IDN2 and Its Paralogs Form a Complex Required for RNA–Directed DNA Methylation
IDN2/RDM12 has been previously identified as a component of the RNA–directed DNA methylation (RdDM) machinery in Arabidopsis thaliana, but how it functions in RdDM remains unknown. By affinity purification of IDN2, we co-purified two IDN2 paralogs IDP1 and IDP2 (IDN2 PARALOG 1 and 2). The coiled-coil domain between the XS and XH domains of IDN2 is essential for IDN2 homodimerization, whereas the IDN2 C-terminal XH domain but not the coiled-coil domain is required for IDN2 interaction with IDP1 and IDP2. By introducing the wild-type IDN2 sequence and its mutated derivatives into the idn2 mutant for complementation testing, we demonstrated that the previously uncharacterized IDN2 XH domain is required for the IDN2-IDP1/IDP2 complex formation as well as for IDN2 function. IDP1 is required for de novo DNA methylation, siRNA accumulation, and transcriptional gene silencing, whereas IDP2 has partially overlapping roles with IDP1. Unlike IDN2, IDP1 and IDP2 are incapable of binding double-stranded RNA, suggesting that the roles of IDP1 and IDP2 are different from those of IDN2 in the IDN2-IDP1/IDP2 complex and that IDP1 and IDP2 are essential for the functioning of the complex in RdDM.
Vyšlo v časopise:
IDN2 and Its Paralogs Form a Complex Required for RNA–Directed DNA Methylation. PLoS Genet 8(5): e32767. doi:10.1371/journal.pgen.1002693
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002693
Souhrn
IDN2/RDM12 has been previously identified as a component of the RNA–directed DNA methylation (RdDM) machinery in Arabidopsis thaliana, but how it functions in RdDM remains unknown. By affinity purification of IDN2, we co-purified two IDN2 paralogs IDP1 and IDP2 (IDN2 PARALOG 1 and 2). The coiled-coil domain between the XS and XH domains of IDN2 is essential for IDN2 homodimerization, whereas the IDN2 C-terminal XH domain but not the coiled-coil domain is required for IDN2 interaction with IDP1 and IDP2. By introducing the wild-type IDN2 sequence and its mutated derivatives into the idn2 mutant for complementation testing, we demonstrated that the previously uncharacterized IDN2 XH domain is required for the IDN2-IDP1/IDP2 complex formation as well as for IDN2 function. IDP1 is required for de novo DNA methylation, siRNA accumulation, and transcriptional gene silencing, whereas IDP2 has partially overlapping roles with IDP1. Unlike IDN2, IDP1 and IDP2 are incapable of binding double-stranded RNA, suggesting that the roles of IDP1 and IDP2 are different from those of IDN2 in the IDN2-IDP1/IDP2 complex and that IDP1 and IDP2 are essential for the functioning of the complex in RdDM.
Zdroje
1. LawJAJacobsenSE 2010 Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature Rev Genet 11 204 220
2. ZhangXYazakiJSundaresanACokusSChanSW 2006 Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126 1189 1201
3. MatzkeMKannoTDaxingerLHuettelBMatzkeAJ 2009 RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol 21 367 376
4. RonemusMJGalbiatiMTicknorCChenJDellaportaSL 1996 Demethylation-induced developmental pleiotropy in Arabidopsis. Science 273 654 657
5. BarteeLMalagnacFBenderJ 2001 Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene. Genes Dev 15 1753 1758
6. LindrothAMCaoXJacksonJPZilbermanDMcCallumCM 2001 Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292 2077 2080
7. JeddelohJAStokesTLRichardsEJ 1999 Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat Genet 22 94 97
8. JacksonJPLindrothAMCaoXJacobsenSE 2002 Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416 556 560
9. JohnsonLMBostickMZhangXKraftEHendersonI 2007 The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr Biol 17 379 384
10. XieZJohansenLKGustafsonAMKasschauKDLellisAD 2004 Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2 e104 doi:10.1371/journal.pbio.0020104
11. HerrAJJensenMBDalmayTBaulcombeDC 2005 RNA polymerase IV directs silencing of endogenous DNA. Science 308 118 120
12. ZaratieguiMIrvineDVMartienssenRA 2007 Noncoding RNAs and gene silencing. Cell 128 763 776
13. CaoXJacobsenSE 2002 Role of the arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12 1138 1144
14. PontesOLiCFNunesPCHaagJReamT 2006 The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell 126 79 92
15. GreenbergMVAusinIChanSWCokusSJCuperusJT 2011 Identification of genes required for de novo DNA methylation in Arabidopsis. Epigenetics 6 344 354
16. NaumannUDaxingerLKannoTEunCLongQ 2011 Genetic evidence that DNA methyltransferase DRM2 has a direct catalytic role in RNA-directed DNA methylation in Arabidopsis thaliana. Genetics 187 977 979
17. HendersonIRDelerisAWongWZhongXChinHG 2010 The de novo cytosine methyltransferase DRM2 requires intact UBA domains and a catalytically mutated paralog DRM3 during RNA-directed DNA methylation in Arabidopsis thaliana. PLoS Genet 6 e1001182 doi:10.1371/journal.pgen.1001182
18. HamiltonAVoinnetOChappellLBaulcombeD 2002 Two classes of short interfering RNA in RNA silencing. EMBO J 21 4671 4679
19. WierzbickiATHaagJRPikaardCS 2008 Non-coding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135 635 648
20. PontierDYahubyanGVegaDBulskiASaez-VasquezJ 2005 Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis. Genes Dev 19 2030 2040
21. KannoTHuettelBMetteMFAufsatzWJaligotE 2005 Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nat Genet 37 761 765
22. ReamTSHaagJRWierzbickiATNicoraCDNorbeckA 2009 Subunit Compositions of the RNA-Silencing Enzymes Pol IV and Pol V Reveal Their Origins as Specialized Forms of RNA Polymerase II. Mol Cell 33 192 203
23. HuangLJonesAMSearleIPatelKVoglerH 2009 An atypical RNA polymerase involved in RNA silencing shares small subunits with RNA polymerase II. Nat Struct Mol Biol 16 91 93
24. HaagJRPikaardCS 2011 Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing. Nat Rev Mol Cell Biol 12 483 492
25. ZhengBWangZLiSYuBLiuJY 2009 Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev 23 2850 2860
26. YangZEbrightYWYuBChenX 2006 HEN1 recognizes 21–24 nt small RNA duplexes and deposits a methyl group onto the 2′ OH of the 3′ terminal nucleotide. Nucleic Acids Res 34 667 675
27. ZilbermanDCaoXJacobsenSE 2003 ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 2003; 299 716 719
28. LiCFPontesOEl-ShamiMHendersonIRBernatavichuteYV 2006 An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell 126 93 106
29. QiYHeXWangXJKohanyOJurkaJ 2006 Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature 443 1008 1012
30. ZhengXZhuJKapoorAZhuJK 2007 Role of Arabidopsis AGO6 in siRNA accumulation, DNA methylation and transcriptional gene silencing. EMBO J 26 1691 1701
31. HaveckerERWallbridgeLMHardcastleTJBushMSKellyKA 2010 The Arabidopsis RNA-directed DNA methylation argonautes functionally diverge based on their expression and interaction with target loci. Plant Cell 22 321 334
32. El-ShamiMPontierDLahmySBraunLPicartC 2007 Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes Dev 21 2539 2544
33. HeXJHsuYFZhuSWierzbickiATPontesO 2009 An effector of RNA-directed DNA methylation in arabidopsis is an ARGONAUTE 4- and RNA-binding protein. Cell 137 498 508
34. Bies-EtheveNPontierDLahmySPicartCVegaD 2009 RNA-directed DNA methylation requires an AGO4-interacting member of the SPT5 elongation factor family. EMBO Rep 10 649 654
35. RowleyMJAvrutskyMISifuentesCJPereiraLWierzbickiAT 2011 Independent chromatin binding of ARGONAUTE4 and SPT5L/KTF1 mediates transcriptional gene silencing. PLoS Genet 7 e1002120 doi:10.1371/journal.pgen.1002120
36. KannoTMetteMFKreilDPAufsatzWMatzkeMMatzkeAJ 2004 Involvement of putative SNF2 chromatin remodeling protein DRD1 in RNA-directed DNA methylation. Curr Biol 14 801 805
37. KannoTBucherEDaxingerLHuettelBBöhmdorferG 2008 A structural-maintenance-of-chromosomes hinge domain-containing protein is required for RNA-directed DNA methylation. Nat Genet 40 670 675
38. GaoZLiuHLDaxingerLPontesOHeX 2010 An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation. Nature 465 106 109
39. LawJAAusinIJohnsonLMVashishtAAZhuJK 2010 A protein complex required for polymerase V transcripts and RNA-directed DNA methylation in Arabidopsis. Curr Biol 20 951 956
40. HeXJHsuYFZhuSLiuHLPontesO 2009 A conserved transcriptional regulator is required for RNA-directed DNA methylation and plant development. Genes Dev 23 2717 2722
41. KannoTBucherEDaxingerLHuettelBKreilDP 2010 RNA-directed DNA methylation and plant development require an IWR1-type transcription factor. EMBO Rep 11 65 71
42. LawJAVashishtAAWohlschlegelJAJacobsenSE 2011 SHH1, a Homeodomain Protein Required for DNA Methylation, As Well As RDR2, RDM4, and Chromatin Remodeling Factors, Associate with RNA Polymerase IV. PLoS Genet 7 e1002195 doi:10.1371/journal.pgen.1002195
43. SmithLMPontesOSearleIYelinaNYousafzaiFK 2007 An SNF2 protein associated with nuclear RNA silencing and the spread of a silencing signal between cells in Arabidopsis. Plant Cell 19 1507 1521
44. LiuJBaiGZhangCChenWZhouJ 2011 An atypical component of RNA-directed DNA methylation machinery has both DNA methylation-dependent and -independent roles in locus-specific transcriptional gene silencing. Cell Res 21 1691 1700
45. AusinIMocklerTCChoryJJacobsenSE 2009 IDN1 and IDN2 are required for de novo DNA methylation in Arabidopsis thaliana. Nature Struct Mol Biol 16 1325 1327
46. ZhengZXingYHeXJLiWHuY 2010 An SGS3-like protein functions in RNA-directed DNA methylation and transcriptional gene silencing in Arabidopsis. Plant J 62 92 99
47. BatemanA 2002 The SGS3 protein involved in PTGS finds a family. BMC Bioinformatics 3 21
48. MourrainPBéclinCElmayanTFeuerbachFGodonC 2000 Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101 533 542
49. FukunagaRDoudnaJA 2009 dsRNA with 5′ overhangs contributes to endogenous and antiviral RNA silencing pathways in plants. EMBO J 28 545 555
50. YoshikawaMPeragineAParkMYPoethigRS 2005 A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev 19 2164 2175
51. BorsaniOZhuJVersluesPESunkarRZhuJK 2005 Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123 1279 1291
52. ElmayanTAdenotXGissotLLauresserguesDGyI 2009 A neomorphic sgs3 allele stabilizing miRNA cleavage products reveals that SGS3 acts as a homodimer. FEBS J 276 835 844
53. HuettelBKannoTDaxingerLAufsatzWMatzkeAJ 2006 Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. EMBO J 25 2828 2836
54. MathieuOReindersJCaikovskiMSmathajittCPaszkowskiJ 2007 Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation. Cell 130 851 862
55. XieMRenGCosta-NunesPPontesOYuB 2012 A subgroup of SGS3-like proteins act redundantly in RNA-directed DNA methylation. Nucleic Acids Res doi:10.1093/nar/gks034
56. HetzlJFoersterAMRaidlGMittelsten ScheidO 2007 CyMATE: a new tool for methylation analysis of plant genomic DNA after bisulfite sequencing. Plant J 51 526 536
57. HeXJHsuYFPontesOZhuJLuJ 2009 NRPD4, a protein related to the RPB4 subunit of RNA polymerase II, is a component of RNA polymerases IV and V and is required for RNA-directed DNA methylation. Genes Dev 23 318 330
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 5
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