DNA topoisomerase 1α promotes transcriptional silencing of transposable elements through DNA methylation and histone lysine 9 dimethylation in Arabidopsis.

RNA-directed DNA methylation (RdDM) and histone H3 lysine 9 dimethylation (H3K9me2) are related transcriptional silencing mechanisms that target transposable elements (TEs) and repeats to maintain genome stability in plants. RdDM is mediated by small and long noncoding RNAs produced by the plant-spe...

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Main Authors: Thanh Theresa Dinh, Lei Gao, Xigang Liu, Dongming Li, Shengben Li, Yuanyuan Zhao, Michael O'Leary, Brandon Le, Robert J Schmitz, Pablo A Manavella, Shaofang Li, Detlef Weigel, Olga Pontes, Joseph R Ecker, Xuemei Chen
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-07-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC4080997?pdf=render
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author Thanh Theresa Dinh
Lei Gao
Xigang Liu
Dongming Li
Shengben Li
Yuanyuan Zhao
Michael O'Leary
Brandon Le
Robert J Schmitz
Pablo A Manavella
Shaofang Li
Detlef Weigel
Olga Pontes
Joseph R Ecker
Xuemei Chen
author_facet Thanh Theresa Dinh
Lei Gao
Xigang Liu
Dongming Li
Shengben Li
Yuanyuan Zhao
Michael O'Leary
Brandon Le
Robert J Schmitz
Pablo A Manavella
Shaofang Li
Detlef Weigel
Olga Pontes
Joseph R Ecker
Xuemei Chen
author_sort Thanh Theresa Dinh
collection DOAJ
description RNA-directed DNA methylation (RdDM) and histone H3 lysine 9 dimethylation (H3K9me2) are related transcriptional silencing mechanisms that target transposable elements (TEs) and repeats to maintain genome stability in plants. RdDM is mediated by small and long noncoding RNAs produced by the plant-specific RNA polymerases Pol IV and Pol V, respectively. Through a chemical genetics screen with a luciferase-based DNA methylation reporter, LUCL, we found that camptothecin, a compound with anti-cancer properties that targets DNA topoisomerase 1α (TOP1α) was able to de-repress LUCL by reducing its DNA methylation and H3K9me2 levels. Further studies with Arabidopsis top1α mutants showed that TOP1α silences endogenous RdDM loci by facilitating the production of Pol V-dependent long non-coding RNAs, AGONAUTE4 recruitment and H3K9me2 deposition at TEs and repeats. This study assigned a new role in epigenetic silencing to an enzyme that affects DNA topology.
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spelling doaj.art-4caa2cf0d62b4b0db8ecd94b4b82be112022-12-21T18:53:40ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042014-07-01107e100444610.1371/journal.pgen.1004446DNA topoisomerase 1α promotes transcriptional silencing of transposable elements through DNA methylation and histone lysine 9 dimethylation in Arabidopsis.Thanh Theresa DinhLei GaoXigang LiuDongming LiShengben LiYuanyuan ZhaoMichael O'LearyBrandon LeRobert J SchmitzPablo A ManavellaShaofang LiDetlef WeigelOlga PontesJoseph R EckerXuemei ChenRNA-directed DNA methylation (RdDM) and histone H3 lysine 9 dimethylation (H3K9me2) are related transcriptional silencing mechanisms that target transposable elements (TEs) and repeats to maintain genome stability in plants. RdDM is mediated by small and long noncoding RNAs produced by the plant-specific RNA polymerases Pol IV and Pol V, respectively. Through a chemical genetics screen with a luciferase-based DNA methylation reporter, LUCL, we found that camptothecin, a compound with anti-cancer properties that targets DNA topoisomerase 1α (TOP1α) was able to de-repress LUCL by reducing its DNA methylation and H3K9me2 levels. Further studies with Arabidopsis top1α mutants showed that TOP1α silences endogenous RdDM loci by facilitating the production of Pol V-dependent long non-coding RNAs, AGONAUTE4 recruitment and H3K9me2 deposition at TEs and repeats. This study assigned a new role in epigenetic silencing to an enzyme that affects DNA topology.http://europepmc.org/articles/PMC4080997?pdf=render
spellingShingle Thanh Theresa Dinh
Lei Gao
Xigang Liu
Dongming Li
Shengben Li
Yuanyuan Zhao
Michael O'Leary
Brandon Le
Robert J Schmitz
Pablo A Manavella
Shaofang Li
Detlef Weigel
Olga Pontes
Joseph R Ecker
Xuemei Chen
DNA topoisomerase 1α promotes transcriptional silencing of transposable elements through DNA methylation and histone lysine 9 dimethylation in Arabidopsis.
PLoS Genetics
title DNA topoisomerase 1α promotes transcriptional silencing of transposable elements through DNA methylation and histone lysine 9 dimethylation in Arabidopsis.
title_full DNA topoisomerase 1α promotes transcriptional silencing of transposable elements through DNA methylation and histone lysine 9 dimethylation in Arabidopsis.
title_fullStr DNA topoisomerase 1α promotes transcriptional silencing of transposable elements through DNA methylation and histone lysine 9 dimethylation in Arabidopsis.
title_full_unstemmed DNA topoisomerase 1α promotes transcriptional silencing of transposable elements through DNA methylation and histone lysine 9 dimethylation in Arabidopsis.
title_short DNA topoisomerase 1α promotes transcriptional silencing of transposable elements through DNA methylation and histone lysine 9 dimethylation in Arabidopsis.
title_sort dna topoisomerase 1α promotes transcriptional silencing of transposable elements through dna methylation and histone lysine 9 dimethylation in arabidopsis
url http://europepmc.org/articles/PMC4080997?pdf=render
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