Dynamic control of enhancer activity drives stage-specific gene expression during flower morphogenesis

Yan, Wenhao; Chen, Dijun; Schumacher, Julia; Durantini, Diego; Engelhorn, Julia; Chen, Ming; Carles, Cristel C.; Kaufmann, Kerstin

doi:10.1038/s41467-019-09513-2

Cited by 90 publications

(93 citation statements)

References 81 publications

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“…In eukaryotes, open chromatin regions (OCRs) along the genome with depleted nucleosomes harbor various categories of cis-regulatory elements (CREs), including promoters, enhancers, and insulators, and are accessible to different trans-acting factors, such as transcription factors (TFs) that dynamically modulate gene expression [1][2][3][4][5][6][7]. Using high-throughput open chromatin mapping technologies, extensive local CREs proximal to genes and distal CREs in intergenic regions have been identified in mammals and plants [1,4,6,[8][9][10][11][12].…”

Section: Introductionmentioning

confidence: 99%

3D genome architecture coordinates trans and cis regulation of differentially expressed ear and tassel genes in maize

et al. 2020

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Background: Maize ears and tassels are two separate types of inflorescence which are initiated by similar developmental processes but gradually develop distinct architectures. However, coordinated trans and cis regulation of differentially expressed genes determining ear and tassel architecture within the 3D genome context is largely unknown. Results: We identify 56,055 and 52,633 open chromatin regions (OCRs) in developing maize ear and tassel primordia using ATAC-seq and characterize combinatorial epigenome features around these OCRs using ChIP-seq, Bisulfite-seq, and RNA-seq datasets. Our integrative analysis of coordinated epigenetic modification and transcription factor binding to OCRs highlights the cis and trans regulation of differentially expressed genes in ear and tassel controlling inflorescence architecture. We further systematically map chromatin interactions at high-resolution in corresponding tissues using in situ digestion-ligation-only Hi-C (DLO Hi-C). The extensive chromatin loops connecting OCRs and genes provide a 3D view on cisand trans-regulatory modules responsible for ear-and tassel-specific gene expression. We find that intergenic SNPs tend to locate in distal OCRs, and our chromatin interaction maps provide a potential mechanism for trait-associated intergenic SNPs that may contribute to phenotypic variation by influencing target gene expression through chromatin loops. Conclusions: Our comprehensive epigenome annotations and 3D genome maps serve as valuable resource and provide a deep understanding of the complex regulatory mechanisms of genes underlying developmental and morphological diversities between maize ear and tassel.

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Section: Introductionmentioning

confidence: 99%

3D genome architecture coordinates trans and cis regulation of differentially expressed ear and tassel genes in maize

et al. 2020

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“…An activating histone modification that was not included in the chromatin state classification is H3K27ac, the antagonist to the Polycomb mark H3K27me3. It is mainly found in gene bodies and correlates positively with gene expression [33]. At genome scale, H3K27ac is negatively correlated with JSD in all three contexts (Fig.…”

Section: Histone Signatures Characteristic For Gene Bodies and With Dmentioning

confidence: 81%

Cell Type-specific Genome Scans of DNA Methylation Diversity Indicate an Important Role for Transposable Elements

Kartal

Schmid

Grossniklaus

2019

Preprint

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The epigenome modulates the activity of genes and supports the stability of the genome. The epigenome can also contain phenotypically relevant, heritable marks that may vary at the organismic and population level. Such non-genetic standing variation may be relevant to ecological and evolutionary processes. To identify loci susceptible to selection, it is common to profile large populations at the genome scale, yet methods to perform such scans for epigenetic diversity are barely tapped. Here, we develop a scalable, information-theoretic approach to assess epigenome diversity based on Jensen-Shannon divergence (JSD) and demonstrate its practicality by measuring cell type-specific methylation diversity in the model plant Arabidopsis thaliana. DNA methylation diversity tends to be increased in the CG as compared to the non-CG (CHG and CHH) sequence context but the tissue or cell type has an impact on diversity at non-CG sites. Less accessible, more heterochromatic states of chromatin exhibit increased diversity. Genes tend to carry more single-methylation polymorphisms when they harbor gene body-like chromatin signatures and flank transposable elements (TEs). In conclusion, the analysis of DNA methylation with JSD in Arabidopsis demonstrates that the genomic location of a gene dominates its methylation diversity, in particular the proximity to TEs which are increasingly viewed as drivers of evolution. Importantly, the JSD-based approach we implemented here is applicable to any population-level epigenomic data set to analyze variation in epigenetic marks among individuals, tissues, or cells of any organism, including the epigenetic heterogeneity of cells in healthy or diseased organs such as tumors.

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“…8-13 ). Furthermore, the resulting chromatin states were interpreted based on enrichment analysis of various types of functional annotations, such as gene elements, neighboring gene expression pattern, TF binding, chromatin accessibility and predicted enhancers 20,35 . To this end, the “OverlapEnrichment” and “NeighborhoodEnrichment” commands were used in the analysis.…”

Section: Methodsmentioning

confidence: 99%

ChIP-Hub: an Integrative Platform for Exploring Plant Regulome

Chen

Zhang

et al. 2019

Preprint

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Plant genomes encode a complex and evolutionary diverse regulatory grammar that forms the basis for most life on earth. A wealth of regulome and epigenome data have been generated in various plant species, but no common, standardized resource is available so far for biologists. Here we present ChIP-Hub, an integrative web-based platform in the ENCODE standards that bundles publicly available datasets reanalyzed from >40 plant species, allowing visualization and meta-analysis.

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Dynamic control of enhancer activity drives stage-specific gene expression during flower morphogenesis

Cited by 90 publications

References 81 publications

3D genome architecture coordinates trans and cis regulation of differentially expressed ear and tassel genes in maize

3D genome architecture coordinates trans and cis regulation of differentially expressed ear and tassel genes in maize

Cell Type-specific Genome Scans of DNA Methylation Diversity Indicate an Important Role for Transposable Elements

ChIP-Hub: an Integrative Platform for Exploring Plant Regulome

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