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      Environmentally Selected Aphid Variants in Clonality Context Display Differential Patterns of Methylation in the Genome

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          Abstract

          Heritability of acquired phenotypic traits is an adaptive evolutionary process that appears more complex than the basic allele selection guided by environmental pressure. In insects, the trans-generational transmission of epigenetic marks in clonal and/or sexual species is poorly documented. Aphids were used as a model to explore this feature because their asexual phase generates a stochastic and/or environment-oriented repertoire of variants. The a priori unchanged genome in clonal individuals prompts us to hypothesize whether covalent methyl DNA marks might be associated to the phenotypic variability and fitness selection. The full differential transcriptome between two environmentally selected clonal variants that originated from the same founder mother was mapped on the entire genomic scaffolds, in parallel with the methyl cytosine distribution. Data suggest that the assortments of heavily methylated DNA sites are distinct in these two clonal phenotypes. This might constitute an epigenetic mechanism that confers the robust adaptation of insect species to various environments involving clonal reproduction.

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          Insects as innovative models for functional studies of DNA methylation.

          The emerging field of epigenomics has the potential to bridge the gap between static genomic sequences and complex phenotypes that arise from multigenic, nonlinear and often context-dependent interactions. However, this goal can only be achieved if easily manageable experimental systems are available in which changes in epigenomic settings can be evaluated in the context of the phenotype under investigation. Recent progress in the characterization of insect DNA methylation patterns enables evaluation of the extent to which epigenetic mechanisms contribute to complex phenotypes in easily accessible organisms whose relatively small genomes are not only sparingly methylated, but the methylated sites are also found almost exclusively in gene bodies. The implementation of insect models in the study of DNA methylation will accelerate progress in understanding the functional significance of this important epigenetic mechanism in controlling gene splicing, in environmentally driven reprogramming of gene expression and in adult brain plasticity. Copyright © 2011 Elsevier Ltd. All rights reserved.
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            Author and article information

            Contributors
            Role: Editor
            Journal
            PLoS One
            PLoS ONE
            plos
            plosone
            PLoS ONE
            Public Library of Science (San Francisco, USA )
            1932-6203
            2014
            31 December 2014
            : 9
            : 12
            : e115022
            Affiliations
            [1 ]Institute Sophia Agrobiotech, INRA/CNRS/UNS, University Nice Sophia Antipolis, Sophia Antipolis, France
            [2 ]Institute of Plant Protection, Volcani Center, Rehovot, Israel
            [3 ]Institute of Developmental Biology and Cancer, CNRS, University Nice Sophia Antipolis, Sophia Antipolis, France
            [4 ]Beckman Coulter Genomics SA, Grenoble, France
            Universität Stuttgart, Germany
            Author notes

            Competing Interests: Stéphanie Penaud is employed by the Company Beckman Coulter Genomics SA, but there are no financial competing interests. Thus, this does not alter the authors’ adherence to PLOS ONE policies on sharing data and materials.

            Conceived and designed the experiments: AR AD CP M. Clément M. Capovilla CR MDR SP NL. Performed the experiments: AR AD CP M. Clément M. Capovilla CR MDR SP NL. Analyzed the data: AR AD CP M. Clément M. Capovilla CR MDR SP NL. Contributed reagents/materials/analysis tools: AR AD CP M. Clément M. Capovilla CR MDR SP NL. Contributed to the writing of the manuscript: CP M. Clément AR M. Capovilla.

            [¤]

            Current address: I3S Laboratory, CNRS, University Nice Sophia Antipolis, Sophia Antipolis, France

            Article
            PONE-D-14-27907
            10.1371/journal.pone.0115022
            4281257
            25551225
            aa44705f-47b4-493e-901e-6f58e23023aa
            Copyright @ 2014

            This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

            History
            : 23 June 2014
            : 17 November 2014
            Page count
            Pages: 25
            Funding
            The authors were supported by ANR “Exdisum” 2006-2009, grant PEPS CNRS 2010 and ANR “Methylclonome” 2011–2015. The authors are thankful for the support of the French National Research Agency (ANR) for PhD students through the “Investments for the Future” LABEX SIGNALIFE (#ANR-11-LABX-0028-01).The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
            Categories
            Research Article
            Biology and Life Sciences
            Ecology
            Genetics
            Organisms
            Population Biology
            Systems Biology
            Ecology and Environmental Sciences
            Environmental Impacts
            Habitats
            Species Colonization
            Custom metadata
            The authors confirm that all data underlying the findings are fully available without restriction. Dataset were deposited to NIH Short Read Archive under the references SRX719266 for the genes up-regulated in the pink variant, SRX719265 for the genes upregulated in the green variant, SRX719262 for methylated fragment found in the green variant and SRX719263 for methylated fragment found in the pink variant.

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