Nucleosomes Shape DNA Polymorphism and Divergence

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

doi:10.1371/journal.pgen.1004457

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); DOE/OSTI
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)

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

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

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1627306

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

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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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
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
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
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

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