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      Dnmt1 is essential for egg production and embryo viability in the large milkweed bug, Oncopeltus fasciatus

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          Abstract

          Background

          The function of cytosine (DNA) methylation in insects remains inconclusive due to a lack of mutant and/or genetic studies.

          Results

          Here, we provide evidence for the functional role of the maintenance DNA methyltransferase 1 ( Dnmt1) in an insect using experimental manipulation. Through RNA interference (RNAi), we successfully posttranscriptionally knocked down Dnmt1 in ovarian tissue of the hemipteran Oncopeltus fasciatus (the large milkweed bug). Individuals depleted for Dnmt1, and subsequently DNA methylation, failed to reproduce. Eggs were inviable and declined in number, and nuclei structure of follicular epithelium was aberrant. Erasure of DNA methylation from gene or transposon element bodies did not reveal a direct causal link to steady-state mRNA levels in somatic cells. These results reveal an important function of Dnmt1 seemingly not contingent on directly controlling gene expression.

          Conclusions

          This study provides direct experimental evidence for a functional role of Dnmt1 in egg production and embryo viability and uncovers a trivial role, if any, for DNA methylation in control of gene expression in O. fasciatus.

          Electronic supplementary material

          The online version of this article (10.1186/s13072-018-0246-5) contains supplementary material, which is available to authorized users.

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          Most cited references40

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          Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning.

          Shawn Cokus, Suhua Feng, Xiaoyu Zhang … (2008)
          Cytosine DNA methylation is important in regulating gene expression and in silencing transposons and other repetitive sequences. Recent genomic studies in Arabidopsis thaliana have revealed that many endogenous genes are methylated either within their promoters or within their transcribed regions, and that gene methylation is highly correlated with transcription levels. However, plants have different types of methylation controlled by different genetic pathways, and detailed information on the methylation status of each cytosine in any given genome is lacking. To this end, we generated a map at single-base-pair resolution of methylated cytosines for Arabidopsis, by combining bisulphite treatment of genomic DNA with ultra-high-throughput sequencing using the Illumina 1G Genome Analyser and Solexa sequencing technology. This approach, termed BS-Seq, unlike previous microarray-based methods, allows one to sensitively measure cytosine methylation on a genome-wide scale within specific sequence contexts. Here we describe methylation on previously inaccessible components of the genome and analyse the DNA methylation sequence composition and distribution. We also describe the effect of various DNA methylation mutants on genome-wide methylation patterns, and demonstrate that our newly developed library construction and computational methods can be applied to large genomes such as that of mouse.
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            Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting.

            Masahiro Kaneda, Masaki Okano, Kenichiro Hata … (2004)
            Imprinted genes are epigenetically marked during gametogenesis so that they are exclusively expressed from either the paternal or the maternal allele in offspring. Imprinting prevents parthenogenesis in mammals and is often disrupted in congenital malformation syndromes, tumours and cloned animals. Although de novo DNA methyltransferases of the Dnmt3 family are implicated in maternal imprinting, the lethality of Dnmt3a and Dnmt3b knockout mice has precluded further studies. We here report the disruption of Dnmt3a and Dnmt3b in germ cells, with their preservation in somatic cells, by conditional knockout technology. Offspring from Dnmt3a conditional mutant females die in utero and lack methylation and allele-specific expression at all maternally imprinted loci examined. Dnmt3a conditional mutant males show impaired spermatogenesis and lack methylation at two of three paternally imprinted loci examined in spermatogonia. By contrast, Dnmt3b conditional mutants and their offspring show no apparent phenotype. The phenotype of Dnmt3a conditional mutants is indistinguishable from that of Dnmt3L knockout mice, except for the discrepancy in methylation at one locus. These results indicate that both Dnmt3a and Dnmt3L are required for methylation of most imprinted loci in germ cells, but also suggest the involvement of other factors.
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              Targeted mutation of the DNA methyltransferase gene results in embryonic lethality

              En Li, Timothy Bestor, Rudolf Jaenisch (1992)
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                Author and article information

                Contributors
                Adam J. Bewick: bewickaj@uga.edu
                Zachary Sanchez: zachary.sanchez25@uga.edu
                Elizabeth C. Mckinney: emckiney@uga.edu
                Allen J. Moore: ajmoore@uga.edu
                Patricia J. Moore: pjmoore@uga.edu
                Robert J. Schmitz: schmitz@uga.edu
                Journal
                Journal ID (nlm-ta): Epigenetics Chromatin
                Journal ID (iso-abbrev): Epigenetics Chromatin
                Title: Epigenetics & Chromatin
                Publisher: BioMed Central (London )
                ISSN (Electronic): 1756-8935
                Publication date (Electronic): 7 January 2019
                Publication date PMC-release: 7 January 2019
                Publication date Collection: 2019
                Volume: 12
                Electronic Location Identifier: 6
                Affiliations
                [1 ]ISNI 0000 0004 1936 738X, GRID grid.213876.9, Department of Genetics, , University of Georgia, ; Athens, GA 30602 USA
                [2 ]ISNI 0000 0004 1936 738X, GRID grid.213876.9, Department of Entomology, , University of Georgia, ; Athens, GA 30602 USA
                Article
                Publisher ID: 246
                DOI: 10.1186/s13072-018-0246-5
                PMC ID: 6322253
                PubMed ID: 30616649
                SO-VID: 4c381c21-670e-41d8-a825-bb3c33db7eab
                Copyright © © The Author(s) 2019
                License:

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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
                Date received : 20 October 2018
                Date accepted : 18 December 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: IOS-1354358
                Award Recipient :
                Funded by: UGA CAES Undergraduate Research Award
                Funded by: FundRef http://dx.doi.org/10.13039/100000875, Pew Charitable Trusts;
                Categories
                Subject: Research
                Custom metadata
                issue-copyright-statement © The Author(s) 2019

                ScienceOpen disciplines: Genetics
                Keywords: dna methylation,dnmt1,reproduction,rnai,transcription
                Data availability:
                ScienceOpen disciplines: Genetics
                Keywords: dna methylation, dnmt1, reproduction, rnai, transcription

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