DNA Topoisomerase 1α Promotes Transcriptional Silencing of Transposable Elements through DNA Methylation and Histone Lysine 9 Dimethylation in Arabidopsis

Autores
Dinh, Thanh Theresa; Gao, Lei; Liu, Xigang; Li, Dongming; Li, Shengben; Zhao, Yuanyuan; O'leary, Michael; Le, Brandon; Schmitz, Robert J.; Manavella, Pablo Andrés; Li, Shaofang; Weigel, Detlef; Pontes, Olga; Ecker, Joseph R.; Chen, Xuemei
Año de publicación
2014
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
RNA-directed DNA methylation (RdDM) and histone H3K9 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.
Fil: Dinh, Thanh Theresa. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology. ChemGen IGERT program; Estados Unidos
Fil: Gao, Lei. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos
Fil: Liu, Xigang . University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos
Fil: Li, Dongming. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos. Lanzhou University. School of Life Sciences Plant Biology Laboratory; China
Fil: Li, Shengben. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos
Fil: Zhao, Yuanyuan. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos
Fil: O'leary, Michael. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos
Fil: Le, Brandon. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos
Fil: Schmitz, Robert J.. The Salk Institute for Biological Studies. Plant Biology Laboratory; Estados Unidos
Fil: Manavella, Pablo Andrés. Max Planck Institute for Developmental Biology. Department of Molecular Biology; Alemania. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Santa Fe. Instituto de Agrobiotecnologia del Litoral; Argentina
Fil: Li, Shaofang. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos
Fil: Weigel, Detlef. Max Planck Institute for Developmental Biology. Department of Molecular Biology; Alemania
Fil: Pontes, Olga. University of New Mexico. Department of Biology; Estados Unidos
Fil: Ecker, Joseph R.. The Salk Institute for Biological Studies. Howard Hughes Medical Institute; Estados Unidos. The Salk Institute for Biological Studies. Plant Biology Laboratory; Estados Unidos
Fil: Chen, Xuemei. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos. University of California Riverside. Howard Hughes Medical Institute, ; Estados Unidos
Materia
Silenciamiento
Epigenetica
Metilación
Arabidopsis
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/14233
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/14233
network_acronym_str CONICETDig
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network_name_str CONICET Digital (CONICET)
spelling DNA Topoisomerase 1α Promotes Transcriptional Silencing of Transposable Elements through DNA Methylation and Histone Lysine 9 Dimethylation in ArabidopsisDinh, Thanh TheresaGao, LeiLiu, Xigang Li, DongmingLi, ShengbenZhao, YuanyuanO'leary, MichaelLe, BrandonSchmitz, Robert J.Manavella, Pablo AndrésLi, ShaofangWeigel, DetlefPontes, OlgaEcker, Joseph R.Chen, XuemeiSilenciamientoEpigeneticaMetilaciónArabidopsishttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1RNA-directed DNA methylation (RdDM) and histone H3K9 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.Fil: Dinh, Thanh Theresa. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology. ChemGen IGERT program; Estados UnidosFil: Gao, Lei. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados UnidosFil: Liu, Xigang . University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados UnidosFil: Li, Dongming. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos. Lanzhou University. School of Life Sciences Plant Biology Laboratory; ChinaFil: Li, Shengben. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados UnidosFil: Zhao, Yuanyuan. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados UnidosFil: O'leary, Michael. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados UnidosFil: Le, Brandon. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados UnidosFil: Schmitz, Robert J.. The Salk Institute for Biological Studies. Plant Biology Laboratory; Estados UnidosFil: Manavella, Pablo Andrés. Max Planck Institute for Developmental Biology. Department of Molecular Biology; Alemania. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Santa Fe. Instituto de Agrobiotecnologia del Litoral; ArgentinaFil: Li, Shaofang. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados UnidosFil: Weigel, Detlef. Max Planck Institute for Developmental Biology. Department of Molecular Biology; AlemaniaFil: Pontes, Olga. University of New Mexico. Department of Biology; Estados UnidosFil: Ecker, Joseph R.. The Salk Institute for Biological Studies. Howard Hughes Medical Institute; Estados Unidos. The Salk Institute for Biological Studies. Plant Biology Laboratory; Estados UnidosFil: Chen, Xuemei. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos. University of California Riverside. Howard Hughes Medical Institute, ; Estados UnidosPublic Library Of Science2014-05info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/14233Dinh, Thanh Theresa; Gao, Lei; Liu, Xigang ; Li, Dongming; Li, Shengben; et al.; DNA Topoisomerase 1α Promotes Transcriptional Silencing of Transposable Elements through DNA Methylation and Histone Lysine 9 Dimethylation in Arabidopsis; Public Library Of Science; Plos Genetics; 10; 7; 5-2014; e10044461553-73901553-7404enginfo:eu-repo/semantics/altIdentifier/doi/10.1371%2Fjournal.pgen.1004446info:eu-repo/semantics/altIdentifier/url/https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4080997/info:eu-repo/semantics/altIdentifier/url/http://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1004446info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:39:01Zoai:ri.conicet.gov.ar:11336/14233instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 10:39:02.002CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv DNA Topoisomerase 1α Promotes Transcriptional Silencing of Transposable Elements through DNA Methylation and Histone Lysine 9 Dimethylation in Arabidopsis
title DNA Topoisomerase 1α Promotes Transcriptional Silencing of Transposable Elements through DNA Methylation and Histone Lysine 9 Dimethylation in Arabidopsis
spellingShingle DNA Topoisomerase 1α Promotes Transcriptional Silencing of Transposable Elements through DNA Methylation and Histone Lysine 9 Dimethylation in Arabidopsis
Dinh, Thanh Theresa
Silenciamiento
Epigenetica
Metilación
Arabidopsis
title_short 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_sort DNA Topoisomerase 1α Promotes Transcriptional Silencing of Transposable Elements through DNA Methylation and Histone Lysine 9 Dimethylation in Arabidopsis
dc.creator.none.fl_str_mv Dinh, Thanh Theresa
Gao, Lei
Liu, Xigang
Li, Dongming
Li, Shengben
Zhao, Yuanyuan
O'leary, Michael
Le, Brandon
Schmitz, Robert J.
Manavella, Pablo Andrés
Li, Shaofang
Weigel, Detlef
Pontes, Olga
Ecker, Joseph R.
Chen, Xuemei
author Dinh, Thanh Theresa
author_facet Dinh, Thanh Theresa
Gao, Lei
Liu, Xigang
Li, Dongming
Li, Shengben
Zhao, Yuanyuan
O'leary, Michael
Le, Brandon
Schmitz, Robert J.
Manavella, Pablo Andrés
Li, Shaofang
Weigel, Detlef
Pontes, Olga
Ecker, Joseph R.
Chen, Xuemei
author_role author
author2 Gao, Lei
Liu, Xigang
Li, Dongming
Li, Shengben
Zhao, Yuanyuan
O'leary, Michael
Le, Brandon
Schmitz, Robert J.
Manavella, Pablo Andrés
Li, Shaofang
Weigel, Detlef
Pontes, Olga
Ecker, Joseph R.
Chen, Xuemei
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Silenciamiento
Epigenetica
Metilación
Arabidopsis
topic Silenciamiento
Epigenetica
Metilación
Arabidopsis
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv RNA-directed DNA methylation (RdDM) and histone H3K9 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.
Fil: Dinh, Thanh Theresa. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology. ChemGen IGERT program; Estados Unidos
Fil: Gao, Lei. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos
Fil: Liu, Xigang . University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos
Fil: Li, Dongming. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos. Lanzhou University. School of Life Sciences Plant Biology Laboratory; China
Fil: Li, Shengben. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos
Fil: Zhao, Yuanyuan. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos
Fil: O'leary, Michael. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos
Fil: Le, Brandon. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos
Fil: Schmitz, Robert J.. The Salk Institute for Biological Studies. Plant Biology Laboratory; Estados Unidos
Fil: Manavella, Pablo Andrés. Max Planck Institute for Developmental Biology. Department of Molecular Biology; Alemania. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Santa Fe. Instituto de Agrobiotecnologia del Litoral; Argentina
Fil: Li, Shaofang. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos
Fil: Weigel, Detlef. Max Planck Institute for Developmental Biology. Department of Molecular Biology; Alemania
Fil: Pontes, Olga. University of New Mexico. Department of Biology; Estados Unidos
Fil: Ecker, Joseph R.. The Salk Institute for Biological Studies. Howard Hughes Medical Institute; Estados Unidos. The Salk Institute for Biological Studies. Plant Biology Laboratory; Estados Unidos
Fil: Chen, Xuemei. University of California Riverside. Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences; Estados Unidos. University of California Riverside. Howard Hughes Medical Institute, ; Estados Unidos
description RNA-directed DNA methylation (RdDM) and histone H3K9 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.
publishDate 2014
dc.date.none.fl_str_mv 2014-05
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/14233
Dinh, Thanh Theresa; Gao, Lei; Liu, Xigang ; Li, Dongming; Li, Shengben; et al.; DNA Topoisomerase 1α Promotes Transcriptional Silencing of Transposable Elements through DNA Methylation and Histone Lysine 9 Dimethylation in Arabidopsis; Public Library Of Science; Plos Genetics; 10; 7; 5-2014; e1004446
1553-7390
1553-7404
url http://hdl.handle.net/11336/14233
identifier_str_mv Dinh, Thanh Theresa; Gao, Lei; Liu, Xigang ; Li, Dongming; Li, Shengben; et al.; DNA Topoisomerase 1α Promotes Transcriptional Silencing of Transposable Elements through DNA Methylation and Histone Lysine 9 Dimethylation in Arabidopsis; Public Library Of Science; Plos Genetics; 10; 7; 5-2014; e1004446
1553-7390
1553-7404
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1371%2Fjournal.pgen.1004446
info:eu-repo/semantics/altIdentifier/url/https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4080997/
info:eu-repo/semantics/altIdentifier/url/http://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1004446
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Public Library Of Science
publisher.none.fl_str_mv Public Library Of Science
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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