Evolutionary rewiring of wheat abiotic stress responsive network by lineage-specific transposable elements I
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ABSTRACT: The yield of wheat is highly impacted by environmental stresses. The combinatorial regulation of sequence-specific transcription factors(TFs) defines a regulatory network that underlies plant stress responses. Here we created a comprehensive catalog of genomic binding sites of 115 TFs underlying abiotic stress responses by leveraging DAP-seq in Triticum Urartu, along with epigenomic profiles. The majority of gene distant TF binding sites(TFBS) are embedded in transposable elements(TEs), whose functional relevance was supported by a signature of purifying selection and active epigenomic features. Furthermore, ~30% non-TE TFBS share high sequence similarity with TE-embeded TFBS, potentially derived from Triticeae-specific TEs and have almost no sequence homology in non-Triticeae species. The expansion of TE-derived TFBS in wheat linked to wheat-specific stress responsive genes, suggesting that TEs are an important driving force for regulatory innovation. Altogether, TEs have significantly and continuously shaped regulatory network in wheat adaptation.
Project description:The yield of wheat is highly impacted by environmental stresses. The combinatorial regulation of sequence-specific transcription factors(TFs) defines a regulatory network that underlies plant stress responses. Here we created a comprehensive catalog of genomic binding sites of 115 TFs underlying abiotic stress responses by leveraging DAP-seq in Triticum Urartu, along with epigenomic profiles. The majority of gene distant TF binding sites(TFBS) are embedded in transposable elements(TEs), whose functional relevance was supported by a signature of purifying selection and active epigenomic features. Furthermore, ~30% non-TE TFBS share high sequence similarity with TE-embeded TFBS, potentially derived from Triticeae-specific TEs and have almost no sequence homology in non-Triticeae species. The expansion of TE-derived TFBS in wheat linked to wheat-specific stress responsive genes, suggesting that TEs are an important driving force for regulatory innovation. Altogether, TEs have significantly and continuously shaped regulatory network in wheat adaptation.
Project description:The yield of wheat is highly impacted by environmental stresses. The combinatorial regulation of sequence-specific transcription factors(TFs) defines a regulatory network that underlies plant stress responses. Here we created a comprehensive catalog of genomic binding sites of 115 TFs underlying abiotic stress responses by leveraging DAP-seq in Triticum Urartu, along with epigenomic profiles. The majority of gene distant TF binding sites(TFBS) are embedded in transposable elements(TEs), whose functional relevance was supported by a signature of purifying selection and active epigenomic features. Furthermore, ~30% non-TE TFBS share high sequence similarity with TE-embeded TFBS, potentially derived from Triticeae-specific TEs and have almost no sequence homology in non-Triticeae species. The expansion of TE-derived TFBS in wheat linked to wheat-specific stress responsive genes, suggesting that TEs are an important driving force for regulatory innovation. Altogether, TEs have significantly and continuously shaped regulatory network in wheat adaptation.
Project description:Common wheat (T. aestivum) converged three subgenomes adapted to different environments. The combinatorial interaction between transcription factors (TFs) and regulatory elements (REs) defines a regulatory circuit that underlies subgenome convergence and divergence. Compared to the relatively conserved gene composition across subgenomes, the intergenic regions with abundant REs is drastically diversified by almost complete TE turnovers, raising major questions regarding how subgenome convergent and divergent regulation is encoded in the highly diversified intergenic regions, and the impact of TE evolution on regulatory conservation and innovation. In the present study, we created genome-wide TF binding catalog to assemble an extensive wheat regulatory network comprising connections among 182 TFs. The different effects of ancient and recent TE insertions on regulatory specificity were observed. Subgenome asymmetric TE expansion is an important source of subgenome divergent TFBS, which help explain the vast occupancy difference across subgenomes. Interestingly, the ancient expansion of RLC_famc1.4-derived TFBS occurred in more than 25% triads promoters. A significant fraction of these TE-derived TFBS subjected to region-specific evolutionary selections, resulting in subgenome-balanced TF binding but unbalanced degeneration of flanking TE sequences. These TE-derived subgenome convergent and divergent regulation linked to subgenome conserved and diversified pathways, suggesting that TEs are an important regulatory driving force contributed to polyploid evolution. Overall, this study demonstrated the impact of TEs on shaping the plasticity and adaptation of common wheat, enriched the theories of TE-promoted transcriptional innovation from the evolutionary aspects of polyploid regulation since first reported by McClintock.
Project description:Transposable elements (TE) have been shown to contrain functional transcription factor (TF) binding sites for long, but the extent to which TEs contribute TF binding sites is not well know. Here, we comprehensively mapped binding sites for 26 pairs of orthologous TFs, in two pairs of human and mouse cell lines (i.e., leukemia, and lymphoblast), along with epigenomic profiles representing DNA methylation and six histone modifications. We found that on average, 20% of TF binding sites were embedded in TEs. We further identified 710 TF-TE relationships in which certain TE subfamilies enriched for TF binidng sites. TE-derived TF binding peaks were also strongly associated with decreased DNA methylation and increased enhancer-associated histone marks. Most of the TE-derived TF binding sites were species-specific, but we also identified conserved binding sites. Additionally, 66% of TE-derived TF binding events were cell-type specific, associated with cell-type specific epigenetic landscape. For data usage terms and conditions, please refer to http://www.genome.gov/27528022 and http://www.genome.gov/Pages/Research/ENCODE/ENCODEDataReleasePolicyFinal2008.pdf To evaluate the contribution of transposable elements (TE) to transcription factor (TF) binding landscapes, we profiled ChIP-seq datasets for 26 TFs in two cell lines in human and mouse, generated by the ENCODE and MouseENCODE consortia. The epigenomic profiles were evaluated from six histone modification in each of the cell lines, also generated by the consortia. We added DNA methylation to the epigenomic profiles, using two complementary techniques, MeDIP-seq and MRE-seq. The mouse data related to this study are available through GSE57230: http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE57230
Project description:Transposable elements (TE) have been shown to contrain functional transcription factor (TF) binding sites for long, but the extent to which TEs contribute TF binding sites is not well know. Here, we comprehensively mapped binding sites for 26 pairs of orthologous TFs, in two pairs of human and mouse cell lines (i.e., leukemia, and lymphoblast), along with epigenomic profiles representing DNA methylation and six histone modifications. We found that on average, 20% of TF binding sites were embedded in TEs. We further identified 710 TF-TE relationships in which certain TE subfamilies enriched for TF binidng sites. TE-derived TF binding peaks were also strongly associated with decreased DNA methylation and increased enhancer-associated histone marks. Most of the TE-derived TF binding sites were species-specific, but we also identified conserved binding sites. Additionally, 66% of TE-derived TF binding events were cell-type specific, associated with cell-type specific epigenetic landscape. For data usage terms and conditions, please refer to http://www.genome.gov/27528022 and http://www.genome.gov/Pages/Research/ENCODE/ENCODEDataReleasePolicyFinal2008.pdf To evaluate the contribution of transposable elements (TE) to transcription factor (TF) binding landscapes, we profiled ChIP-seq datasets for 26 TFs in two cell lines in human and mouse, generated by the ENCODE and MouseENCODE consortia. The epigenomic profiles were evaluated from six histone modification in each of the cell lines, also generated by the consortia. We added DNA methylation to the epigenomic profiles, using two complementary techniques, MeDIP-seq and MRE-seq. The human data related to this study are available through GSE56774: http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE56774
Project description:Arbuscular mycorrhizal (AM) fungi form mutualistic relationships with most land plant species. AM fungi have long been considered as ancient asexuals. Long-term clonal evolution would be remarkable for a eukaryotic lineage and suggests the importance of alternative mechanisms to promote genetic variability facilitating adaptation. Here, we assessed the potential of transposable elements (TEs) for generating genomic diversity. The dynamic expression of TEs during Rhizophagus irregularis spore development suggests ongoing TE activity. We find Mutator-like elements located near genes belonging to highly expanded gene families. Characterising the epigenomic status of R. irregularis provides evidence of DNA methylation and small RNA production occurring at TE loci. Our results support a potential role for TEs in shaping the genome, and roles for DNA methylation and small RNA-mediated silencing in regulating TEs. A well-controlled balance between TE activity and repression may therefore contribute to genome evolution in AM fungi.
Project description:De-repression of transposable elements (TEs) occurs concomitantly with the progressive loss of DNA methylation during carcinogenesis. The activation of promoters within high copy number TE families can thereby massively remodel the transcriptional and epigenetic state of cancer cells. This effect is accelerated following epigenetic therapy. However, whether TE de-repression is purely stochastic or co-regulated with genic transcriptional programs is poorly understood. Using single cell 5’ RNA-sequencing, we characterize over ten-fold variation in global TE expression per single cancer cell following epigenetic therapy . We uncover combinatorial TE expression patterns across thousands of transcribed TE loci from hundreds of conserved families. These signatures are associated with distinct cell cycle stages, stress responses and additional gene regulatory processes. We finally exemplify how sequence composition and epigenomic context cooperate to shape the dynamic transcriptional landscape of large TE families.. Single cell RNA-sequencing thereby implicates thousands of potent promoters within TEs as an underestimated source of regulatory heterogeneity in cancer.
Project description:Transposable elements (TEs) have significantly influenced the evolution of transcriptional regulatory networks in the human genome. Post-transcriptional regulation of human genes by TE-derived sequences has been observed in specific contexts, but has yet to be systematically and comprehensively investigated. Here, studied a collection of CLIP-Seq (CrossLinked ImmunoPrecipitation) experiments mapping the RNA binding sites for a diverse set of 46 human proteins across 68 experiments to explore the role of TEs in post-transcriptional regulation genome-wide via RNA-protein interactions. We detected widespread interactions between RNA binding proteins (RBPs) and various families of TE-derived sequence in the CLIP-Seq data. Alignment coverage clustered on specific positions of the TE consensus sequences, illuminating a diversity of TE-specific motifs for many RBPs. Evidence of binding and conservation of these motifs in the nonrepetitive transcriptome suggest that TEs have appropriated existing sequence preferences of the RBP. Upon depletion of the RBPs, transcripts possessing TE-derived binding sites were similarly regulated as those bound in nonrepetitive sequence. However, in a few cases the effect of RBP binding depended on the specific TE family boundM-bM-^@M-^Te.g., the ubiquitously expressed RBP HuR conferred opposite effects on stability to transcripts when bound to Alu elements versus other families. Our meta-analysis suggests a widespread role for TEs in shaping RNA-protein regulatory networks in the human genome. HuR formaldehyde RIP-Seq in K562 cells, with RIP and input sequenced in triplicate.
Project description:Transposable elements (TE) have been shown to contrain functional transcription factor (TF) binding sites for long, but the extent to which TEs contribute TF binding sites is not well know. Here, we comprehensively mapped binding sites for 26 pairs of orthologous TFs, in two pairs of human and mouse cell lines (i.e., leukemia, and lymphoblast), along with epigenomic profiles representing DNA methylation and six histone modifications. We found that on average, 20% of TF binding sites were embedded in TEs. We further identified 710 TF-TE relationships in which certain TE subfamilies enriched for TF binidng sites. TE-derived TF binding peaks were also strongly associated with decreased DNA methylation and increased enhancer-associated histone marks. Most of the TE-derived TF binding sites were species-specific, but we also identified conserved binding sites. Additionally, 66% of TE-derived TF binding events were cell-type specific, associated with cell-type specific epigenetic landscape. For data usage terms and conditions, please refer to http://www.genome.gov/27528022 and http://www.genome.gov/Pages/Research/ENCODE/ENCODEDataReleasePolicyFinal2008.pdf
Project description:Transposable elements (TE) have been shown to contrain functional transcription factor (TF) binding sites for long, but the extent to which TEs contribute TF binding sites is not well know. Here, we comprehensively mapped binding sites for 26 pairs of orthologous TFs, in two pairs of human and mouse cell lines (i.e., leukemia, and lymphoblast), along with epigenomic profiles representing DNA methylation and six histone modifications. We found that on average, 20% of TF binding sites were embedded in TEs. We further identified 710 TF-TE relationships in which certain TE subfamilies enriched for TF binidng sites. TE-derived TF binding peaks were also strongly associated with decreased DNA methylation and increased enhancer-associated histone marks. Most of the TE-derived TF binding sites were species-specific, but we also identified conserved binding sites. Additionally, 66% of TE-derived TF binding events were cell-type specific, associated with cell-type specific epigenetic landscape. For data usage terms and conditions, please refer to http://www.genome.gov/27528022 and http://www.genome.gov/Pages/Research/ENCODE/ENCODEDataReleasePolicyFinal2008.pdf