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      Epigenetic Modifications during Angiosperm Gametogenesis

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          Abstract

          Angiosperms do not contain a distinct germline, but rather develop gametes from gametophyte initials that undergo cell division. These gametes contain cells that give rise to an endosperm and the embryo. DNA methylation is decreased in the vegetative nucleus (VN) and central cell nuclei (CCN) resulting in expression of transposable elements (TEs). It is thought that the siRNAs produced in response to TE expression are able to travel to the sperm cells and egg cells (EC) from VN and CCN, respectively, in order to enforce silencing there. Demethylation during gametogenesis helps ensure that even newly integrated TEs are expressed and therefore silenced by the resulting siRNA production. A final form of epigenetic control is modification of histones, which includes accumulation of the H3 variant HTR10 in mature sperm that is then completely replaced following fertilization. In females, the histone isoforms present in the EC and CCN differ, potentially helping to differentiate the two components during gametogenesis.

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          ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase.

          Zhizhong Gong, Teresa Morales-Ruiz, Rafael Ariza … (2002)
          Mutations in the Arabidopsis ROS1 locus cause transcriptional silencing of a transgene and a homologous endogenous gene. In the ros1 mutants, the promoter of the silenced loci is hypermethylated, which may be triggered by small RNAs produced from the transgene repeats. The transcriptional silencing in ros1 mutants can be released by the ddm1 mutation or the application of the DNA methylation inhibitor 5-aza-2'-deoxycytidine. ROS1 encodes an endonuclease III domain nuclear protein with bifunctional DNA glycosylase/lyase activity against methylated but not unmethylated DNA. The ros1 mutant shows enhanced sensitivity to genotoxic agents methyl methanesulfonate and hydrogen peroxide. We suggest that ROS1 is a DNA repair protein that represses homology-dependent transcriptional gene silencing by demethylating the target promoter DNA.
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            DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation.

            Mary Gehring, Jin Huh, Tzung-Fu Hsieh … (2006)
            MEDEA (MEA) is an Arabidopsis Polycomb group gene that is imprinted in the endosperm. The maternal allele is expressed and the paternal allele is silent. MEA is controlled by DEMETER (DME), a DNA glycosylase required to activate MEA expression, and METHYLTRANSFERASE I (MET1), which maintains CG methylation at the MEA locus. Here we show that DME is responsible for endosperm maternal-allele-specific hypomethylation at the MEA gene. DME can excise 5-methylcytosine in vitro and when expressed in E. coli. Abasic sites opposite 5-methylcytosine inhibit DME activity and might prevent DME from generating double-stranded DNA breaks. Unexpectedly, paternal-allele silencing is not controlled by DNA methylation. Rather, Polycomb group proteins that are expressed from the maternal genome, including MEA, control paternal MEA silencing. Thus, DME establishes MEA imprinting by removing 5-methylcytosine to activate the maternal allele. MEA imprinting is subsequently maintained in the endosperm by maternal MEA silencing the paternal allele.
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              Extensive demethylation of repetitive elements during seed development underlies gene imprinting.

              Mary Gehring, Kerry Bubb, Steven Henikoff (2009)
              DNA methylation is an epigenetic mark associated with transposable element silencing and gene imprinting in flowering plants and mammals. In plants, imprinting occurs in the endosperm, which nourishes the embryo during seed development. We have profiled Arabidopsis DNA methylation genome-wide in the embryo and endosperm and found that large-scale methylation changes accompany endosperm development and endosperm-specific gene expression. Transposable element fragments are extensively demethylated in the endosperm. We discovered new imprinted genes by the identification of candidates associated with regions of reduced endosperm methylation and preferential expression in endosperm relative to other parts of the plant. These data suggest that imprinting in plants evolved from targeted methylation of transposable element insertions near genic regulatory elements followed by positive selection when the resulting expression change was advantageous.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Front Plant Sci
                Journal ID (iso-abbrev): Front Plant Sci
                Journal ID (publisher-id): Front. Plant Sci.
                Title: Frontiers in plant science
                Publisher: Frontiers Research Foundation
                ISSN (Electronic): 1664-462X
                Publication date (Electronic): 06 February 2012
                Publication date Collection: 2012
                Volume: 3
                Electronic Location Identifier: 20
                Affiliations
                [1] 1simpleDepartment of Biological Sciences, University of Lethbridge Lethbridge, AB, Canada
                Author notes

                Edited by: Shawn Kaeppler, University of Wisconsin-Madison, USA

                Reviewed by: Nathan M. Springer, University of Minnesota, USA; Joseph F. Petolino, Dow AgroSciences, USA; Daphné Autran, Institut de Recherche pour le Développement, France

                *Correspondence: Igor Kovalchuk, University of Lethbridge, 4401 University Drive, Lethbridge, AB, Canada e-mail: igor.kovalchuk@ 123456uleth.ca

                This article was submitted to Frontiers in Plant Genetics and Genomics, a specialty of Frontiers in Plant Science.

                Article
                DOI: 10.3389/fpls.2012.00020
                PMC ID: 3355800
                PubMed ID: 22645573
                SO-VID: 2d4dd5c7-0ac7-471e-a974-972a43a2409d
                Copyright © Copyright © 2012 Migicovsky and Kovalchuk.
                License:

                This is an open-access article distributed under the terms of the Creative Commons Attribution Non Commercial License, which permits non-commercial use, distribution, and reproduction in other forums, provided the original authors and source are credited.

                History
                Date received : 08 October 2011
                Date accepted : 19 January 2012
                Page count
                Figures: 0, Tables: 3, Equations: 0, References: 72, Pages: 7, Words: 6496
                Categories
                Subject: Plant Science
                Subject: Review Article

                ScienceOpen disciplines: Plant science & Botany
                Keywords: transposon reactivation,epigenetic modifications,plant gametogenesis,histone modifications,dna methylation,genomic imprinting
                Data availability:
                ScienceOpen disciplines: Plant science & Botany
                Keywords: transposon reactivation, epigenetic modifications, plant gametogenesis, histone modifications, dna methylation, genomic imprinting

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