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Widespread contribution of transposable elements to the innovation of gene regulatory networks.

ABSTRACT: Transposable elements (TEs) have been shown to contain functional binding sites for certain transcription factors (TFs). However, the extent to which TEs contribute to the evolution of TF binding sites is not well known. We comprehensively mapped binding sites for 26 pairs of orthologous TFs in two pairs of human and mouse cell lines (representing two cell lineages), along with epigenomic profiles, including DNA methylation and six histone modifications. Overall, we found that 20% of binding sites were embedded within TEs. This number varied across different TFs, ranging from 2% to 40%. We further identified 710 TF-TE relationships in which genomic copies of a TE subfamily contributed a significant number of binding peaks for a TF, and we found that LTR elements dominated these relationships in human. Importantly, TE-derived binding peaks were strongly associated with open and active chromatin signatures, including reduced DNA methylation and increased enhancer-associated histone marks. On average, 66% of TE-derived binding events were cell type-specific with a cell type-specific epigenetic landscape. Most of the binding sites contributed by TEs were species-specific, but we also identified binding sites conserved between human and mouse, the functional relevance of which was supported by a signature of purifying selection on DNA sequences of these TEs. Interestingly, several TFs had significantly expanded binding site landscapes only in one species, which were linked to species-specific gene functions, suggesting that TEs are an important driving force for regulatory innovation. Taken together, our data suggest that TEs have significantly and continuously shaped gene regulatory networks during mammalian evolution.

SUBMITTER: Sundaram V

PROVIDER: S-EPMC4248313 | biostudies-literature | 2014 Dec

REPOSITORIES: biostudies-literature

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Widespread contribution of transposable elements to the innovation of gene regulatory networks.

Sundaram Vasavi V Cheng Yong Y Ma Zhihai Z Li Daofeng D Xing Xiaoyun X Edge Peter P Snyder Michael P MP Wang Ting T

Genome research 20141015 12

Transposable elements (TEs) have been shown to contain functional binding sites for certain transcription factors (TFs). However, the extent to which TEs contribute to the evolution of TF binding sites is not well known. We comprehensively mapped binding sites for 26 pairs of orthologous TFs in two pairs of human and mouse cell lines (representing two cell lineages), along with epigenomic profiles, including DNA methylation and six histone modifications. Overall, we found that 20% of binding sit ...[more]

PMID: 25319995

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Project description:BackgroundTransposable elements (TE) make up a large portion of many plant genomes and are playing innovative roles in genome evolution. Several TEs can contribute to gene regulation by influencing expression of nearby genes as stress-responsive regulatory motifs. To delineate TE-mediated plant stress regulatory networks, we took a 2-step computational approach consisting of identifying TEs in the proximity of stress-responsive genes, followed by searching for cis-regulatory motifs in these TE sequences and linking them to known regulatory factors. Through a systematic meta-analysis of RNA-seq expression profiles and genome annotations, we investigated the relation between the presence of TE superfamilies upstream, downstream or within introns of nearby genes and the differential expression of these genes in various stress conditions in the TE-poor Arabidopsis thaliana and the TE-rich Solanum lycopersicum.ResultsWe found that stress conditions frequently expressed genes having members of various TE superfamilies in their genomic proximity, such as SINE upon proteotoxic stress and Copia and Gypsy upon heat stress in A. thaliana, and EPRV and hAT upon infection, and Harbinger, LINE and Retrotransposon upon light stress in S. lycopersicum. These stress-specific gene-proximal TEs were mostly located within introns and more detected near upregulated than downregulated genes. Similar stress conditions were often related to the same TE superfamily. Additionally, we detected both novel and known motifs in the sequences of those TEs pointing to regulatory cooption of these TEs upon stress. Next, we constructed the regulatory network of TFs that act through binding these TEs to their target genes upon stress and discovered TE-mediated regulons targeted by TFs such as BRB/BPC, HD, HSF, GATA, NAC, DREB/CBF and MYB factors in Arabidopsis and AP2/ERF/B3, NAC, NF-Y, MYB, CXC and HD factors in tomato.ConclusionsOverall, we map TE-mediated plant stress regulatory networks using numerous stress expression profile studies for two contrasting plant species to study the regulatory role TEs play in the response to stress. As TE-mediated gene regulation allows plants to adapt more rapidly to new environmental conditions, this study contributes to the future development of climate-resilient plants.

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Widespread contribution of transposable elements to the innovation of gene regulatory networks.

Publications

Widespread contribution of transposable elements to the innovation of gene regulatory networks.

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