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      Allele-Specific Transcriptome and Methylome Analysis Reveals Stable Inheritance and Cis-Regulation of DNA Methylation in Nasonia

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          Abstract

          Gene expression divergence between closely related species could be attributed to both cis- and trans- DNA sequence changes during evolution, but it is unclear how the evolutionary dynamics of epigenetic marks are regulated. In eutherian mammals, biparental DNA methylation marks are erased and reset during gametogenesis, resulting in paternal or maternal imprints, which lead to genomic imprinting. Whether DNA methylation reprogramming exists in insects is not known. Wasps of the genus Nasonia are non-social parasitoids that are emerging as a model for studies of epigenetic processes in insects. In this study, we quantified allele-specific expression and methylation genome-wide in Nasonia vitripennis and Nasonia giraulti and their reciprocal F1 hybrids. No parent-of-origin effect in allelic expression was found for >8,000 covered genes, suggesting a lack of genomic imprinting in adult Nasonia. As we expected, both significant cis- and trans- effects are responsible for the expression divergence between N. vitripennis and N. giraulti. Surprisingly, all 178 differentially methylated genes are also differentially methylated between the two alleles in F1 hybrid offspring, recapitulating the parental methylation status with nearly 100% fidelity, indicating the presence of strong cis-elements driving the target of gene body methylation. In addition, we discovered that total and allele-specific expression are positively correlated with allele-specific methylation in a subset of the differentially methylated genes. The 100% cis-regulation in F1 hybrids suggests the methylation machinery is conserved and DNA methylation is targeted by cis features in Nasonia. The lack of genomic imprinting and parent-of-origin differentially methylated regions in Nasonia, together with the stable inheritance of methylation status between generations, suggests either a cis-regulatory motif for methylation at the DNA level or highly stable inheritance of an epigenetic signal in Nasonia.

          Abstract

          RNA-sequencing and whole-genome bisulfite sequencing in the hybrid offspring of two Nasonia parasitoid wasp species revealed strong cis-regulation of methylation and allele-specific expression. No gene was found to display genomic imprinting.

          Author Summary

          The relationship between methylation of genomic DNA and expression of the genes that it encodes—and how this relationship changes during evolution—has been widely studied in mammals, but remains less well understood for insects. Here we analyze the expressed mRNA transcripts and genomic DNA methylation of the hybrid offspring of a pair of Nasonia parasitoid wasp species, producing a wealth of information about the regulation of gene expression. We find that variation in DNA sequence impacts expression on the same strand (called “ cis-regulation”), and that cytosine methylation state is also associated in cis with the regulatory consequences of this base alteration. We show that these wasp species lack differential expression dependent on parent-of-origin (called “genomic imprinting”), and that in the hybrids the alleles retain the methylation status of the parental species in a strong cis-regulated fashion. Transcript abundances were also largely driven in a cis-regulated manner, consistent with a correlation between methylation status and expression levels. Despite the many differences between Nasonia and mammals in the impact of genomic DNA methylation, in both groups the use of methylated cytosine has been co-opted in ways that help tune gene expression.

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          Most cited references52

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          Evolutionary changes in cis and trans gene regulation.

          Differences in gene expression are central to evolution. Such differences can arise from cis-regulatory changes that affect transcription initiation, transcription rate and/or transcript stability in an allele-specific manner, or from trans-regulatory changes that modify the activity or expression of factors that interact with cis-regulatory sequences. Both cis- and trans-regulatory changes contribute to divergent gene expression, but their respective contributions remain largely unknown. Here we examine the distribution of cis- and trans-regulatory changes underlying expression differences between closely related Drosophila species, D. melanogaster and D. simulans, and show functional cis-regulatory differences by comparing the relative abundance of species-specific transcripts in F1 hybrids. Differences in trans-regulatory activity were inferred by comparing the ratio of allelic expression in hybrids with the ratio of gene expression between species. Of 29 genes with interspecific expression differences, 28 had differences in cis-regulation, and these changes were sufficient to explain expression divergence for about half of the genes. Trans-regulatory differences affected 55% (16 of 29) of genes, and were always accompanied by cis-regulatory changes. These data indicate that interspecific expression differences are not caused by select trans-regulatory changes with widespread effects, but rather by many cis-acting changes spread throughout the genome.
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            DNA methylation in mammals.

            En Li, Yi Zhang (2014)
            DNA methylation is one of the best characterized epigenetic modifications. In mammals it is involved in various biological processes including the silencing of transposable elements, regulation of gene expression, genomic imprinting, and X-chromosome inactivation. This article describes how DNA methylation serves as a cellular memory system and how it is dynamically regulated through the action of the DNA methyltransferase (DNMT) and ten eleven translocation (TET) enzymes. Its role in the regulation of gene expression, through its interplay with histone modifications, is also described, and its implication in human diseases discussed. The exciting areas of investigation that will likely become the focus of research in the coming years are outlined in the summary.
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              Epigenetic reprogramming in mammals.

              Epigenetic marking systems confer stability of gene expression during mammalian development. Genome-wide epigenetic reprogramming occurs at stages when developmental potency of cells changes. At fertilization, the paternal genome exchanges protamines for histones, undergoes DNA demethylation, and acquires histone modifications, whereas the maternal genome appears epigenetically more static. During preimplantation development, there is passive DNA demethylation and further reorganization of histone modifications. In blastocysts, embryonic and extraembryonic lineages first show different epigenetic marks. This epigenetic reprogramming is likely to be needed for totipotency, correct initiation of embryonic gene expression, and early lineage development in the embryo. Comparative work demonstrates reprogramming in all mammalian species analysed, but the extent and timing varies, consistent with notable differences between species during preimplantation development. Parental imprinting marks originate in sperm and oocytes and are generally protected from this genome-wide reprogramming. Early primordial germ cells possess imprinting marks similar to those of somatic cells. However, rapid DNA demethylation after midgestation erases these parental imprints, in preparation for sex-specific de novo methylation during gametogenesis. Aberrant reprogramming of somatic epigenetic marks after somatic cell nuclear transfer leads to epigenetic defects in cloned embryos and stem cells. Links between epigenetic marking systems appear to be developmentally regulated contributing to plasticity. A number of activities that confer epigenetic marks are firmly established, while for those that remove marks, particularly methylation, some interesting candidates have emerged recently which need thorough testing in vivo. A mechanistic understanding of reprogramming will be crucial for medical applications of stem cell technology.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, CA USA )
                1544-9173
                1545-7885
                5 July 2016
                July 2016
                5 July 2016
                : 14
                : 7
                : e1002500
                Affiliations
                [1 ]Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York, United States of America
                [2 ]Cornell Center for Comparative and Population Genomics, Cornell University, Ithaca, New York, United States of America
                [3 ]Department of Biology, University of Rochester, Rochester, New York, United States of America
                Institute of Science and Technology Austria (IST Austria), AUSTRIA
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: XW JHW AGC. Performed the experiments: XW. Analyzed the data: XW JHW AGC. Contributed reagents/materials/analysis tools: JHW AGC. Wrote the paper: XW JHW AGC.

                Author information
                http://orcid.org/0000-0001-9353-2070
                Article
                PBIOLOGY-D-16-00219
                10.1371/journal.pbio.1002500
                4933354
                27380029
                a1e8fe32-2a09-4279-8546-3e4a7a0df4e9
                © 2016 Wang et al

                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
                : 31 January 2016
                : 3 June 2016
                Page count
                Figures: 5, Tables: 0, Pages: 21
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000057, National Institute of General Medical Sciences;
                Award ID: GM64590
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000057, National Institute of General Medical Sciences;
                Award ID: GM098667
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: 1250790
                Award Recipient :
                This work was supported in part by NIH grant R01 GM64590, the Cornell Center for Comparative and Population Genomics and by the Meinig Family professorship to AGC, and by NSF IOS 1250790, NIH R01 GM098667 and the Nathaniel and Helen Wisch Professorship to JHW. Funding for data deposit provided by the University of Rochester River Campus Libraries. 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
                Cell biology
                Chromosome biology
                Chromatin
                Chromatin modification
                DNA methylation
                Biology and life sciences
                Genetics
                Epigenetics
                Chromatin
                Chromatin modification
                DNA methylation
                Biology and life sciences
                Genetics
                Gene expression
                Chromatin
                Chromatin modification
                DNA methylation
                Biology and life sciences
                Genetics
                DNA
                DNA modification
                DNA methylation
                Biology and life sciences
                Biochemistry
                Nucleic acids
                DNA
                DNA modification
                DNA methylation
                Biology and life sciences
                Genetics
                Epigenetics
                DNA modification
                DNA methylation
                Biology and life sciences
                Genetics
                Gene expression
                DNA modification
                DNA methylation
                Biology and Life Sciences
                Developmental Biology
                Genomic Imprinting
                Biology and Life Sciences
                Genetics
                Epigenetics
                Genomic Imprinting
                Biology and Life Sciences
                Genetics
                Gene Expression
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Biology and Life Sciences
                Genetics
                Epigenetics
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                Vertebrates
                Amniotes
                Mammals
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                Custom metadata
                All F1 RNA-seq data have been deposited in GEO under accession no. GSE74300. WGBS-seq data for N. vitripennis male and N. giraulti F1 samples have been deposited in GEO under accession no. GSE74301. The data presented in the paper has been uploaded to data Dryad ( http://dx.doi.org/10.5061/dryad.qf2t8).

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