title: The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin.
abstract: Nucleosome remodelers of the DDM1/Lsh family are required for DNA methylation of transposable elements, but the reason for this is unknown. How DDM1 interacts with other methylation pathways, such as small-RNA-directed DNA methylation (RdDM), which is thought to mediate plant asymmetric methylation through DRM enzymes, is also unclear. Here, we show that most asymmetric methylation is facilitated by DDM1 and mediated by the methyltransferase CMT2 separately from RdDM. We find that heterochromatic sequences preferentially require DDM1 for DNA methylation and that this preference depends on linker histone H1. RdDM is instead inhibited by heterochromatin and absolutely requires the nucleosome remodeler DRD1. Together, DDM1 and RdDM mediate nearly all transposon methylation and collaborate to repress transposition and regulate the methylation and expression of genes. Our results indicate that DDM1 provides DNA methyltransferases access to H1-containing heterochromatin to allow stable silencing of transposable elements in cooperation with the RdDM pathway.
authors.affiliation: Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA 94720, USA.
authors.forename: Assaf
authors.initials: A
authors.lastname: Zemach
authors.forename: M Yvonne
authors.initials: MY
authors.lastname: Kim
authors.forename: Ping-Hung
authors.initials: PH
authors.lastname: Hsieh
authors.forename: Devin
authors.initials: D
authors.lastname: Coleman-Derr
authors.forename: Leor
authors.initials: L
authors.lastname: Eshed-Williams
authors.forename: Ka
authors.initials: K
authors.lastname: Thao
authors.forename: Stacey L
authors.initials: SL
authors.lastname: Harmer
authors.forename: Daniel
authors.initials: D
authors.lastname: Zilberman
mesh_terms: D017360:Arabidopsis / Q000201:enzymology / Q000235:genetics / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000378:metabolism*; D004248:DNA (Cytosine-5-)-Methyltransferases / Q000378:metabolism; D019175:DNA Methylation; D004251:DNA Transposable Elements; D004268:DNA-Binding Proteins / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant; D006570:Heterochromatin; D006657:Histones / Q000378:metabolism*; D009707:Nucleosomes / Q000378:metabolism; D014157:Transcription Factors / Q000378:metabolism*
chemical_list: D029681:Arabidopsis Proteins; C118957:DDM1 protein, Arabidopsis; D004251:DNA Transposable Elements; D004268:DNA-Binding Proteins; D006570:Heterochromatin; D006657:Histones; D009707:Nucleosomes; D014157:Transcription Factors; D004248:DNA (Cytosine-5-)-Methyltransferases; C112810:chromomethylase
references.citation: Nat Genet. 2003 Nov;35(3):213-4
references.pmid: 14593407
references.citation: Nat Rev Mol Cell Biol. 2011 Jul 22;12(8):483-92
references.pmid: 21779025
references.citation: PLoS One. 2008 Sep 08;3(9):e3156
references.pmid: 18776934
references.citation: Curr Opin Chem Biol. 2011 Oct;15(5):649-56
references.pmid: 21862382
references.citation: Plant J. 2012 Sep;71(5):776-86
references.pmid: 22519754
references.citation: Genomics. 2008 May;91(5):467-75
references.pmid: 18343092
references.citation: Cell. 2005 Dec 29;123(7):1199-212
references.pmid: 16377562
references.citation: Nature. 2009 Sep 17;461(7262):423-6
references.pmid: 19734880
references.citation: Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10275-9
references.pmid: 7937940
references.citation: Science. 2012 Jun 15;336(6087):1445-8
references.pmid: 22700931
references.citation: Nat Rev Genet. 2010 Mar;11(3):204-20
references.pmid: 20142834
references.citation: Chromosoma. 1999 Nov;108(6):345-55
references.pmid: 10591994
references.citation: Genes Dev. 2008 Jun 15;22(12):1597-606
references.pmid: 18559476
references.citation: Curr Opin Plant Biol. 2011 Feb;14(1):81-7
references.pmid: 20869294
references.citation: Nat Struct Mol Biol. 2012 Sep;19(9):870-5
references.pmid: 22864289
references.citation: Science. 2012 Sep 14;337(6100):1360-1364
references.pmid: 22984074
references.citation: Proc Natl Acad Sci U S A. 2011 Apr 5;108(14):5626-31
references.pmid: 21427231
references.citation: PLoS Genet. 2012;8(10):e1002988
references.pmid: 23071449
references.citation: EMBO Rep. 2009 Sep;10(9):1015-21
references.pmid: 19680290
references.citation: Nat Genet. 1999 May;22(1):94-7
references.pmid: 10319870
references.citation: Cell. 2008 May 2;133(3):523-36
references.pmid: 18423832
references.citation: PLoS Genet. 2012;8(3):e1002512
references.pmid: 22457632
references.citation: Cell. 2012 Sep 28;151(1):167-80
references.pmid: 23021223
references.citation: Biochem Cell Biol. 2009 Feb;87(1):189-206
references.pmid: 19234534
references.citation: Nature. 2004 Jul 22;430(6998):471-6
references.pmid: 15269773
references.citation: EMBO J. 2012 Jun 29;31(13):2981-93
references.pmid: 22580822
references.citation: Epigenetics. 2012 Jul;7(7):781-95
references.pmid: 22647529
references.citation: EMBO J. 2011 May 18;30(10):1928-38
references.pmid: 21487388
references.citation: Trends Cell Biol. 2012 May;22(5):250-6
references.pmid: 22421062
references.citation: Proc Natl Acad Sci U S A. 2011 Feb 1;108(5):1755-62
references.pmid: 21257907
references.citation: Plant Cell. 2004 Apr;16(4):1021-34
references.pmid: 15037732
references.citation: Bioinformatics. 2010 Jan 1;26(1):139-40
references.pmid: 19910308
references.citation: Nature. 2008 Mar 13;452(7184):215-9
references.pmid: 18278030
references.citation: Mol Cell Biol. 2000 Jan;20(1):61-9
references.pmid: 10594009
references.citation: J Biol Chem. 2003 Jan 10;278(2):823-8
references.pmid: 12403775
references.citation: Nature. 2009 Sep 17;461(7262):427-30
references.pmid: 19734882
references.citation: BMC Plant Biol. 2012 Apr 19;12:51
references.pmid: 22512782
references.citation: Nat Rev Genet. 2007 Jan;8(1):35-46
references.pmid: 17173056
references.citation: Nucleic Acids Res. 2011 Sep 1;39(16):6919-31
references.pmid: 21586580
references.citation: Science. 2010 May 14;328(5980):916-9
references.pmid: 20395474
references.citation: Genes Dev. 2012 Aug 15;26(16):1825-36
references.pmid: 22855789
references.citation: Nature. 2008 Nov 6;456(7218):125-9
references.pmid: 18815594
references.citation: PLoS Biol. 2004 May;2(5):E104
references.pmid: 15024409
references.citation: Dev Cell. 2003 Dec;5(6):891-901
references.pmid: 14667411
references.citation: Curr Biol. 2004 May 4;14(9):801-5
references.pmid: 15120073
references.citation: Curr Biol. 2012 Oct 9;22(19):1825-30
references.pmid: 22940470
references.citation: PLoS One. 2009 Jun 16;4(6):e5932
references.pmid: 19529764
references.citation: Science. 2009 Mar 20;323(5921):1600-4
references.pmid: 19179494
references.citation: Curr Opin Cell Biol. 1999 Jun;11(3):312-7
references.pmid: 10395563
references.citation: EMBO J. 2007 Aug 8;26(15):3641-52
references.pmid: 17627280
references.citation: Genetics. 2005 Feb;169(2):997-1008
references.pmid: 15489532
references.citation: Curr Biol. 2010 May 25;20(10):951-6
references.pmid: 20409711
references.citation: Curr Opin Struct Biol. 2006 Jun;16(3):336-43
references.pmid: 16714106
references.citation: Proc Natl Acad Sci U S A. 2010 Oct 26;107(43):18729-34
references.pmid: 20937895
references.citation: Science. 2012 Jun 15;336(6087):1448-51
references.pmid: 22555433
references.citation: EMBO J. 2009 Apr 22;28(8):1078-86
references.pmid: 19262562