Nucleosomes Shape DNA Polymorphism and Divergence

Langley, Sasha A.; Karpen, Gary H.; Langley, Charles H.

doi:10.1371/journal.pgen.1004457

Title: Nucleosomes Shape DNA Polymorphism and Divergence

Journal Article · Thu Jul 03 00:00:00 EDT 2014 · PLoS Genetics

DOI:https://doi.org/10.1371/journal.pgen.1004457· OSTI ID:1627306

Langley, Sasha A. ^[1]; Karpen, Gary H. ^[2]; Langley, Charles H. ^[3]

Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); University of California, Berkeley, CA (United States)
University of California, Davis, CA (United States)

An estimated 80% of genomic DNA in eukaryotes is packaged as nucleosomes, which, together with the remaining interstitial linker regions, generate higher order chromatin structures. Nucleosome sequences isolated from diverse organisms exhibit ,10 bp periodic variations in AA, TT and GC dinucleotide frequencies. These sequence elements generate intrinsically curved DNA and help establish the histone-DNA interface. We investigated an important unanswered question concerning the interplay between chromatin organization and genome evolution: do the DNA sequence preferences inherent to the highly conserved histone core exert detectable natural selection on genomic divergence and polymorphism? To address this hypothesis, we isolated nucleosomal DNA sequences from Drosophila melanogaster embryos and examined the underlying genomic variation within and between species. We found that divergence along the D. melanogaster lineage is periodic across nucleosome regions with base changes following preferred nucleotides, providing new evidence for systematic evolutionary forces in the generation and maintenance of nucleosome-associated dinucleotide periodicities. Further, Single Nucleotide Polymorphism (SNP) frequency spectra show striking periodicities across nucleosomal regions, paralleling divergence patterns. Preferred alleles occur at higher frequencies in natural populations, consistent with a central role for natural selection. These patterns are stronger for nucleosomes in introns than in intergenic regions, suggesting selection is stronger in transcribed regions where nucleosomes undergo more displacement, remodeling and functional modification. In addition, we observe a large-scale (~180 bp) periodic enrichment of AA/TT dinucleotides associated with nucleosome occupancy, while GC dinucleotide frequency peaks in linker regions. Divergence and polymorphism data also support a role for natural selection in the generation and maintenance of these super-nucleosomal patterns. Our results demonstrate that nucleosome-associated sequence periodicities are under selective pressure, implying that structural interactions between nucleosomes and DNA sequence shape sequence evolution, particularly in introns.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)

Grant/Contract Number:: AC02-05CH11231; HG02942; GM066272

OSTI ID:: 1627306

Journal Information:: PLoS Genetics, Vol. 10, Issue 7; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (93)

Solvent Mediated Interactions in the Structure of the Nucleosome Core Particle at 1.9Å Resolution Davey, Curt A.; Sargent, David F.; Luger, Karolin Journal of Molecular Biology, Vol. 319, Issue 5 https://doi.org/10.1016/S0022-2836(02)00386-8	journal	June 2002
The Distribution of Gene Frequencies Under Irreversible Mutation Wright, S. Proceedings of the National Academy of Sciences, Vol. 24, Issue 7 https://doi.org/10.1073/pnas.24.7.253	journal	July 1938
The Effects of Deleterious Mutations on Evolution at Linked Sites Charlesworth, Brian Genetics, Vol. 190, Issue 1 https://doi.org/10.1534/genetics.111.134288	journal	January 2012
Nucleosomes Suppress Spontaneous Mutations Base-Specifically in Eukaryotes Chen, Xiaoshu; Chen, Zhidong; Chen, Han Science, Vol. 335, Issue 6073 https://doi.org/10.1126/science.1217580	journal	March 2012
A genomic code for nucleosome positioning Segal, Eran; Fondufe-Mittendorf, Yvonne; Chen, Lingyi Nature, Vol. 442, Issue 7104 https://doi.org/10.1038/nature04979	journal	July 2006
Rotational dynamics of DNA on the nucleosome surface markedly impact accessibility to a DNA repair enzyme Hinz, J. M.; Rodriguez, Y.; Smerdon, M. J. Proceedings of the National Academy of Sciences, Vol. 107, Issue 10 https://doi.org/10.1073/pnas.0914443107	journal	February 2010
Functional Conservation of Nucleosome Formation Selectively Biases Presumably Neutral Molecular Variation in Yeast Genomes Babbitt, Gregory A.; Cotter, C. R. Genome Biology and Evolution, Vol. 3 https://doi.org/10.1093/gbe/evq081	journal	December 2010
Intraspecific nuclear DNA variation in Drosophila Moriyama, E. N.; Powell, J. R. Molecular Biology and Evolution, Vol. 13, Issue 1 https://doi.org/10.1093/oxfordjournals.molbev.a025563	journal	January 1996
Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors Wang, J.; Zhuang, J.; Iyer, S. Genome Research, Vol. 22, Issue 9 https://doi.org/10.1101/gr.139105.112	journal	September 2012
A Packing Mechanism for Nucleosome Organization Reconstituted Across a Eukaryotic Genome Zhang, Z.; Wippo, C. J.; Wal, M. Science, Vol. 332, Issue 6032 https://doi.org/10.1126/science.1200508	journal	May 2011
GC-Biased Segregation of Noncoding Polymorphisms in Drosophila Galtier, Nicolas; Bazin, Eric; Bierne, Nicolas Genetics, Vol. 172, Issue 1 https://doi.org/10.1534/genetics.105.046524	journal	September 2005
Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo Zhang, Yong; Moqtaderi, Zarmik; Rattner, Barbara P. Nature Structural & Molecular Biology, Vol. 16, Issue 8 https://doi.org/10.1038/nsmb.1636	journal	July 2009
DNA methylation in Drosophila melanogaster Lyko, Frank; Ramsahoye, Bernard H.; Jaenisch, Rudolf Nature, Vol. 408, Issue 6812 https://doi.org/10.1038/35046205	journal	November 2000
Dual role of DNA intrinsic curvature and flexibility in determining nucleosome stability 1 1Edited by T. Richmond Anselmi, C.; Bocchinfuso, G.; De Santis, P. Journal of Molecular Biology, Vol. 286, Issue 5 https://doi.org/10.1006/jmbi.1998.2575	journal	March 1999
The mechanics behind DNA sequence-dependent properties of the nucleosome Chua, Eugene Y. D.; Vasudevan, Dileep; Davey, Gabriela E. Nucleic Acids Research, Vol. 40, Issue 13 https://doi.org/10.1093/nar/gks261	journal	March 2012
Mechanisms of ATP-dependent nucleosome sliding Bowman, Gregory D. Current Opinion in Structural Biology, Vol. 20, Issue 1 https://doi.org/10.1016/j.sbi.2009.12.002	journal	February 2010
Widespread signatures of recent selection linked to nucleosome positioning in the human lineage Prendergast, J. G. D.; Semple, C. A. M. Genome Research, Vol. 21, Issue 11 https://doi.org/10.1101/gr.122275.111	journal	September 2011
Sequence periodicities in chicken nucleosome core DNA Satchwell, Sandra C.; Drew, Horace R.; Travers, Andrew A. Journal of Molecular Biology, Vol. 191, Issue 4 https://doi.org/10.1016/0022-2836(86)90452-3	journal	October 1986
G+C content dominates intrinsic nucleosome occupancy Tillo, Desiree; Hughes, Timothy R. BMC Bioinformatics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2105-10-442	journal	December 2009
The sampling theory of selectively neutral alleles Watterson, G. A. Advances in Applied Probability, Vol. 6, Issue 3 https://doi.org/10.2307/1426228	journal	September 1974
Nucleosome positioning: How is it established, and why does it matter? Radman-Livaja, Marta; Rando, Oliver J. Developmental Biology, Vol. 339, Issue 2 https://doi.org/10.1016/j.ydbio.2009.06.012	journal	March 2010
Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome Albert, Istvan; Mavrich, Travis N.; Tomsho, Lynn P. Nature, Vol. 446, Issue 7135 https://doi.org/10.1038/nature05632	journal	March 2007
The Impact of the Nucleosome Code on Protein-Coding Sequence Evolution in Yeast Warnecke, Tobias; Batada, Nizar N.; Hurst, Laurence D. PLoS Genetics, Vol. 4, Issue 11 https://doi.org/10.1371/journal.pgen.1000250	journal	November 2008
Analysis of the genome sequences of three Drosophila melanogaster spontaneous mutation accumulation lines Keightley, P. D.; Trivedi, U.; Thomson, M. Genome Research, Vol. 19, Issue 7 https://doi.org/10.1101/gr.091231.109	journal	May 2009
Nucleosome Remodeling by hMSH2-hMSH6 Javaid, Sarah; Manohar, Mridula; Punja, Nidhi Molecular Cell, Vol. 36, Issue 6 https://doi.org/10.1016/j.molcel.2009.12.010	journal	December 2009
Nucleosome organization in the Drosophila genome Mavrich, Travis N.; Jiang, Cizhong; Ioshikhes, Ilya P. Nature, Vol. 453, Issue 7193 https://doi.org/10.1038/nature06929	journal	April 2008
Population Genomic Analysis of Base Composition Evolution in Drosophila melanogaster Poh, Yu-Ping; Ting, Chau-Ti; Fu, Hua-Wen Genome Biology and Evolution, Vol. 4, Issue 12 https://doi.org/10.1093/gbe/evs097	journal	November 2012
The sampling theory of selectively neutral alleles Ewens, W. J. Theoretical Population Biology, Vol. 3, Issue 1 https://doi.org/10.1016/0040-5809(72)90035-4	journal	March 1972
Evolutionary footprints of nucleosome positions in yeast Washietl, Stefan; Machné, Rainer; Goldman, Nick Trends in Genetics, Vol. 24, Issue 12 https://doi.org/10.1016/j.tig.2008.09.003	journal	December 2008
Population Genomics of Sub-Saharan Drosophila melanogaster: African Diversity and Non-African Admixture Pool, John E.; Corbett-Detig, Russell B.; Sugino, Ryuichi P. PLoS Genetics, Vol. 8, Issue 12 https://doi.org/10.1371/journal.pgen.1003080	journal	December 2012
Nucleosome positioning signals in genomic DNA Peckham, H. E.; Thurman, R. E.; Fu, Y. Genome Research, Vol. 17, Issue 8 https://doi.org/10.1101/gr.6101007	journal	July 2007
Genomic Variation in Natural Populations of Drosophila melanogaster Langley, Charles H.; Stevens, Kristian; Cardeno, Charis Genetics, Vol. 192, Issue 2 https://doi.org/10.1534/genetics.112.142018	journal	June 2012
Impact of chromatin structure on sequence variability in the human genome Tolstorukov, Michael Y.; Volfovsky, Natalia; Stephens, Robert M. Nature Structural & Molecular Biology, Vol. 18, Issue 4 https://doi.org/10.1038/nsmb.2012	journal	March 2011
Interplay between mismatch repair and chromatin assembly Schopf, B.; Bregenhorn, S.; Quivy, J. -P. Proceedings of the National Academy of Sciences, Vol. 109, Issue 6 https://doi.org/10.1073/pnas.1106696109	journal	January 2012
Micrococcal Nuclease Does Not Substantially Bias Nucleosome Mapping Allan, James; Fraser, Ross M.; Owen-Hughes, Tom Journal of Molecular Biology, Vol. 417, Issue 3 https://doi.org/10.1016/j.jmb.2012.01.043	journal	March 2012
Transcriptional activation of yeast genes disrupts intragenic nucleosome phasing Cui, Feng; Cole, Hope A.; Clark, David J. Nucleic Acids Research, Vol. 40, Issue 21 https://doi.org/10.1093/nar/gks870	journal	September 2012
The Structural Location of DNA Lesions in Nucleosome Core Particles Determines Accessibility by Base Excision Repair Enzymes Rodriguez, Yesenia; Smerdon, Michael J. Journal of Biological Chemistry, Vol. 288, Issue 19 https://doi.org/10.1074/jbc.M112.441444	journal	March 2013
The role of DNA shape in protein–DNA recognition Rohs, Remo; West, Sean M.; Sosinsky, Alona Nature, Vol. 461, Issue 7268 https://doi.org/10.1038/nature08473	journal	October 2009
Transcription Factors Bind Thousands of Active and Inactive Regions in the Drosophila Blastoderm Li, Xiao-yong; MacArthur, Stewart; Bourgon, Richard PLoS Biology, Vol. 6, Issue 2 https://doi.org/10.1371/journal.pbio.0060027	journal	February 2008
Interplay between mismatch repair and chromatin assembly B., Schöpf,; S., Bregenhorn,; P., Quivy, J. National Academy of Sciences https://doi.org/10.5167/uzh-55570	text	January 2012
New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning Lowary, P. T.; Widom, J. Journal of Molecular Biology, Vol. 276, Issue 1 https://doi.org/10.1006/jmbi.1997.1494	journal	February 1998
The DNA-encoded nucleosome organization of a eukaryotic genome Kaplan, Noam; Moore, Irene K.; Fondufe-Mittendorf, Yvonne Nature, Vol. 458, Issue 7236 https://doi.org/10.1038/nature07667	journal	December 2008
Intrinsic Histone-DNA Interactions and Low Nucleosome Density Are Important for Preferential Accessibility of Promoter Regions in Yeast Sekinger, Edward A.; Moqtaderi, Zarmik; Struhl, Kevin Molecular Cell, Vol. 18, Issue 6 https://doi.org/10.1016/j.molcel.2005.05.003	journal	June 2005
Nucleosome positions predicted through comparative genomics Ioshikhes, Ilya P.; Albert, Istvan; Zanton, Sara J. Nature Genetics, Vol. 38, Issue 10 https://doi.org/10.1038/ng1878	journal	September 2006
Correlation between the abundance of yeast transfer RNAs and the occurrence of the respective codons in protein genes Ikemura, Toshimichi Journal of Molecular Biology, Vol. 158, Issue 4 https://doi.org/10.1016/0022-2836(82)90250-9	journal	July 1982
Bayesian Markov chain Monte Carlo sequence analysis reveals varying neutral substitution patterns in mammalian evolution Hwang, D. G.; Green, P. Proceedings of the National Academy of Sciences, Vol. 101, Issue 39 https://doi.org/10.1073/pnas.0404142101	journal	August 2004
Context Dependence, Ancestral Misidentification, and Spurious Signatures of Natural Selection Hernandez, R. D.; Williamson, S. H.; Bustamante, C. D. Molecular Biology and Evolution, Vol. 24, Issue 8 https://doi.org/10.1093/molbev/msm108	journal	April 2007
Enzymatic Excision of Uracil Residues in Nucleosomes Depends on the Local DNA Structure and Dynamics Ye, Yu; Stahley, Mary R.; Xu, Jianqing Biochemistry, Vol. 51, Issue 30 https://doi.org/10.1021/bi3006412	journal	July 2012
Nucleosome positioning as a determinant of exon recognition Tilgner, Hagen; Nikolaou, Christoforos; Althammer, Sonja Nature Structural & Molecular Biology, Vol. 16, Issue 9 https://doi.org/10.1038/nsmb.1658	journal	August 2009
Artificial nucleosome positioning sequences. Shrader, T. E.; Crothers, D. M. Proceedings of the National Academy of Sciences, Vol. 86, Issue 19 https://doi.org/10.1073/pnas.86.19.7418	journal	October 1989
Nucleosome positioning and gene regulation: advances through genomics Jiang, Cizhong; Pugh, B. Franklin Nature Reviews Genetics, Vol. 10, Issue 3 https://doi.org/10.1038/nrg2522	journal	March 2009
Nucleosome sequence preferences influence in vivo nucleosome organization Kaplan, Noam; Moore, Irene; Fondufe-Mittendorf, Yvonne Nature Structural & Molecular Biology, Vol. 17, Issue 8 https://doi.org/10.1038/nsmb0810-918	journal	August 2010
Evidence that nucleosomes inhibit mismatch repair in eukaryotic cells Li, Feng; Tian, Lei; Gu, Liya The FASEB Journal, Vol. 24, Issue S1 https://doi.org/10.1096/fasebj.24.1_supplement.876.7	journal	April 2010
Plasticity in patterns of histone modifications and chromosomal proteins in Drosophila heterochromatin Riddle, N. C.; Minoda, A.; Kharchenko, P. V. Genome Research, Vol. 21, Issue 2 https://doi.org/10.1101/gr.110098.110	journal	December 2010
Distinct Modes of Regulation by Chromatin Encoded through Nucleosome Positioning Signals Field, Yair; Kaplan, Noam; Fondufe-Mittendorf, Yvonne PLoS Computational Biology, Vol. 4, Issue 11 https://doi.org/10.1371/journal.pcbi.1000216	journal	November 2008
Chromatin-Associated Periodicity in Genetic Variation Downstream of Transcriptional Start Sites Sasaki, S.; Mello, C. C.; Shimada, A. Science, Vol. 323, Issue 5912 https://doi.org/10.1126/science.1163183	journal	January 2009
Controls of Nucleosome Positioning in the Human Genome Gaffney, Daniel J.; McVicker, Graham; Pai, Athma A. PLoS Genetics, Vol. 8, Issue 11 https://doi.org/10.1371/journal.pgen.1003036	journal	November 2012
Purifying Selection Maintains Highly Conserved Noncoding Sequences in Drosophila Casillas, S.; Barbadilla, A.; Bergman, C. M. Molecular Biology and Evolution, Vol. 24, Issue 10 https://doi.org/10.1093/molbev/msm150	journal	July 2007
Divergent human remodeling complexes remove nucleosomes from strong positioning sequences Pham, Chuong D.; He, Xi; Schnitzler, Gavin R. Nucleic Acids Research, Vol. 38, Issue 2 https://doi.org/10.1093/nar/gkp1030	journal	November 2009
Sequence motifs and free energies of selected natural and non-natural nucleosome positioning DNA sequences Thåström, A.; Lowary, P. T.; Widlund, H. R. Journal of Molecular Biology, Vol. 288, Issue 2 https://doi.org/10.1006/jmbi.1999.2686	journal	April 1999
DNA bending and its relation to nucleosome positioning Drew, Horace R.; Travers, Andrew A. Journal of Molecular Biology, Vol. 186, Issue 4 https://doi.org/10.1016/0022-2836(85)90396-1	journal	December 1985
Inferring Natural Selection on Fine-Scale Chromatin Organization in Yeast Babbitt, G. A.; Kim, Y. Molecular Biology and Evolution, Vol. 25, Issue 8 https://doi.org/10.1093/molbev/msn127	journal	April 2008
Integrating Genomics, Bioinformatics, and Classical Genetics to Study the Effects of Recombination on Genome Evolution Birdsell, John A. Molecular Biology and Evolution, Vol. 19, Issue 7 https://doi.org/10.1093/oxfordjournals.molbev.a004176	journal	July 2002
Evolution of a large population under gene conversion. Nagylaki, T. Proceedings of the National Academy of Sciences, Vol. 80, Issue 19 https://doi.org/10.1073/pnas.80.19.5941	journal	October 1983
The DNA-encoded nucleosome organization of a eukaryotic genome Yair, Field,; D., Lieb, Jason; J., Gossett, Andrea The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/cste-0t39	text	January 2009
Finishing a whole-genome shotgun: Release 3 of the Drosophila melanogastereuchromatic genome sequence Celniker, Susan E.; Wheeler, David A.; Kronmiller, Brent Genome Biology, Vol. 3, Issue 12, p. research0079.1 https://doi.org/10.1186/gb-2002-3-12-research0079	journal	January 2002
Determinants of nucleosome organization in primary human cells Valouev, Anton; Johnson, Steven M.; Boyd, Scott D. Nature, Vol. 474, Issue 7352 https://doi.org/10.1038/nature10002	journal	May 2011
Precise Maps of RNA Polymerase Reveal How Promoters Direct Initiation and Pausing Kwak, H.; Fuda, N. J.; Core, L. J. Science, Vol. 339, Issue 6122 https://doi.org/10.1126/science.1229386	journal	February 2013
Ubiquitous selective constraints in the Drosophila genome revealed by a genome-wide interspecies comparison Halligan, D. L. Genome Research, Vol. 16, Issue 7 https://doi.org/10.1101/gr.5022906	journal	July 2006
Chromatin-Associated Periodicity in Genetic Variation Downstream of Transcriptional Start Sites Sasaki, Shin; Mello, Cecilia C.; Shimada, Atsuko Medaka https://doi.org/10.1007/978-4-431-92691-7_3	book	January 2011
A map of nucleosome positions in yeast at base-pair resolution Brogaard, Kristin; Xi, Liqun; Wang, Ji-Ping Nature, Vol. 486, Issue 7404 https://doi.org/10.1038/nature11142	journal	June 2012
The role of Mediator and Little Elongation Complex in transcription termination Takahashi, Hidehisa; Ranjan, Amol; Chen, Shiyuan Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14849-1	journal	February 2020
A high-resolution atlas of nucleosome occupancy in yeast Lee, William; Tillo, Desiree; Bray, Nicolas Nature Genetics, Vol. 39, Issue 10 https://doi.org/10.1038/ng2117	journal	September 2007
Electrostatic Interactions between Arginines and the Minor Groove in the Nucleosome West, Sean M.; Rohs, Remo; Mann, Richard S. Journal of Biomolecular Structure and Dynamics, Vol. 27, Issue 6 https://doi.org/10.1080/07391102.2010.10508587	journal	June 2010
The Molecular Evolution of Nucleosome Positioning Through Sequence-Dependent Deformation of the DNA Polymer Babbitt, G. A.; Tolstorukov, M. Y.; Kim, Y. Journal of Biomolecular Structure and Dynamics, Vol. 27, Issue 6 https://doi.org/10.1080/07391102.2010.10508584	journal	June 2010
Evolution in Mendelian Populations Wright, Sewall Genetics, Vol. 16, Issue 2 https://doi.org/10.1093/genetics/16.2.97	journal	March 1931
The selection-mutation-drift theory of synonymous codon usage. Bulmer, M. Genetics, Vol. 129, Issue 3 https://doi.org/10.1093/genetics/129.3.897	journal	November 1991
Selection intensity for codon bias. Hartl, D. L.; Moriyama, E. N.; Sawyer, S. A. Genetics, Vol. 138, Issue 1 https://doi.org/10.1093/genetics/138.1.227	journal	September 1994
Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Akashi, H. Genetics, Vol. 136, Issue 3 https://doi.org/10.1093/genetics/136.3.927	journal	March 1994
Molecular Evolution Between Drosophila melanogaster and D. simulans Reduced Codon Bias, Faster Rates of Amino Acid Substitution, and Larger Proteins in D. melanogaster Akashi, Hiroshi Genetics, Vol. 144, Issue 3 https://doi.org/10.1093/genetics/144.3.1297	journal	November 1996
Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Tajima, F. Genetics, Vol. 123, Issue 3 https://doi.org/10.1093/genetics/123.3.585	journal	November 1989
Population genetics of polymorphism and divergence. Sawyer, S. A.; Hartl, D. L. Genetics, Vol. 132, Issue 4 https://doi.org/10.1093/genetics/132.4.1161	journal	December 1992
When Did the Human Population Size Start Increasing? Wall, Jeffrey D.; Przeworski, Molly Genetics, Vol. 155, Issue 4 https://doi.org/10.1093/genetics/155.4.1865	journal	August 2000
The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Braverman, J. M.; Hudson, R. R.; Kaplan, N. L. Genetics, Vol. 140, Issue 2 https://doi.org/10.1093/genetics/140.2.783	journal	June 1995
Molecular Population Genetics of Xdh and the Evolution of Base Composition in Drosophila Begun, David J.; Whitley, Penn Genetics, Vol. 162, Issue 4 https://doi.org/10.1093/genetics/162.4.1725	journal	December 2002
Evolution of synonymous codon usage in metazoans Duret, L. Current Opinion in Genetics & Development, Vol. 12, Issue 6 https://doi.org/10.1016/s0959-437x(02)00353-2	journal	December 2002
A population genetic model for the evolution of synonymous codon usage: patterns and predictions McVEAN, Gilean A. T.; Charlesworth, Brian Genetical Research, Vol. 74, Issue 2 https://doi.org/10.1017/s0016672399003912	journal	October 1999
Role of DNA sequence in nucleosome stability and dynamics Widom, J. Quarterly Reviews of Biophysics, Vol. 34, Issue 3 https://doi.org/10.1017/s0033583501003699	journal	August 2001
Evidence That Nucleosomes Inhibit Mismatch Repair in Eukaryotic Cells Li, Feng; Tian, Lei; Gu, Liya Journal of Biological Chemistry, Vol. 284, Issue 48 https://doi.org/10.1074/jbc.m109.049874	journal	November 2009
Activity of FEN1 Endonuclease on Nucleosome Substrates Is Dependent upon DNA Sequence but Not Flap Orientation Jagannathan, Indu; Pepenella, Sharon; Hayes, Jeffrey J. Journal of Biological Chemistry, Vol. 286, Issue 20 https://doi.org/10.1074/jbc.m111.229658	journal	May 2011
Chromatin Remodeling Activities Act on UV-damaged Nucleosomes and Modulate DNA Damage Accessibility to Photolyase Gaillard, Hélène; Fitzgerald, Daniel J.; Smith, Corey L. Journal of Biological Chemistry, Vol. 278, Issue 20 https://doi.org/10.1074/jbc.m300770200	journal	May 2003
Remodelers Organize Cellular Chromatin by Counteracting Intrinsic Histone-DNA Sequence Preferences in a Class-Specific Manner Moshkin, Y. M.; Chalkley, G. E.; Kan, T. W. Molecular and Cellular Biology, Vol. 32, Issue 3 https://doi.org/10.1128/mcb.06365-11	journal	November 2011
Accessibility of a glucocorticoid response element in a nucleosome depends on its rotational positioning. Li, Q.; Wrange, O. Molecular and Cellular Biology, Vol. 15, Issue 8 https://doi.org/10.1128/mcb.15.8.4375	journal	August 1995

Cited By (13)

Evidence of selection for an accessible nucleosomal array in human Drillon, Guénola; Audit, Benjamin; Argoul, Françoise BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-2880-2	journal	July 2016
Purifying Selection, Drift, and Reversible Mutation with Arbitrarily High Mutation Rates Charlesworth, Brian; Jain, Kavita Genetics, Vol. 198, Issue 4 https://doi.org/10.1534/genetics.114.167973	journal	September 2014
Extremely low nucleotide diversity in the X-linked region of papaya caused by a strong selective sweep VanBuren, Robert; Wai, Ching Man; Zhang, Jisen Genome Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s13059-016-1095-9	journal	November 2016
Human exonization through differential nucleosome occupancy Li, Yumei; Li, Chen; Li, Shuxian Proceedings of the National Academy of Sciences, Vol. 115, Issue 35 https://doi.org/10.1073/pnas.1802561115	journal	August 2018
TRX-LOGOS - a graphical tool to demonstrate DNA information content dependent upon backbone dynamics in addition to base sequence Fortin, Connor H.; Schulze, Katharina V.; Babbitt, Gregory A. Source Code for Biology and Medicine, Vol. 10, Issue 1 https://doi.org/10.1186/s13029-015-0040-8	journal	September 2015
Patterns of Genetic Variability in Genomic Regions with Low Rates of Recombination Becher, Hannes; Jackson, Benjamin C.; Charlesworth, Brian Current Biology, Vol. 30, Issue 1 https://doi.org/10.1016/j.cub.2019.10.047	journal	January 2020
Patterns of genetic variability in genomic regions with low rates of recombination Becher, Hannes; Jackson, Benjamin C.; Charlesworth, Brian Current Biology https://doi.org/10.1101/739888	posted_content	August 2019
Associations between nucleosome phasing, sequence asymmetry, and tissue-specific expression in a set of inbred Medaka species Nakatani, Yoichiro; Mello, Cecilia C.; Hashimoto, Shin-ichi BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-2198-5	journal	November 2015
New insights into structural features and optimal detection of circulating tumor DNA determined by single-strand DNA analysis Sanchez, Cynthia; Snyder, Matthew W.; Tanos, Rita npj Genomic Medicine, Vol. 3, Issue 1 https://doi.org/10.1038/s41525-018-0069-0	journal	November 2018
Rates and Patterns of Mutation in Tandem Repetitive DNA in Six Independent Lineages of Chlamydomonas reinhardtii Flynn, Jullien M.; Lower, Sarah E.; Barbash, Daniel A. Genome Biology and Evolution, Vol. 10, Issue 7 https://doi.org/10.1093/gbe/evy123	journal	June 2018
Chromatin structure is distinct between coding and non-coding single nucleotide polymorphisms Liu, Hongde; Zhai, Jinchen; Luo, Kun BMC Molecular Biology, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2199-15-22	journal	January 2014
Increasing Nucleosome Occupancy Is Correlated with an Increasing Mutation Rate so Long as DNA Repair Machinery Is Intact Yazdi, Puya G.; Pedersen, Brian A.; Taylor, Jared F. PLOS ONE, Vol. 10, Issue 8 https://doi.org/10.1371/journal.pone.0136574	journal	August 2015
Effects of DNA Methylation and Chromatin State on Rates of Molecular Evolution in Insects Glastad, Karl M.; Goodisman, Michael A. D.; Yi, Soojin V. G3 Genes\|Genomes\|Genetics, Vol. 6, Issue 2 https://doi.org/10.1534/g3.115.023499	journal	February 2016

Similar Records

DNA as a language

Conference · Fri Dec 31 00:00:00 EST 1993 · OSTI ID:1627306

Trifonov, E N

Identification of functional elements and regulatory circuits by Drosophila modENCODE

Journal Article · Wed Dec 22 00:00:00 EST 2010 · Science · OSTI ID:1627306

Roy, Sushmita; Ernst, Jason; Kharchenko, Peter V; +93 more

Local chromatin structure of heterochromatin regulates repeated DNA stability, nucleolus structure, and genome integrity

Thesis/Dissertation · Mon Jan 01 00:00:00 EST 2007 · OSTI ID:1627306

Peng, Jamy C.

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
nucleosomes
invertebrate genomics
drosophila melanogaster
natural selection
histones
single nucleotide polymorphisms
genomics
nucleosome mapping

Title: Nucleosomes Shape DNA Polymorphism and Divergence

Citation Formats

References (93)

Cited By (13)

Similar Records

Related Subjects