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Evidence of association between Nucleosome Occupancy and the Evolution of Transcription Factor Binding Sites in Yeast

BACKGROUND: Divergence of transcription factor binding sites is considered to be an important source of regulatory evolution. The associations between transcription factor binding sites and phenotypic diversity have been investigated in many model organisms. However, the understanding of other facto...

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Autores principales: Swamy, Krishna BS, Chu, Wen-Yi, Wang, Chun-Yi, Tsai, Huai-Kuang, Wang, Daryi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3124427/
https://www.ncbi.nlm.nih.gov/pubmed/21627806
http://dx.doi.org/10.1186/1471-2148-11-150
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author Swamy, Krishna BS
Chu, Wen-Yi
Wang, Chun-Yi
Tsai, Huai-Kuang
Wang, Daryi
author_facet Swamy, Krishna BS
Chu, Wen-Yi
Wang, Chun-Yi
Tsai, Huai-Kuang
Wang, Daryi
author_sort Swamy, Krishna BS
collection PubMed
description BACKGROUND: Divergence of transcription factor binding sites is considered to be an important source of regulatory evolution. The associations between transcription factor binding sites and phenotypic diversity have been investigated in many model organisms. However, the understanding of other factors that contribute to it is still limited. Recent studies have elucidated the effect of chromatin structure on molecular evolution of genomic DNA. Though the profound impact of nucleosome positions on gene regulation has been reported, their influence on transcriptional evolution is still less explored. With the availability of genome-wide nucleosome map in yeast species, it is thus desirable to investigate their impact on transcription factor binding site evolution. Here, we present a comprehensive analysis of the role of nucleosome positioning in the evolution of transcription factor binding sites. RESULTS: We compared the transcription factor binding site frequency in nucleosome occupied regions and nucleosome depleted regions in promoters of old (orthologs among Saccharomycetaceae) and young (Saccharomyces specific) genes; and in duplicate gene pairs. We demonstrated that nucleosome occupied regions accommodate greater binding site variations than nucleosome depleted regions in young genes and in duplicate genes. This finding was confirmed by measuring the difference in evolutionary rates of binding sites in sensu stricto yeasts at nucleosome occupied regions and nucleosome depleted regions. The binding sites at nucleosome occupied regions exhibited a consistently higher evolution rate than those at nucleosome depleted regions, corroborating the difference in the selection constraints at the two regions. Finally, through site-directed mutagenesis experiment, we found that binding site gain or loss events at nucleosome depleted regions may cause more expression differences than those in nucleosome occupied regions. CONCLUSIONS: Our study indicates the existence of different selection constraint on binding sites at nucleosome occupied regions than at the nucleosome depleted regions. We found that the binding sites have a different rate of evolution at nucleosome occupied and depleted regions. Finally, using transcription factor binding site-directed mutagenesis experiment, we confirmed the difference in the impact of binding site changes on expression at these regions. Thus, our work demonstrates the importance of composite analysis of chromatin and transcriptional evolution.
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spelling pubmed-31244272011-06-28 Evidence of association between Nucleosome Occupancy and the Evolution of Transcription Factor Binding Sites in Yeast Swamy, Krishna BS Chu, Wen-Yi Wang, Chun-Yi Tsai, Huai-Kuang Wang, Daryi BMC Evol Biol Research Article BACKGROUND: Divergence of transcription factor binding sites is considered to be an important source of regulatory evolution. The associations between transcription factor binding sites and phenotypic diversity have been investigated in many model organisms. However, the understanding of other factors that contribute to it is still limited. Recent studies have elucidated the effect of chromatin structure on molecular evolution of genomic DNA. Though the profound impact of nucleosome positions on gene regulation has been reported, their influence on transcriptional evolution is still less explored. With the availability of genome-wide nucleosome map in yeast species, it is thus desirable to investigate their impact on transcription factor binding site evolution. Here, we present a comprehensive analysis of the role of nucleosome positioning in the evolution of transcription factor binding sites. RESULTS: We compared the transcription factor binding site frequency in nucleosome occupied regions and nucleosome depleted regions in promoters of old (orthologs among Saccharomycetaceae) and young (Saccharomyces specific) genes; and in duplicate gene pairs. We demonstrated that nucleosome occupied regions accommodate greater binding site variations than nucleosome depleted regions in young genes and in duplicate genes. This finding was confirmed by measuring the difference in evolutionary rates of binding sites in sensu stricto yeasts at nucleosome occupied regions and nucleosome depleted regions. The binding sites at nucleosome occupied regions exhibited a consistently higher evolution rate than those at nucleosome depleted regions, corroborating the difference in the selection constraints at the two regions. Finally, through site-directed mutagenesis experiment, we found that binding site gain or loss events at nucleosome depleted regions may cause more expression differences than those in nucleosome occupied regions. CONCLUSIONS: Our study indicates the existence of different selection constraint on binding sites at nucleosome occupied regions than at the nucleosome depleted regions. We found that the binding sites have a different rate of evolution at nucleosome occupied and depleted regions. Finally, using transcription factor binding site-directed mutagenesis experiment, we confirmed the difference in the impact of binding site changes on expression at these regions. Thus, our work demonstrates the importance of composite analysis of chromatin and transcriptional evolution. BioMed Central 2011-05-31 /pmc/articles/PMC3124427/ /pubmed/21627806 http://dx.doi.org/10.1186/1471-2148-11-150 Text en Copyright © 2011 Swamy et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Swamy, Krishna BS
Chu, Wen-Yi
Wang, Chun-Yi
Tsai, Huai-Kuang
Wang, Daryi
Evidence of association between Nucleosome Occupancy and the Evolution of Transcription Factor Binding Sites in Yeast
title Evidence of association between Nucleosome Occupancy and the Evolution of Transcription Factor Binding Sites in Yeast
title_full Evidence of association between Nucleosome Occupancy and the Evolution of Transcription Factor Binding Sites in Yeast
title_fullStr Evidence of association between Nucleosome Occupancy and the Evolution of Transcription Factor Binding Sites in Yeast
title_full_unstemmed Evidence of association between Nucleosome Occupancy and the Evolution of Transcription Factor Binding Sites in Yeast
title_short Evidence of association between Nucleosome Occupancy and the Evolution of Transcription Factor Binding Sites in Yeast
title_sort evidence of association between nucleosome occupancy and the evolution of transcription factor binding sites in yeast
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3124427/
https://www.ncbi.nlm.nih.gov/pubmed/21627806
http://dx.doi.org/10.1186/1471-2148-11-150
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