ECB-ART-51341
BMC Biol
2023 Jun 26;211:149. doi: 10.1186/s12915-023-01645-8.
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Associations between DNA methylation and gene regulation depend on chromatin accessibility during transgenerational plasticity.
Bogan SN
,
Strader ME
,
Hofmann GE
.
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BACKGROUND: Epigenetic processes are proposed to be a mechanism regulating gene expression during phenotypic plasticity. However, environmentally induced changes in DNA methylation exhibit little-to-no association with differential gene expression in metazoans at a transcriptome-wide level. It remains unexplored whether associations between environmentally induced differential methylation and expression are contingent upon other epigenomic processes such as chromatin accessibility. We quantified methylation and gene expression in larvae of the purple sea urchin Strongylocentrotus purpuratus exposed to different ecologically relevant conditions during gametogenesis (maternal conditioning) and modeled changes in gene expression and splicing resulting from maternal conditioning as functions of differential methylation, incorporating covariates for genomic features and chromatin accessibility. We detected significant interactions between differential methylation, chromatin accessibility, and genic feature type associated with differential expression and splicing. RESULTS: Differential gene body methylation had significantly stronger effects on expression among genes with poorly accessible transcriptional start sites while baseline transcript abundance influenced the direction of this effect. Transcriptional responses to maternal conditioning were 4-13 × more likely when accounting for interactions between methylation and chromatin accessibility, demonstrating that the relationship between differential methylation and gene regulation is partially explained by chromatin state. CONCLUSIONS: DNA methylation likely possesses multiple associations with gene regulation during transgenerational plasticity in S. purpuratus and potentially other metazoans, but its effects are dependent on chromatin accessibility and underlying genic features.
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References [+] :
Anastasiadi,
Footprints of global change in marine life: Inferring past environment based on DNA methylation and gene expression marks.
2021, Pubmed
Anastasiadi, Footprints of global change in marine life: Inferring past environment based on DNA methylation and gene expression marks. 2021, Pubmed
Anastasiadi, Consistent inverse correlation between DNA methylation of the first intron and gene expression across tissues and species. 2018, Pubmed
Arenas-Mena, Identification and prediction of developmental enhancers in sea urchin embryos. 2021, Pubmed , Echinobase
Arsenault, The effect of maternal care on gene expression and DNA methylation in a subsocial bee. 2018, Pubmed
Barnett, ATAC-Me Captures Prolonged DNA Methylation of Dynamic Chromatin Accessibility Loci during Cell Fate Transitions. 2020, Pubmed
Bewick, Evolutionary and Experimental Loss of Gene Body Methylation and Its Consequence to Gene Expression. 2019, Pubmed
Bieberstein, First exon length controls active chromatin signatures and transcription. 2012, Pubmed
Biergans, Dnmts and Tet target memory-associated genes after appetitive olfactory training in honey bees. 2015, Pubmed
Boyes, Repression of genes by DNA methylation depends on CpG density and promoter strength: evidence for involvement of a methyl-CpG binding protein. 1992, Pubmed
Brown, Chromatin and epigenetic regulation of pre-mRNA processing. 2012, Pubmed
Chan, The alternative splicing landscape of a coral reef fish during a marine heatwave. 2022, Pubmed
Chen, Differential methylation analysis of reduced representation bisulfite sequencing experiments using edgeR. 2017, Pubmed
Dai, Molecular characterizations of DNA methyltransferase 3 and its roles in temperature tolerance in the whitefly, Bemisia tabaci Mediterranean. 2018, Pubmed
De Paoli-Iseppi, Isoform Age - Splice Isoform Profiling Using Long-Read Technologies. 2021, Pubmed
Dixon, Changes in gene body methylation do not correlate with changes in gene expression in Anthozoa or Hexapoda. 2022, Pubmed
Dixon, Role of gene body methylation in acclimatization and adaptation in a basal metazoan. 2018, Pubmed
Dixon, Evolutionary Consequences of DNA Methylation in a Basal Metazoan. 2016, Pubmed
Donelan, Transgenerational Plasticity in Human-Altered Environments. 2020, Pubmed
Donelson, Transgenerational plasticity and climate change experiments: Where do we go from here? 2018, Pubmed
Ehrlich, DNA methylation and differentiation: silencing, upregulation and modulation of gene expression. 2013, Pubmed
Eirin-Lopez, Marine Environmental Epigenetics. 2019, Pubmed
Engström, Systematic evaluation of spliced alignment programs for RNA-seq data. 2013, Pubmed
Evans, Transcriptomic responses to seawater acidification among sea urchin populations inhabiting a natural pH mosaic. 2017, Pubmed , Echinobase
Flores, Genome-wide association between DNA methylation and alternative splicing in an invertebrate. 2012, Pubmed
Fuchs, Regulation of polyp-to-jellyfish transition in Aurelia aurita. 2014, Pubmed
Fujii, DNA methylation as a mediator of associations between the environment and chronic diseases: A scoping review on application of mediation analysis. 2022, Pubmed
Gallegos, Intron DNA Sequences Can Be More Important Than the Proximal Promoter in Determining the Site of Transcript Initiation. 2017, Pubmed
Galloway, Transgenerational plasticity is adaptive in the wild. 2007, Pubmed
Gao, Differential DNA methylation in discrete developmental stages of the parasitic nematode Trichinella spiralis. 2012, Pubmed
Gatzmann, The methylome of the marbled crayfish links gene body methylation to stable expression of poorly accessible genes. 2018, Pubmed
Glastad, The caste- and sex-specific DNA methylome of the termite Zootermopsis nevadensis. 2016, Pubmed
Grishkevich, Gene length and expression level shape genomic novelties. 2014, Pubmed
Gruber, Rapid progression of ocean acidification in the California Current System. 2012, Pubmed
Guerin, Dual detection of chromatin accessibility and DNA methylation using ATAC-Me. 2021, Pubmed
Hawes, Effects of temperature and salinity stress on DNA methylation in a highly invasive marine invertebrate, the colonial ascidian Didemnum vexillum. 2018, Pubmed
Hong, Genome-wide association study identifies peanut allergy-specific loci and evidence of epigenetic mediation in US children. 2015, Pubmed
Hunt, Functional conservation of DNA methylation in the pea aphid and the honeybee. 2010, Pubmed
Husby, Wild epigenetics: insights from epigenetic studies on natural populations. 2022, Pubmed
Jakšić, The Interplay of Temperature and Genotype on Patterns of Alternative Splicing in Drosophila melanogaster. 2016, Pubmed
Johnson, Differential DNA methylation across environments has no effect on gene expression in the eastern oyster. 2022, Pubmed
Jones, Oil and hypoxia alter DNA methylation and transcription of genes related to neurological function in larval Cyprinodon variegatus. 2022, Pubmed
Keller, Evolutionary Transition of Promoter and Gene Body DNA Methylation across Invertebrate-Vertebrate Boundary. 2016, Pubmed
Kelly, Natural variation and the capacity to adapt to ocean acidification in the keystone sea urchin Strongylocentrotus purpuratus. 2013, Pubmed , Echinobase
Kim, HISAT: a fast spliced aligner with low memory requirements. 2015, Pubmed
Kribelbauer, Toward a Mechanistic Understanding of DNA Methylation Readout by Transcription Factors. 2020, Pubmed
Krueger, Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. 2011, Pubmed
Kudtarkar, Echinobase: an expanding resource for echinoderm genomic information. 2017, Pubmed
Kvist, Pattern of DNA Methylation in Daphnia: Evolutionary Perspective. 2018, Pubmed
Lai, Hypoxia Causes Transgenerational Impairment of Ovarian Development and Hatching Success in Fish. 2019, Pubmed
Laine, An ecologist's guide for studying DNA methylation variation in wild vertebrates. 2023, Pubmed
Lawrence, Software for computing and annotating genomic ranges. 2013, Pubmed
Lea, Genome-wide quantification of the effects of DNA methylation on human gene regulation. 2018, Pubmed
Lea, Maximizing ecological and evolutionary insight in bisulfite sequencing data sets. 2017, Pubmed
Lev Maor, The alternative role of DNA methylation in splicing regulation. 2015, Pubmed
Li, DNA methylation regulates transcriptional homeostasis of algal endosymbiosis in the coral model Aiptasia. 2018, Pubmed
Li-Byarlay, RNA interference knockdown of DNA methyl-transferase 3 affects gene alternative splicing in the honey bee. 2013, Pubmed
Liao, featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. 2014, Pubmed
Libbrecht, Robust DNA Methylation in the Clonal Raider Ant Brain. 2016, Pubmed
Lindeman, Epigenetic, transcriptional and phenotypic responses in two generations of Daphnia magna exposed to the DNA methylation inhibitor 5-azacytidine. 2019, Pubmed
Lindner, Temporal changes in DNA methylation and RNA expression in a small song bird: within- and between-tissue comparisons. 2021, Pubmed
Loughland, DNA methyltransferase 3a mediates developmental thermal plasticity. 2021, Pubmed
Ma, Multiple network algorithm for epigenetic modules via the integration of genome-wide DNA methylation and gene expression data. 2017, Pubmed
Makowski, Indices of Effect Existence and Significance in the Bayesian Framework. 2019, Pubmed
Maunakea, Intragenic DNA methylation modulates alternative splicing by recruiting MeCP2 to promote exon recognition. 2013, Pubmed
McCarthy, Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. 2012, Pubmed
Mehmood, Systematic evaluation of differential splicing tools for RNA-seq studies. 2020, Pubmed
Nanty, Comparative methylomics reveals gene-body H3K36me3 in Drosophila predicts DNA methylation and CpG landscapes in other invertebrates. 2011, Pubmed
Neri, Intragenic DNA methylation prevents spurious transcription initiation. 2017, Pubmed
Nielsen, Genotype and SNP calling from next-generation sequencing data. 2011, Pubmed
Pacis, Gene activation precedes DNA demethylation in response to infection in human dendritic cells. 2019, Pubmed
Park, Comparative analyses of DNA methylation and sequence evolution using Nasonia genomes. 2011, Pubmed
Pearse, Ecological role of purple sea urchins. 2006, Pubmed , Echinobase
Pespeni, Signs of adaptation to local pH conditions across an environmental mosaic in the California Current Ecosystem. 2013, Pubmed , Echinobase
Putnam, Ocean acidification influences host DNA methylation and phenotypic plasticity in environmentally susceptible corals. 2016, Pubmed
Rizzardi, Neuronal brain-region-specific DNA methylation and chromatin accessibility are associated with neuropsychiatric trait heritability. 2019, Pubmed
Robinson, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. 2010, Pubmed
Rose, Introns as Gene Regulators: A Brick on the Accelerator. 2018, Pubmed
Ruhr, Developmental programming of DNA methylation and gene expression patterns is associated with extreme cardiovascular tolerance to anoxia in the common snapping turtle. 2021, Pubmed
Sarda, The evolution of invertebrate gene body methylation. 2012, Pubmed
Secco, Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements. 2015, Pubmed
Shashikant, Global analysis of primary mesenchyme cell cis-regulatory modules by chromatin accessibility profiling. 2018, Pubmed , Echinobase
Shaul, How introns enhance gene expression. 2017, Pubmed
Shayevitch, The importance of DNA methylation of exons on alternative splicing. 2018, Pubmed
Shi, Chromatin accessibility contributes to simultaneous mutations of cancer genes. 2016, Pubmed
Skjærven, Parental micronutrient deficiency distorts liver DNA methylation and expression of lipid genes associated with a fatty-liver-like phenotype in offspring. 2018, Pubmed
Song, The association between DNA methylation and exon expression in the Pacific oyster Crassostrea gigas. 2017, Pubmed
Strader, Genetic variation underlies plastic responses to global change drivers in the purple sea urchin, Strongylocentrotus purpuratus. 2022, Pubmed , Echinobase
Su, Neuronal activity modifies the chromatin accessibility landscape in the adult brain. 2017, Pubmed
Sultan, Influence of RNA extraction methods and library selection schemes on RNA-seq data. 2014, Pubmed
Suzuki, CpG methylation is targeted to transcription units in an invertebrate genome. 2007, Pubmed
Trigg, Invertebrate methylomes provide insight into mechanisms of environmental tolerance and reveal methodological biases. 2022, Pubmed
VanderWeele, Mediation Analysis: A Practitioner's Guide. 2016, Pubmed
Wang, Hypoxia causes transgenerational impairments in reproduction of fish. 2016, Pubmed
Wang, Network-guided regression for detecting associations between DNA methylation and gene expression. 2014, Pubmed
Wang, Allele-Specific Transcriptome and Methylome Analysis Reveals Stable Inheritance and Cis-Regulation of DNA Methylation in Nasonia. 2016, Pubmed
Wong, Transcriptomics reveal transgenerational effects in purple sea urchin embryos: Adult acclimation to upwelling conditions alters the response of their progeny to differential pCO2 levels. 2018, Pubmed , Echinobase
Wong, Intron retention is regulated by altered MeCP2-mediated splicing factor recruitment. 2017, Pubmed
Wright, Gene expression associated with white syndromes in a reef building coral, Acropora hyacinthus. 2015, Pubmed
Xu, Population-level analysis reveals the widespread occurrence and phenotypic consequence of DNA methylation variation not tagged by genetic variation in maize. 2019, Pubmed
Xu, Intragenic DNA methylation regulates insect gene expression and reproduction through the MBD/Tip60 complex. 2021, Pubmed
Yang, Gene body methylation can alter gene expression and is a therapeutic target in cancer. 2014, Pubmed
Yearim, HP1 is involved in regulating the global impact of DNA methylation on alternative splicing. 2015, Pubmed
Yu, ChIPseeker: an R/Bioconductor package for ChIP peak annotation, comparison and visualization. 2015, Pubmed
Zemach, Genome-wide evolutionary analysis of eukaryotic DNA methylation. 2010, Pubmed
Zilberman, An evolutionary case for functional gene body methylation in plants and animals. 2017, Pubmed