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      Bimodal signatures of germline methylation are linked with gene expression plasticity in the coral Acropora millepora

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          Abstract

          Background

          In invertebrates, genes belonging to dynamically regulated functional categories appear to be less methylated than “housekeeping” genes, suggesting that DNA methylation may modulate gene expression plasticity. To date, however, experimental evidence to support this hypothesis across different natural habitats has been lacking.

          Results

          Gene expression profiles were generated from 30 pairs of genetically identical fragments of coral Acropora millepora reciprocally transplanted between distinct natural habitats for 3 months. Gene expression was analyzed in the context of normalized CpG content, a well-established signature of historical germline DNA methylation. Genes with weak methylation signatures were more likely to demonstrate differential expression based on both transplant environment and population of origin than genes with strong methylation signatures. Moreover, the magnitude of expression differences due to environment and population were greater for genes with weak methylation signatures.

          Conclusions

          Our results support a connection between differential germline methylation and gene expression flexibility across environments and populations. Studies of phylogenetically basal invertebrates such as corals will further elucidate the fundamental functional aspects of gene body methylation in Metazoa.

          Electronic supplementary material

          The online version of this article (doi:10.1186/1471-2164-15-1109) contains supplementary material, which is available to authorized users.

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          Most cited references50

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          R: A language and environment for statistical computing

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            Conserved Role of Intragenic DNA Methylation in Regulating Alternative Promoters

            While the methylation of DNA in 5′ promoters suppresses gene expression, the role of DNA methylation in gene bodies is unclear 1–5 . In mammals, tissue- and cell type-specific methylation is present in a small percentage of 5′ CpG island (CGI) promoters, while a far greater proportion occurs across gene bodies, coinciding with highly conserved sequences 5–10 . Tissue-specific intragenic methylation might reduce, 3 or, paradoxically, enhance transcription elongation efficiency 1,2,4,5 . Capped analysis of gene expression (CAGE) experiments also indicate that transcription commonly initiates within and between genes 11–15 . To investigate the role of intragenic methylation, we generated a map of DNA methylation from human brain encompassing 24.7 million of the 28 million CpG sites. From the dense, high-resolution coverage of CpG islands, the majority of methylated CpG islands were revealed to be in intragenic and intergenic regions, while less than 3% of CpG islands in 5′ promoters were methylated. The CpG islands in all three locations overlapped with RNA markers of transcription initiation, and unmethylated CpG islands also overlapped significantly with trimethylation of H3K4, a histone modification enriched at promoters 16 . The general and CpG-island-specific patterns of methylation are conserved in mouse tissues. An in-depth investigation of the human SHANK3 locus 17,18 and its mouse homologue demonstrated that this tissue-specific DNA methylation regulates intragenic promoter activity in vitro and in vivo. These methylation-regulated, alternative transcripts are expressed in a tissue and cell type-specific manner, and are expressed differentially within a single cell type from distinct brain regions. These results support a major role for intragenic methylation in regulating cell context-specific alternative promoters in gene bodies.
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              Plant phenotypic plasticity in a changing climate.

              Climate change is altering the availability of resources and the conditions that are crucial to plant performance. One way plants will respond to these changes is through environmentally induced shifts in phenotype (phenotypic plasticity). Understanding plastic responses is crucial for predicting and managing the effects of climate change on native species as well as crop plants. Here, we provide a toolbox with definitions of key theoretical elements and a synthesis of the current understanding of the molecular and genetic mechanisms underlying plasticity relevant to climate change. By bringing ecological, evolutionary, physiological and molecular perspectives together, we hope to provide clear directives for future research and stimulate cross-disciplinary dialogue on the relevance of phenotypic plasticity under climate change. Copyright © 2010 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                grovesdixon@utexas.edu
                l.bay@aims.gov.au
                matz@utexas.edu
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                15 December 2014
                15 December 2014
                2014
                : 15
                : 1
                : 1109
                Affiliations
                [ ]Institute for Cell and Molecular Biology, University of Texas Austin, Austin, USA
                [ ]Australian Institute of Marine Science, PMB 3, Townsville, QLD 4810 Australia
                [ ]ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD 4811 Australia
                [ ]Department of Integrative Biology, University of Texas Austin, Austin, USA
                Article
                6871
                10.1186/1471-2164-15-1109
                4378018
                25511458
                9b686c76-1bdb-470f-8a5f-e75240b08eb8
                © Dixon et al.; licensee BioMed Central. 2014

                This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 21 August 2014
                : 10 December 2014
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2014

                Genetics
                acropora millepora,coral,dna methylation,gene body methylation,gene expression,flexibility,plasticity

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