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Novel mRNAs 3' end-associated cis-regulatory elements with epigenomic signatures of mammalian enhancers in the Arabidopsis genome.

ABSTRACT: The precise spatial and temporal control of gene expression requires the coordinated action of genomic cis-regulatory elements (CREs), including transcriptional enhancers. However, our knowledge of enhancers in plants remains rudimentary and only a few plant enhancers have been experimentally defined. Here, we screened the Arabidopsis thaliana genome and identified >1900 unique candidate CREs that carry the genomic signatures of mammalian enhancers. These were termed putative enhancer-like elements (PEs). Nearly all PEs are intragenic and, unexpectedly, most associate with the 3' ends of protein-coding genes. PEs are hotspots for transcription factor binding and harbor motifs resembling cleavage/polyadenylation signals, potentially coupling 3' end processing to the transcriptional regulation of other genes. Hi-C data showed that 24% of PEs are located at regions that can interact intrachromosomally with other protein-coding genes and, surprisingly, many of these target genes interact with PEs through their 3' UTRs. Examination of the genomes of 1135 sequenced Arabidopsis accessions showed that PEs are conserved. Our findings suggest that the identified PEs may serve as transcriptional enhancers and sites for mRNA 3' end processing, and constitute a novel group of CREs in Arabidopsis.

SUBMITTER: Wang HV

PROVIDER: S-EPMC6800480 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Novel mRNAs 3' end-associated cis-regulatory elements with epigenomic signatures of mammalian enhancers in the Arabidopsis genome.

Wang Hsiao-Lin V HV Chekanova Julia A JA

RNA (New York, N.Y.) 20190716 10

The precise spatial and temporal control of gene expression requires the coordinated action of genomic cis-regulatory elements (CREs), including transcriptional enhancers. However, our knowledge of enhancers in plants remains rudimentary and only a few plant enhancers have been experimentally defined. Here, we screened the Arabidopsis thaliana genome and identified >1900 unique candidate CREs that carry the genomic signatures of mammalian enhancers. These were termed putative enhan ...[more]

PMID: 31311821

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Project description:cis-regulatory DNA sequences known as enhancers control gene expression in space and time. They are central to metazoan development and are often responsible for changes in gene regulation that contribute to phenotypic evolution. Here, we examine the sequence, function, and genomic location of enhancers controlling tissue- and cell-type specific expression of the yellow gene in six Drosophila species. yellow is required for the production of dark pigment, and its expression has evolved largely in concert with divergent pigment patterns. Using Drosophila melanogaster as a transgenic host, we examined the expression of reporter genes in which either 5' intergenic or intronic sequences of yellow from each species controlled the expression of Green Fluorescent Protein. Surprisingly, we found that sequences controlling expression in the wing veins, as well as sequences controlling expression in epidermal cells of the abdomen, thorax, and wing, were located in different genomic regions in different species. By contrast, sequences controlling expression in bristle-associated cells were located in the intron of all species. Differences in the precise pattern of spatial expression within the developing epidermis of D. melanogaster transformants usually correlated with adult pigmentation in the species from which the cis-regulatory sequences were derived, which is consistent with cis-regulatory evolution affecting yellow expression playing a central role in Drosophila pigmentation divergence. Sequence comparisons among species favored a model in which sequential nucleotide substitutions were responsible for the observed changes in cis-regulatory architecture. Taken together, these data demonstrate frequent changes in yellow cis-regulatory architecture among Drosophila species. Similar analyses of other genes, combining in vivo functional tests of enhancer activity with in silico comparative genomics, are needed to determine whether the pattern of regulatory evolution we observed for yellow is characteristic of genes with rapidly evolving expression patterns.

Project description:BackgroundSequence features in promoter regions are involved in regulating gene transcription initiation. Although numerous computational methods have been developed for predicting transcriptional start sites (TSSs) or transcription factor (TF) binding sites (TFBSs), they lack annotations for do not consider some important regulatory features such as CpG islands, tandem repeats, the TATA box, CCAAT box, GC box, over-represented oligonucleotides, DNA stability, and GC content. Additionally, the combinatorial interaction of TFs regulates the gene group that is associated with same expression pattern. To investigate gene transcriptional regulation, an integrated system that annotates regulatory features in a promoter sequence and detects co-regulation of TFs in a group of genes is needed.ResultsThis work identifies TSSs and regulatory features in a promoter sequence, and recognizes co-occurrence of cis-regulatory elements in co-expressed genes using a novel system. Three well-known TSS prediction tools are incorporated with orthologous conserved features, such as CpG islands, nucleotide composition, over-represented hexamer nucleotides, and DNA stability, to construct the novel Gene Promoter Miner (GPMiner) using a support vector machine (SVM). According to five-fold cross-validation results, the predictive sensitivity and specificity are both roughly 80%. The proposed system allows users to input a group of gene names/symbols, enabling the co-occurrence of TFBSs to be determined. Additionally, an input sequence can also be analyzed for homogeneity of experimental mammalian promoter sequences, and conserved regulatory features between homologous promoters can be observed through cross-species analysis. After identifying promoter regions, regulatory features are visualized graphically to facilitate gene promoter observations.ConclusionsThe GPMiner, which has a user-friendly input/output interface, has numerous benefits in analyzing human and mouse promoters. The proposed system is freely available at http://GPMiner.mbc.nctu.edu.tw/.

Dataset Information

Novel mRNAs 3' end-associated cis-regulatory elements with epigenomic signatures of mammalian enhancers in the Arabidopsis genome.

Publications

Novel mRNAs 3' end-associated <i>cis</i>-regulatory elements with epigenomic signatures of mammalian enhancers in the <i>Arabidopsis</i> genome.

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