Co-targeting RNA Polymerases IV and V Promotes Efficient De Novo DNA Methylation in Arabidopsis

The RNA-directed DNA methylation (RdDM) pathway in plants controls gene expression via cytosine DNA methylation. The ability to manipulate RdDM would shed light on the mechanisms and applications of DNA methylation to control gene expression. Here, we identified diverse RdDM proteins that are capabl...

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Published in	Cell Vol. 176; no. 5; pp. 1068 - 1082.e19
Main Authors	Gallego-Bartolomé, Javier, Liu, Wanlu, Kuo, Peggy Hsuanyu, Feng, Suhua, Ghoshal, Basudev, Gardiner, Jason, Zhao, Jenny Miao-Chi, Park, Soo Young, Chory, Joanne, Jacobsen, Steven E.
Format	Journal Article
Language	English
Published	United States Elsevier Inc 21.02.2019 Cell Press
Subjects	Arabidopsis Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism biogenesis cytosine Cytosine - metabolism DNA - metabolism DNA methylation DNA Methylation - genetics DNA Methylation - physiology DNA-directed RNA polymerase DNA-Directed RNA Polymerases - genetics DNA-Directed RNA Polymerases - metabolism epigenetics gene expression Gene Expression Regulation, Plant - genetics genes mutants proteins RNA Polymerase II - metabolism RNA, Plant - genetics RNA, Small Interfering - metabolism small interfering RNA zinc finger motif
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Abstract	The RNA-directed DNA methylation (RdDM) pathway in plants controls gene expression via cytosine DNA methylation. The ability to manipulate RdDM would shed light on the mechanisms and applications of DNA methylation to control gene expression. Here, we identified diverse RdDM proteins that are capable of targeting methylation and silencing in Arabidopsis when tethered to an artificial zinc finger (ZF-RdDM). We studied their order of action within the RdDM pathway by testing their ability to target methylation in different mutants. We also evaluated ectopic siRNA biogenesis, RNA polymerase V (Pol V) recruitment, targeted DNA methylation, and gene-expression changes at thousands of ZF-RdDM targets. We found that co-targeting both arms of the RdDM pathway, siRNA biogenesis and Pol V recruitment, dramatically enhanced targeted methylation. This work defines how RdDM components establish DNA methylation and enables new strategies for epigenetic gene regulation via targeted DNA methylation. [Display omitted] •A panel of RdDM factors can target DNA methylation when fused to an artificial ZF•ZF-RdDM fusions in different mutant backgrounds reveal RdDM hierarchy of action•MORC6 can target DNA methylation•Co-targeting of Pol IV and Pol V synergistically enhances DNA methylation targeting Comprehensive investigation into the genetic pathway of RNA-directed DNA methylation in Arabidopsis defines epistatic relationships and allows for efficient manipulation of DNA methylation to specifically modify developmental phenotypes.
AbstractList	The RNA-directed DNA methylation (RdDM) pathway in plants controls gene expression via cytosine DNA methylation. The ability to manipulate RdDM would shed light on the mechanisms and applications of DNA methylation to control gene expression. Here, we identified diverse RdDM proteins that are capable of targeting methylation and silencing in Arabidopsis when tethered to an artificial zinc finger (ZF-RdDM). We studied their order of action within the RdDM pathway by testing their ability to target methylation in different mutants. We also evaluated ectopic siRNA biogenesis, RNA polymerase V (Pol V) recruitment, targeted DNA methylation, and gene-expression changes at thousands of ZF-RdDM targets. We found that co-targeting both arms of the RdDM pathway, siRNA biogenesis and Pol V recruitment, dramatically enhanced targeted methylation. This work defines how RdDM components establish DNA methylation and enables new strategies for epigenetic gene regulation via targeted DNA methylation. The RNA-directed DNA methylation (RdDM) pathway in plants controls gene expression via cytosine DNA methylation. The ability to manipulate RdDM would shed light on the mechanisms and applications of DNA methylation to control gene expression. Here, we identified diverse RdDM proteins that are capable of targeting methylation and silencing in Arabidopsis when tethered to an artificial zinc finger (ZF-RdDM). We studied their order of action within the RdDM pathway by testing their ability to target methylation in different mutants. We also evaluated ectopic siRNA biogenesis, RNA polymerase V (Pol V) recruitment, targeted DNA methylation, and gene-expression changes at thousands of ZF-RdDM targets. We found that co-targeting both arms of the RdDM pathway, siRNA biogenesis and Pol V recruitment, dramatically enhanced targeted methylation. This work defines how RdDM components establish DNA methylation and enables new strategies for epigenetic gene regulation via targeted DNA methylation. • A panel of RdDM factors can target DNA methylation when fused to an artificial ZF • ZF-RdDM fusions in different mutant backgrounds reveal RdDM hierarchy of action • MORC6 can target DNA methylation • Co-targeting of Pol IV and Pol V synergistically enhances DNA methylation targeting Comprehensive investigation into the genetic pathway of RNA-directed DNA methylation in Arabidopsis defines epistatic relationships and allows for efficient manipulation of DNA methylation to specifically modify developmental phenotypes. The RNA-directed DNA methylation (RdDM) pathway in plants controls gene expression via cytosine DNA methylation. The ability to manipulate RdDM would shed light on the mechanisms and applications of DNA methylation to control gene expression. Here, we identified diverse RdDM proteins that are capable of targeting methylation and silencing in Arabidopsis when tethered to an artificial zinc finger (ZF-RdDM). We studied their order of action within the RdDM pathway by testing their ability to target methylation in different mutants. We also evaluated ectopic siRNA biogenesis, RNA polymerase V (Pol V) recruitment, targeted DNA methylation, and gene-expression changes at thousands of ZF-RdDM targets. We found that co-targeting both arms of the RdDM pathway, siRNA biogenesis and Pol V recruitment, dramatically enhanced targeted methylation. This work defines how RdDM components establish DNA methylation and enables new strategies for epigenetic gene regulation via targeted DNA methylation. [Display omitted] •A panel of RdDM factors can target DNA methylation when fused to an artificial ZF•ZF-RdDM fusions in different mutant backgrounds reveal RdDM hierarchy of action•MORC6 can target DNA methylation•Co-targeting of Pol IV and Pol V synergistically enhances DNA methylation targeting Comprehensive investigation into the genetic pathway of RNA-directed DNA methylation in Arabidopsis defines epistatic relationships and allows for efficient manipulation of DNA methylation to specifically modify developmental phenotypes. The RNA-directed DNA methylation (RdDM) pathway in plants controls gene expression via cytosine DNA methylation. The ability to manipulate RdDM would shed light on the mechanisms and applications of DNA methylation to control gene expression. Here, we identified diverse RdDM proteins that are capable of targeting methylation and silencing in Arabidopsis when tethered to an artificial zinc finger (ZF-RdDM). We studied their order of action within the RdDM pathway by testing their ability to target methylation in different mutants. We also evaluated ectopic siRNA biogenesis, RNA polymerase V (Pol V) recruitment, targeted DNA methylation, and gene-expression changes at thousands of ZF-RdDM targets. We found that co-targeting both arms of the RdDM pathway, siRNA biogenesis and Pol V recruitment, dramatically enhanced targeted methylation. This work defines how RdDM components establish DNA methylation and enables new strategies for epigenetic gene regulation via targeted DNA methylation.The RNA-directed DNA methylation (RdDM) pathway in plants controls gene expression via cytosine DNA methylation. The ability to manipulate RdDM would shed light on the mechanisms and applications of DNA methylation to control gene expression. Here, we identified diverse RdDM proteins that are capable of targeting methylation and silencing in Arabidopsis when tethered to an artificial zinc finger (ZF-RdDM). We studied their order of action within the RdDM pathway by testing their ability to target methylation in different mutants. We also evaluated ectopic siRNA biogenesis, RNA polymerase V (Pol V) recruitment, targeted DNA methylation, and gene-expression changes at thousands of ZF-RdDM targets. We found that co-targeting both arms of the RdDM pathway, siRNA biogenesis and Pol V recruitment, dramatically enhanced targeted methylation. This work defines how RdDM components establish DNA methylation and enables new strategies for epigenetic gene regulation via targeted DNA methylation.
Author	Park, Soo Young Gallego-Bartolomé, Javier Ghoshal, Basudev Zhao, Jenny Miao-Chi Gardiner, Jason Chory, Joanne Jacobsen, Steven E. Liu, Wanlu Feng, Suhua Kuo, Peggy Hsuanyu
AuthorAffiliation	1 Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, CA 90095, USA 2 Eli & Edythe Broad Center of Regenerative Medicine & Stem Cell Research, University of California at Los Angeles, Los Angeles, CA 90095, USA 5 Howard Hughes Medical Institute, University of California at Los Angeles, Los Angeles, CA 90095, USA 3 Howard Hughes Medical Institute, La Jolla, CA 92037, USA 4 The Salk Institute, La Jolla, CA 92037, USA
AuthorAffiliation_xml	– name: 5 Howard Hughes Medical Institute, University of California at Los Angeles, Los Angeles, CA 90095, USA – name: 3 Howard Hughes Medical Institute, La Jolla, CA 92037, USA – name: 4 The Salk Institute, La Jolla, CA 92037, USA – name: 1 Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, CA 90095, USA – name: 2 Eli & Edythe Broad Center of Regenerative Medicine & Stem Cell Research, University of California at Los Angeles, Los Angeles, CA 90095, USA
Author_xml	– sequence: 1 givenname: Javier surname: Gallego-Bartolomé fullname: Gallego-Bartolomé, Javier organization: Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, CA 90095, USA – sequence: 2 givenname: Wanlu surname: Liu fullname: Liu, Wanlu organization: Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, CA 90095, USA – sequence: 3 givenname: Peggy Hsuanyu surname: Kuo fullname: Kuo, Peggy Hsuanyu organization: Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, CA 90095, USA – sequence: 4 givenname: Suhua surname: Feng fullname: Feng, Suhua organization: Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, CA 90095, USA – sequence: 5 givenname: Basudev surname: Ghoshal fullname: Ghoshal, Basudev organization: Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, CA 90095, USA – sequence: 6 givenname: Jason surname: Gardiner fullname: Gardiner, Jason organization: Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, CA 90095, USA – sequence: 7 givenname: Jenny Miao-Chi surname: Zhao fullname: Zhao, Jenny Miao-Chi organization: Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, CA 90095, USA – sequence: 8 givenname: Soo Young surname: Park fullname: Park, Soo Young organization: Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, CA 90095, USA – sequence: 9 givenname: Joanne surname: Chory fullname: Chory, Joanne organization: Howard Hughes Medical Institute, La Jolla, CA 92037, USA – sequence: 10 givenname: Steven E. surname: Jacobsen fullname: Jacobsen, Steven E. email: jacobsen@ucla.edu organization: Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, CA 90095, USA
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Copyright	2019 The Author(s) Copyright © 2019 The Author(s). Published by Elsevier Inc. All rights reserved. 2019 The Author(s) 2019
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Snippet	The RNA-directed DNA methylation (RdDM) pathway in plants controls gene expression via cytosine DNA methylation. The ability to manipulate RdDM would shed...
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SubjectTerms	Arabidopsis Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism biogenesis cytosine Cytosine - metabolism DNA - metabolism DNA methylation DNA Methylation - genetics DNA Methylation - physiology DNA-directed RNA polymerase DNA-Directed RNA Polymerases - genetics DNA-Directed RNA Polymerases - metabolism epigenetics gene expression Gene Expression Regulation, Plant - genetics genes mutants proteins RNA Polymerase II - metabolism RNA, Plant - genetics RNA, Small Interfering - metabolism small interfering RNA zinc finger motif
Title	Co-targeting RNA Polymerases IV and V Promotes Efficient De Novo DNA Methylation in Arabidopsis
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