Dataset Information

Protein evolution in yeast transcription factor subnetworks.

ABSTRACT: When averaged over the full yeast protein-protein interaction and transcriptional regulatory networks, protein hubs with many interaction partners or regulators tend to evolve significantly more slowly due to increased negative selection. However, genome-wide analysis of protein evolution in the subnetworks of associations involving yeast transcription factors (TFs) reveals that TF hubs do not tend to evolve significantly more slowly than TF non-hubs. This result holds for all four major types of TF hubs: interaction hubs, regulatory in-degree and out-degree hubs, as well as co-regulatory hubs that jointly regulate target genes with many TFs. Furthermore, TF regulatory in-degree hubs tend to evolve significantly more quickly than TF non-hubs. Most importantly, the correlations between evolutionary rate (K(A)/K(S)) and degrees for TFs are significantly more positive than those for generic proteins within the same global protein-protein interaction and transcriptional regulatory networks. Compared to generic protein hubs, TF hubs operate at a higher level in the hierarchical structure of cellular networks, and hence experience additional evolutionary forces (relaxed negative selection or positive selection through network rewiring). The striking difference between the evolution of TF hubs and generic protein hubs demonstrates that components within the same global network can be governed by distinct organizational and evolutionary principles.

SUBMITTER: Wang Y

PROVIDER: S-EPMC2952844 | biostudies-other | 2010 Oct

REPOSITORIES: biostudies-other

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Protein evolution in yeast transcription factor subnetworks.

Wang Yong Y Franzosa Eric A EA Zhang Xiang-Sun XS Xia Yu Y

Nucleic acids research 20100513 18

When averaged over the full yeast protein-protein interaction and transcriptional regulatory networks, protein hubs with many interaction partners or regulators tend to evolve significantly more slowly due to increased negative selection. However, genome-wide analysis of protein evolution in the subnetworks of associations involving yeast transcription factors (TFs) reveals that TF hubs do not tend to evolve significantly more slowly than TF non-hubs. This result holds for all four major types o ...[more]

PMID: 20466810

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Project description:BackgroundDivergence 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.ResultsWe 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.ConclusionsOur 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.

Dataset Information

Protein evolution in yeast transcription factor subnetworks.

Publications

Protein evolution in yeast transcription factor subnetworks.

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