmadK (2009) Genome-wide profiling of salt fractions maps physical properties of chromatin. Genome Res 19: 460–469.
29. ZhangY, VastenhouwNL, FengJX, FuK, WangCF, et al. (2014) Canonical nucleosome organization at promoters forms during genome activation. Genome Res 24: 260–266.
30. HeintzmanND, HonGC, HawkinsRD, KheradpourP, StarkA, et al. (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459: 108–112.
31. BarskiA, CuddapahS, CuiKR, RohTY, SchonesDE, et al. (2007) High-resolution profiling of histone methylations in the human genome. Cell 129: 823–837.
32. BoyleAP, DavisS, ShulhaHP, MeltzerP, MarguliesEH, et al. (2008) High-resolution mapping and characterization of open chromatin across the genome. Cell 132: 311–322.
33. LeeW, TilloD, BrayN, MorseRH, DavisRW, et al. (2007) A high-resolution atlas of nucleosome occupancy in yeast. Nat Genet 39: 1235–1244.
34. ShivaswamyS, BhingeA, ZhaoYJ, JonesS, HirstM, et al. (2008) Dynamic remodeling of individual nucleosomes across a eukaryotic genome in response to transcriptional perturbation. PLoS Biol 6: 618–630.
35. BrogaardK, XiLQ, WangJP, WidomJ (2012) A map of nucleosome positions in yeast at base-pair resolution. Nature 486: 496–501.
36. ValouevA, IchikawaJ, TonthatT, StuartJ, RanadeS, et al. (2008) A high-resolution, nucleosome position map of C. elegans reveals a lack of universal sequence-dictated positioning. Genome Res 18: 1051–1063.
37. ChodavarapuRK, FengSH, BernatavichuteYV, ChenPY, StroudH, et al. (2010) Relationship between nucleosome positioning and DNA methylation. Nature 466: 388–392.
38. WeinerA, HughesA, YassourM, RandoOJ, FriedmanN (2010) High-resolution nucleosome mapping reveals transcription-dependent promoter packaging. Genome Res 20: 90–100.
39. GkikopoulosT, SchofieldP, SinghV, PinskayaM, MellorJ, et al. (2011) A role for Snf2-related nucleosome-spacing enzymes in genome-wide nucleosome organization. Science 333: 1758–1760.
40. ZhangZH, WippoCJ, WalM, WardE, KorberP, et al. (2011) A packing mechanism for nucleosome organization reconstituted across a eukaryotic genome. Science 332: 977–980.
41. YenKY, VinayachandranV, BattaK, KoerberRT, PughBF (2012) Genome-wide nucleosome specificity and directionality of chromatin remodelers. Cell 149: 1461–1473.
42. TolstorukovMY, SansamCG, LuP, KoellhofferEC, HelmingKC, et al. (2013) Swi/Snf chromatin remodeling/tumor suppressor complex establishes nucleosome occupancy at target promoters. Proc Natl Acad Sci USA 110: 10165–10170.
43. KornbergRD, StryerL (1988) Statistical distributions of nucleosomes - Nonrandom locations by a stochastic mechanism. Nucleic Acids Res 16: 6677–6690.
44. FuYT, SinhaM, PetersonCL, WengZP (2008) The insulator binding protein CTCF positions 20 nucleosomes around its binding sites across the human genome. PLoS Genet 4: e1000138.
45. LiXY, ThomasS, SaboPJ, EisenMB, StamatoyannopoulosJA, et al. (2011) The role of chromatin accessibility in directing the widespread, overlapping patterns of Drosophila transcription factor binding. Genome Biol 12: 17.
46. ZhangWL, ZhangT, WuYF, JiangJM (2012) Genome-wide identification of regulatory DNA elements and protein-binding footprints using signatures of open chromatin in Arabidopsis. Plant Cell 24: 2719–2731.
47. LiH, RuanJ, DurbinR (2008) Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res 18: 1851–1858.
48. BoyleAP, GuinneyJ, CrawfordGE, FureyTS (2008) F-Seq: a feature density estimator for high-throughput sequence tags. Bioinformatics 24: 2537–2538.
49. FloresO, OrozcoM (2011) nucleR: a package for non-parametric nucleosome positioning. Bioinformatics 27: 2149–2150.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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