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Conserved Substitution Patterns around Nucleosome Footprints in Eukaryotes and Archaea Derive from Frequent Nucleosome Repositioning through Evolution

Abstract:
Nucleosomes, the basic repeat units of eukaryotic chromatin, have been suggested to influence the evolution of eukaryotic genomes, both by altering the propensity of DNA to mutate and by selection acting to maintain or exclude nucleosomes in particular locations. Contrary to the popular idea that nucleosomes are unique to eukaryotes, histone proteins have also been discovered in some archaeal genomes. Archaeal nucleosomes, however, are quite unlike their eukaryotic counterparts in many respects, including their assembly into tetramers (rather than octamers) from histone proteins that lack N- and C-terminal tails. Here, we show that despite these fundamental differences the association between nucleosome footprints and sequence evolution is strikingly conserved between humans and the model archaeon Haloferax volcanii. In light of this finding we examine whether selection or mutation can explain concordant substitution patterns in the two kingdoms. Unexpectedly, we find that neither the mutation nor the selection model are sufficient to explain the observed association between nucleosomes and sequence divergence. Instead, we demonstrate that nucleosome-associated substitution patterns are more consistent with a third model where sequence divergence results in frequent repositioning of nucleosomes during evolution. Indeed, we show that nucleosome repositioning is both necessary and largely sufficient to explain the association between current nucleosome positions and biased substitution patterns. This finding highlights the importance of considering the direction of causality between genetic and epigenetic change
Publication status:
Published
Peer review status:
Peer reviewed

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Publisher copy:
10.1371/journal.pcbi.1003373

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Institution:
University of Oxford
Role:
Author
ORCID:
0000-0002-4936-5428
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Role:
Author
ORCID:
0000-0002-6832-0233
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Role:
Author
ORCID:
0000-0003-4453-3274
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Role:
Author
ORCID:
0000-0002-4016-8874
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Role:
Author
ORCID:
0000-0002-8817-1124


Publisher:
Public Library of Science
Journal:
PLoS Computational Biology More from this journal
Volume:
9
Issue:
11
Pages:
e1003373-e1003373
Publication date:
2013-11-21
DOI:
EISSN:
1553-7358
ISSN:
1553-734X


Language:
English
Keywords:
Pubs id:
2358504
Local pid:
pubs:2358504
Source identifiers:
W2033981776
Deposit date:
2026-01-14
ARK identifier:
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