The role of nucleosome positioning in the evolution of gene regulation

PLoS Biology

Volumn 8, Issue 7, 2010, Pages

  Tsankov, Alexander M ^a,b   Thompson, Dawn Anne ^a   Socha, Amanda ^a   Regev, Aviv ^a,c,d   Rando, Oliver J ^e  

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b USA   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^e UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN; MESSENGER RNA; DNA DIRECTED RNA POLYMERASE; FUNGAL PROTEIN; PROTEASOME; TRANSCRIPTION FACTOR;

ARTICLE; CHROMATIN STRUCTURE; CONTROLLED STUDY; CYTOSKELETON; FERMENTATION; FUNGAL METABOLISM; FUNGUS GROWTH; GENE EXPRESSION; GENE FUNCTION; GENE MAPPING; GENETIC CONSERVATION; GENETIC REGULATION; GENOME ANALYSIS; HEMIASCOMYCOTA; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOSOME; PROMOTER REGION; REPRESSOR GENE; YEAST; ALTERNATIVE RNA SPLICING; ASCOMYCETES; CHROMOSOME POSITIONING; DNA PACKAGING; ENZYMOLOGY; FUNGAL GENE; GENE DUPLICATION; GENE EXPRESSION REGULATION; GENETICS; MEIOSIS; METABOLISM; MITOCHONDRION; NUCLEAR PORE; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PEROXISOME; PHYLOGENY; SPECIES DIFFERENCE;

ALTERNATIVE SPLICING; ASCOMYCOTA; CHROMOSOME POSITIONING; CONSERVED SEQUENCE; CYTOSKELETON; DNA PACKAGING; DNA-DIRECTED RNA POLYMERASES; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; GENE DUPLICATION; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; MEIOSIS; MITOCHONDRIA; NUCLEAR PORE; NUCLEOSOMES; OPEN READING FRAMES; PEROXISOMES; PHYLOGENY; PROTEASOME ENDOPEPTIDASE COMPLEX; SPECIES SPECIFICITY; TRANSCRIPTION FACTORS;

EID: 77955045449     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1000414     Document Type: Article

References (81)

1. King MC, Wilson AC (1975) Evolution at two levels in humans and chimpanzees. Science 188: 107-116.
2. Thompson DA, Regev A (2009) Fungal regulatory evolution: cis and trans in the balance. FEBS Lett.
3. Wohlbach DJ, Thompson DA, Gasch AP, Regev A (2009) From elements to modules: regulatory evolution in Ascomycota fungi. Curr Opin Genet Dev 19: 571-578.
4. McAdams HH, Srinivasan B, Arkin AP (2004) The evolution of genetic regulatory systems in bacteria. Nat Rev Genet 5: 169-178.
5. Gasch AP, Moses AM, Chiang DY, Fraser HB, Berardini M, et al. (2004) Conservation and evolution of cis-regulatory systems in ascomycete fungi. PLoS Biol 2: e398. doi:10.1371/journal.pbio.0020398.
6. Tirosh I, Weinberger A, Carmi M, Barkai N (2006) A genetic signature of interspecies variations in gene expression. Nat Genet 38: 830-834.
7. Tuch BB, Galgoczy DJ, Hernday AD, Li H, Johnson AD (2008) The evolution of combinatorial gene regulation in fungi. PLoS Biol 6: e38. doi:10.1371/ journal.pbio.0060038.
8. Lavoie H, Hogues H, Mallick J, Sellam A, Nantel A, et al. (2010) Evolutionary tinkering with conserved components of a transcriptional regulatory network. PLoS Biol 8: e1000329. doi:10.1371/journal.pbio.1000329.
9. Prud'homme B, Gompel N, Carroll SB (2007) Emerging principles of regulatory evolution. Proc Natl Acad Sci U S A 104 Suppl 1: 8605-8612.
10. Khaitovich P, Enard W, Lachmann M, Paabo S (2006) Evolution of primate gene expression. Nat Rev Genet 7: 693-702.
11. Kellis M, Birren BW, Lander ES (2004) Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428: 617-624.
12. Conant GC, Wolfe KH (2007) Increased glycolytic flux as an outcome of whole genome duplication in yeast. Mol Syst Biol 3: 129.
13. Kornberg RD, Lorch Y (1999) Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98: 285-294.
14. Radman-Livaja M, Rando OJ (2009) Nucleosome positioning: How is it established, and why does it matter? Dev Biol. 15. Rando OJ, Chang HY (2009) Genome-wide views of chromatin structure. Annu Rev Biochem 78: 245-271.
15. Jiang C, Pugh BF (2009) Nucleosome positioning and gene regulation: advances through genomics. Nat Rev Genet 10: 161-172.
16. Li B, Carey M, Workman JL (2007) The role of chromatin during transcription. Cell 128: 707-719.
17. Venters BJ, Pugh BF (2009) A canonical promoter organization of the transcription machinery and its regulators in the Saccharomyces genome. Genome Res 19: 360-371.
18. Weiner A, Hughes A, Yassour M, Rando OJ, Friedman N (2009) High resolution nucleosome mapping reveals transcription-dependent promoter packaging. Genome Res.
19. Drew HR, Travers AA (1985) DNA bending and its relation to nucleosome positioning. J Mol Biol 186: 773-790.
20. Kaplan N, Moore IK, Fondufe-Mittendorf Y, Gossett AJ, Tillo D, et al. (2008) The DNA-encoded nucleosome organization of a eukaryotic genome. Nature.
21. Sekinger EA, Moqtaderi Z, Struhl K (2005) Intrinsic histone-DNA interactions and low nucleosome density are important for preferential accessibility of promoter regions in yeast. Mol Cell 18: 735-748.
22. Yuan GC, Liu YJ, Dion MF, Slack MD, Wu LF, et al. (2005) Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309: 626-630.
23. Zhang Y, Moqtaderi Z, Rattner BP, Euskirchen G, Snyder M, et al. (2009) Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo. Nat Struct Mol Biol 16: 847-852.
24. Clapier CR, Cairns BR (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78: 273-304.
25. Whitehouse I, Rando OJ, Delrow J, Tsukiyama T (2007) Chromatin remodelling at promoters suppresses antisense transcription. Nature 450: 1031-1035.
26. Brem RB, Yvert G, Clinton R, Kruglyak L (2002) Genetic dissection of transcriptional regulation in budding yeast. Science 296: 752-755.
27. Lee SI, Pe'er D, Dudley AM, Church GM, Koller D (2006) Identifying regulatory mechanisms using individual variation reveals key role for chromatin modification. Proc Natl Acad Sci U S A 103: 14062-14067.
28. Tirosh I, Reikhav S, Levy AA, Barkai N (2009) A yeast hybrid provides insight into the evolution of gene expression regulation. Science 324: 659-662.
29. Tirosh I, Weinberger A, Bezalel D, Kaganovich M, Barkai N (2008) On the relation between promoter divergence and gene expression evolution. Mol Syst Biol 4: 159.
30. Ihmels J, Bergmann S, Gerami-Nejad M, Yanai I, McClellan M, et al. (2005) Rewiring of the yeast transcriptional network through the evolution of motif usage. Science 309: 938-940.
31. Field Y, Fondufe-Mittendorf Y, Moore IK, Mieczkowski P, Kaplan N, et al. (2009) Gene expression divergence in yeast is coupled to evolution of DNA-encoded nucleosome organization. Nat Genet 41: 438-445.
32. Lantermann AB, Straub T, Stralfors A, Yuan GC, Ekwall K, et al. (2010) Schizosaccharomyces pombe genome-wide nucleosome mapping reveals positioning mechanisms distinct from those of Saccharomyces cerevisiae. Nat Struct Mol Biol 17: 251-257.
33. Wapinski I, Pfeffer A, Friedman N, Regev A (2007) Natural history and evolutionary principles of gene duplication in fungi. Nature 449: 54-61.
34. Shivaswamy S, Bhinge A, Zhao Y, Jones S, Hirst M, et al. (2008) Dynamic remodeling of individual nucleosomes across a eukaryotic genome in response to transcriptional perturbation. PLoS Biol 6: e65. doi:10.1371/journal. pbio.0060065.
35. Segal E, Widom J (2009) What controls nucleosome positions? Trends Genet 25: 335-343.
36. Kornberg RD, Stryer L (1988) Statistical distributions of nucleosomes: nonrandom locations by a stochastic mechanism. Nucleic Acids Res 16: 6677-6690.
37. Mavrich TN, Ioshikhes IP, Venters BJ, Jiang C, Tomsho LP, et al. (2008) A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res 18: 1073-1083.
38. Heus JJ, Zonneveld BJ, Bloom KS, de Steensma HY, van den Berg JA (1993) The nucleosome repeat length of Kluyveromyces lactis is 16 bp longer than that of Saccharomyces cerevisiae. Nucleic Acids Res 21: 2247-2248.
39. Van Holde KE (1989) Chromatin. New York: Springer-Verlag. xii, 497 p.
40. Sasaki S, Mello CC, Shimada A, Nakatani Y, Hashimoto S, et al. (2009) Chromatin-associated periodicity in genetic variation downstream of transcriptional start sites. Science 323: 401-404.
41. Warnecke T, Batada NN, Hurst LD (2008) The impact of the nucleosome code on protein-coding sequence evolution in yeast. PLoS Genet 4: e1000250. doi:10.1371/journal.pgen.1000250.
42. Washietl S, Machne R, Goldman N (2008) Evolutionary footprints of nucleosome positions in yeast. Trends Genet 24: 583-587.
43. Routh A, Sandin S, Rhodes D (2008) Nucleosome repeat length and linker histone stoichiometry determine chromatin fiber structure. Proc Natl Acad Sci U S A 105: 8872-8877.
44. Tirosh I, Berman J, Barkai N (2007) The pattern and evolution of yeast promoter bendability. Trends Genet 23: 318-321.
45. Albert I, Mavrich TN, Tomsho LP, Qi J, Zanton SJ, et al. (2007) Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature 446: 572-576.
46. Choi JK, Kim YJ (2009) Intrinsic variability of gene expression encoded in nucleosome positioning sequences. Nat Genet 41: 498-503.
47. Field Y, Kaplan N, Fondufe-Mittendorf Y, Moore IK, Sharon E, et al. (2008) Distinct modes of regulation by chromatin encoded through nucleosome positioning signals. PLoS Comput Biol 4: e1000216. doi:10.1371/journal. pcbi.1000216.
48. Tirosh I, Barkai N (2008) Two strategies for gene regulation by promoter nucleosomes. Genome Res 18: 1084-1091.
49. Xu Z, Wei W, Gagneur J, Perocchi F, Clauder-Munster S, et al. (2009) Bidirectional promoters generate pervasive transcription in yeast. Nature 457: 1033-1037.
50. MacKay VL, Li X, Flory MR, Turcott E, Law GL, et al. (2004) Gene expression analyzed by high-resolution state array analysis and quantitative proteomics: response of yeast to mating pheromone. Mol Cell Proteomics 3: 478-489.
51. Kurtzman CP, Fell JW (2000) The yeasts: a taxonomic study. Amsterdam; New York: Elsevier. xviii, 1055 p.
52. Marck C, Kachouri-Lafond R, Lafontaine I, Westhof E, Dujon B, et al. (2006) The RNA polymerase III-dependent family of genes in hemiascomycetes: comparative RNomics, decoding strategies, transcription and evolutionary implications. Nucleic Acids Res 34: 1816-1835.
53. Iyer V, Struhl K (1995) Poly(dA:dT), a ubiquitous promoter element that stimulates transcription via its intrinsic DNA structure. Embo J 14: 2570-2579.
54. Kunkel GR, Martinson HG (1981) Nucleosomes will not form on double stranded RNa or over poly(dA).poly(dT) tracts in recombinant DNA. Nucleic Acids Res 9: 6869-6888.
55. Hartley PD, Madhani HD (2009) Mechanisms that specify promoter nucleosome location and identity. Cell 137: 445-458.
56. Yarragudi A, Parfrey LW, Morse RH (2007) Genome-wide analysis of transcriptional dependence and probable target sites for Abf1 and Rap1 in Saccharomyces cerevisiae. Nucleic Acids Res 35: 193-202.
57. Badis G, Chan ET, van Bakel H, Pena-Castillo L, Tillo D, et al. (2008) A library of yeast transcription factor motifs reveals a widespread function for Rsc3 in targeting nucleosome exclusion at promoters. Mol Cell 32: 878-887.
58. Zhu C, Byers KJ, McCord RP, Shi Z, Berger MF, et al. (2009) High-resolution DNA-binding specificity analysis of yeast transcription factors. Genome Res 19: 556-566.
59. Harbison CT, Gordon DB, Lee TI, Rinaldi NJ, Macisaac KD, et al. (2004) Transcriptional regulatory code of a eukaryotic genome. Nature 431: 99-104.
60. Hogues H, Lavoie H, Sellam A, Mangos M, Roemer T, et al. (2008) Transcription factor substitution during the evolution of fungal ribosome regulation. Mol Cell 29: 552-562.
61. Tanay A, Regev A, Shamir R (2005) Conservation and evolvability in regulatory networks: the evolution of ribosomal regulation in yeast. Proc Natl Acad Sci U S A 102: 7203-7208.
62. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, et al. (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: 4241-4257.
63. Lam FH, Steger DJ, O'Shea EK (2008) Chromatin decouples promoter threshold from dynamic range. Nature 453: 246-250.
64. Lomvardas S, Thanos D (2002) Modifying gene expression programs by altering core promoter chromatin architecture. Cell 110: 261-271.
65. MacIsaac KD, Wang T, Gordon DB, Gifford DK, Stormo GD, et al. (2006) An improved map of conserved regulatory sites for Saccharomyces cerevisiae. BMC Bioinformatics 7: 113.
66. Muller H, Hennequin C, Gallaud J, Dujon B, Fairhead C (2008) The asexual yeast Candida glabrata maintains distinct a and alpha haploid mating types. Eukaryot Cell 7: 848-858.
67. Williams RM, Primig M, Washburn BK, Winzeler EA, Bellis M, et al. (2002) The Ume6 regulon coordinates metabolic and meiotic gene expression in yeast. Proc Natl Acad Sci U S A 99: 13431-13436.
68. Wapinski I, Pfiffner J, French C, Socha A, Thompson DA, et al. (2010) Gene duplication and the evolution of ribosomal protein gene regulation in yeast. Proc Natl Acad Sci U S A 107: 5505-5510.
69. Tillo D, Hughes TR (2009) G+C content dominates intrinsic nucleosome occupancy. BMC Bioinformatics 10: 442.
70. Kent WJ (2002) BLAT-the BLAST-like alignment tool. Genome Res 12: 656-664.
71. Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, et al. (1999) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 27: 29-34.
72. Harris MA, Clark J, Ireland A, Lomax J, Ashburner M, et al. (2004) The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res 32: D258-D261.
73. Mewes HW, Frishman D, Guldener U, Mannhaupt G, Mayer K, et al. (2002) MIPS: a database for genomes and protein sequences. Nucleic Acids Res 30: 31-34.
74. Karp PD, Ouzounis CA, Moore-Kochlacs C, Goldovsky L, Kaipa P, et al. (2005) Expansion of the BioCyc collection of pathway/genome databases to 160 genomes. Nucleic Acids Res 33: 6083-6089.
75. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc B 57: 289-300.
76. Barash Y, Elidan G, Kaplan T, Friedman N (2005) CIS: compound importance sampling method for protein-DNA binding site p-value estimation. Bioinformatics 21: 596-600.
77. Li Y, Flanagan PM, Tschochner H, Kornberg RD (1994) RNA polymerase II initiation factor interactions and transcription start site selection. Science 263: 805-807.
78. Mavrich TN, Jiang C, Ioshikhes IP, Li X, Venters BJ, et al. (2008) Nucleosome organization in the Drosophila genome. Nature 453: 358-362.
79. Schones DE, Cui K, Cuddapah S, Roh TY, Barski A, et al. (2008) Dynamic regulation of nucleosome positioning in the human genome. Cell 132: 887-898.
80. Fuda NJ, Ardehali MB, Lis JT (2009) Defining mechanisms that regulate RNA polymerase II transcription in vivo. Nature 461: 186-192.
81. Byrne KP, Wolfe KH (2006) Visualizing synthetic relationships among the hemiascomycetes with the Yeast Gene Order Browser. Nucleic Acids Res 34: D452-D455.