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      Taking the Wheel – de novo DNA Methylation as a Driving Force of Plant Embryonic Development

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          Abstract

          During plant embryogenesis, regardless of whether it begins with a fertilized egg cell (zygotic embryogenesis) or an induced somatic cell (somatic embryogenesis), significant epigenetic reprogramming occurs with the purpose of parental or vegetative transcript silencing and establishment of a next-generation epigenetic patterning. To ensure genome stability of a developing embryo, large-scale transposon silencing occurs by an RNA-directed DNA methylation (RdDM) pathway, which introduces methylation patterns de novo and as such potentially serves as a global mechanism of transcription control during developmental transitions. RdDM is controlled by a two-armed mechanism based around the activity of two RNA polymerases. While PolIV produces siRNAs accompanied by protein complexes comprising the methylation machinery, PolV produces lncRNA which guides the methylation machinery toward specific genomic locations. Recently, RdDM has been proposed as a dominant methylation mechanism during gamete formation and early embryo development in Arabidopsis thaliana, overshadowing all other methylation mechanisms. Here, we bring an overview of current knowledge about different roles of DNA methylation with emphasis on RdDM during plant zygotic and somatic embryogenesis. Based on published chromatin immunoprecipitation data on PolV binding sites within the A. thaliana genome, we uncover groups of auxin metabolism, reproductive development and embryogenesis-related genes, and discuss possible roles of RdDM at the onset of early embryonic development via targeted methylation at sites involved in different embryogenesis-related developmental mechanisms.

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          Most cited references144

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          Dynamics and function of DNA methylation in plants

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            Targeted mutation of the DNA methyltransferase gene results in embryonic lethality

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

              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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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                29 October 2021
                2021
                : 12
                : 764999
                Affiliations
                Division of Molecular Biology, Department of Biology, Faculty of Science, University of Zagreb , Zagreb, Croatia
                Author notes

                Edited by: Paloma Moncaleán, Neiker-Tecnalia, Spain

                Reviewed by: Markus Kuhlmann, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Germany; Célia M. Miguel, University of Lisbon, Portugal; Joseph Colasanti, University of Guelph, Canada

                *Correspondence: Dunja Leljak Levanić, dunja@ 123456zg.biol.pmf.hr

                These authors have contributed equally to this work and share first authorship

                This article was submitted to Plant Development and EvoDevo, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2021.764999
                8585777
                dbdf4de6-941f-4af8-8c7a-c3162333365d
                Copyright © 2021 Markulin, Škiljaica, Tokić, Jagić, Vuk, Bauer and Leljak Levanić.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 26 August 2021
                : 13 October 2021
                Page count
                Figures: 2, Tables: 2, Equations: 0, References: 144, Pages: 17, Words: 15579
                Funding
                Funded by: Hrvatska Zaklada za Znanost, doi 10.13039/501100004488;
                Categories
                Plant Science
                Review

                Plant science & Botany
                dna methylation,rddm,plant embryogenesis,zygotic embryogenesis,somatic embryogenesis,rna polymerase v,arabidopsis thaliana

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