The impact of the nucleosome code on protein-coding sequence evolution in yeast.
Coding sequence evolution was once thought to be the result of selection on optimal protein function alone. Selection can, however, also act at the RNA level, for example, to facilitate rapid translation or ensure correct splicing. Here, we ask whether the way DNA works also imposes constraints on c...
| Main Authors: | , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2008-11-01
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| Series: | PLoS Genetics |
| Online Access: | http://europepmc.org/articles/PMC2570795?pdf=render |
| _version_ | 1818330591996674048 |
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| author | Tobias Warnecke Nizar N Batada Laurence D Hurst |
| author_facet | Tobias Warnecke Nizar N Batada Laurence D Hurst |
| author_sort | Tobias Warnecke |
| collection | DOAJ |
| description | Coding sequence evolution was once thought to be the result of selection on optimal protein function alone. Selection can, however, also act at the RNA level, for example, to facilitate rapid translation or ensure correct splicing. Here, we ask whether the way DNA works also imposes constraints on coding sequence evolution. We identify nucleosome positioning as a likely candidate to set up such a DNA-level selective regime and use high-resolution microarray data in yeast to compare the evolution of coding sequence bound to or free from nucleosomes. Controlling for gene expression and intra-gene location, we find a nucleosome-free "linker" sequence to evolve on average 5-6% slower at synonymous sites. A reduced rate of evolution in linker is especially evident at the 5' end of genes, where the effect extends to non-synonymous substitution rates. This is consistent with regular nucleosome architecture in this region being important in the context of gene expression control. As predicted, codons likely to generate a sequence unfavourable to nucleosome formation are enriched in linker sequence. Amino acid content is likewise skewed as a function of nucleosome occupancy. We conclude that selection operating on DNA to maintain correct positioning of nucleosomes impacts codon choice, amino acid choice, and synonymous and non-synonymous rates of evolution in coding sequence. The results support the exclusion model for nucleosome positioning and provide an alternative interpretation for runs of rare codons. As the intimate association of histones and DNA is a universal characteristic of genic sequence in eukaryotes, selection on coding sequence composition imposed by nucleosome positioning should be phylogenetically widespread. |
| first_indexed | 2024-12-13T13:06:24Z |
| format | Article |
| id | doaj.art-63d256413cbc407a8b2f4d59f9c53f61 |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-12-13T13:06:24Z |
| publishDate | 2008-11-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-63d256413cbc407a8b2f4d59f9c53f612022-12-21T23:44:48ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042008-11-01411e100025010.1371/journal.pgen.1000250The impact of the nucleosome code on protein-coding sequence evolution in yeast.Tobias WarneckeNizar N BatadaLaurence D HurstCoding sequence evolution was once thought to be the result of selection on optimal protein function alone. Selection can, however, also act at the RNA level, for example, to facilitate rapid translation or ensure correct splicing. Here, we ask whether the way DNA works also imposes constraints on coding sequence evolution. We identify nucleosome positioning as a likely candidate to set up such a DNA-level selective regime and use high-resolution microarray data in yeast to compare the evolution of coding sequence bound to or free from nucleosomes. Controlling for gene expression and intra-gene location, we find a nucleosome-free "linker" sequence to evolve on average 5-6% slower at synonymous sites. A reduced rate of evolution in linker is especially evident at the 5' end of genes, where the effect extends to non-synonymous substitution rates. This is consistent with regular nucleosome architecture in this region being important in the context of gene expression control. As predicted, codons likely to generate a sequence unfavourable to nucleosome formation are enriched in linker sequence. Amino acid content is likewise skewed as a function of nucleosome occupancy. We conclude that selection operating on DNA to maintain correct positioning of nucleosomes impacts codon choice, amino acid choice, and synonymous and non-synonymous rates of evolution in coding sequence. The results support the exclusion model for nucleosome positioning and provide an alternative interpretation for runs of rare codons. As the intimate association of histones and DNA is a universal characteristic of genic sequence in eukaryotes, selection on coding sequence composition imposed by nucleosome positioning should be phylogenetically widespread.http://europepmc.org/articles/PMC2570795?pdf=render |
| spellingShingle | Tobias Warnecke Nizar N Batada Laurence D Hurst The impact of the nucleosome code on protein-coding sequence evolution in yeast. PLoS Genetics |
| title | The impact of the nucleosome code on protein-coding sequence evolution in yeast. |
| title_full | The impact of the nucleosome code on protein-coding sequence evolution in yeast. |
| title_fullStr | The impact of the nucleosome code on protein-coding sequence evolution in yeast. |
| title_full_unstemmed | The impact of the nucleosome code on protein-coding sequence evolution in yeast. |
| title_short | The impact of the nucleosome code on protein-coding sequence evolution in yeast. |
| title_sort | impact of the nucleosome code on protein coding sequence evolution in yeast |
| url | http://europepmc.org/articles/PMC2570795?pdf=render |
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