The SET Domain Proteins SUVH2 and SUVH9 Are Required for Pol V Occupancy at RNA-Directed DNA Methylation Loci

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RNA-directed DNA methylation (RdDM) is required for transcriptional silencing of transposons and other DNA repeats in Arabidopsis thaliana. Although previous research has demonstrated that the SET domain-containing SU(VAR)3–9 homologs SUVH2 and SUVH9 are involved in the RdDM pathway, the underlying mechanism remains unknown. Our results indicated that SUVH2 and/or SUVH9 not only interact with the chromatin-remodeling complex termed DDR (DMS3, DRD1, and RDM1) but also with the newly characterized complex composed of two conserved Microrchidia (MORC) family proteins, MORC1 and MORC6. The effect of suvh2suvh9 on Pol IV-dependent siRNA accumulation and DNA methylation is comparable to that of the Pol V mutant nrpe1 and the DDR complex mutant dms3, suggesting that SUVH2 and SUVH9 are functionally associated with RdDM. Our CHIP assay demonstrated that SUVH2 and SUVH9 are required for the occupancy of Pol V at RdDM loci and facilitate the production of Pol V-dependent noncoding RNAs. Moreover, SUVH2 and SUVH9 are also involved in the occupancy of DMS3 at RdDM loci. The putative catalytic active site in the SET domain of SUVH2 is dispensable for the function of SUVH2 in RdDM and H3K9 dimethylation. We propose that SUVH2 and SUVH9 bind to methylated DNA and facilitate the recruitment of Pol V to RdDM loci by associating with the DDR complex and the MORC complex.

Vyšlo v časopise: The SET Domain Proteins SUVH2 and SUVH9 Are Required for Pol V Occupancy at RNA-Directed DNA Methylation Loci. PLoS Genet 10(1): e32767. doi:10.1371/journal.pgen.1003948
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003948

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Zdroje

1. MatzkeM, KannoT, DaxingerL, HuettelB, MatzkeAJ (2009) RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol 21: 367–376.

2. LawJA, JacobsenSE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11: 204–220.

3. CastelSE, MartienssenRA (2013) RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat Rev Genet 14: 100–112.

4. MirouzeM, ReindersJ, BucherE, NishimuraT, SchneebergerK, et al. (2009) Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461: 427–430.

5. TsukaharaS, KobayashiA, KawabeA, MathieuO, MiuraA, et al. (2009) Bursts of retrotransposition reproduced in Arabidopsis. Nature 461: 423–426.

6. SlotkinRK, VaughnM, BorgesF, TanurdzicM, BeckerJD, et al. (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136: 461–472.

7. MosherRA, MelnykCW, KellyKA, DunnRM, StudholmeDJ, et al. (2009) Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis. Nature 460: 283–286.

8. Olmedo-MonfilV, Duran-FigueroaN, Arteaga-VazquezM, Demesa-ArevaloE, AutranD, et al. (2010) Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464: 628–632.

9. ItoH, GaubertH, BucherE, MirouzeM, VaillantI, et al. (2011) An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472: 115–119.

10. HerrAJ, JensenMB, DalmayT, BaulcombeDC (2005) RNA polymerase IV directs silencing of endogenous DNA. Science 308: 118–120.

11. XieZ, JohansenLK, GustafsonAM, KasschauKD, LellisAD, et al. (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2: E104.

12. HaagJR, ReamTS, MarascoM, NicoraCD, NorbeckAD, et al. (2012) In vitro transcription activities of Pol IV, Pol V, and RDR2 reveal coupling of Pol IV and RDR2 for dsRNA synthesis in plant RNA silencing. Mol Cell 48: 811–818.

13. LawJA, VashishtAA, WohlschlegelJA, JacobsenSE (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.

14. LiuJ, BaiG, ZhangC, ChenW, ZhouJ, et al. (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.

15. YeR, WangW, IkiT, LiuC, WuY, et al. (2012) Cytoplasmic assembly and selective nuclear import of Arabidopsis Argonaute4/siRNA complexes. Mol Cell 46: 859–870.

16. ReamTS, HaagJR, WierzbickiAT, NicoraCD, NorbeckAD, et al. (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.

17. WierzbickiAT, HaagJR, PikaardCS (2008) Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135: 635–648.

18. WierzbickiAT, ReamTS, HaagJR, PikaardCS (2009) RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat Genet 41: 630–634.

19. KannoT, MetteMF, KreilDP, AufsatzW, MatzkeM, et al. (2004) Involvement of putative SNF2 chromatin remodeling protein DRD1 in RNA-directed DNA methylation. Curr Biol 14: 801–805.

20. KannoT, BucherE, DaxingerL, HuettelB, BohmdorferG, et al. (2008) A structural-maintenance-of-chromosomes hinge domain-containing protein is required for RNA-directed DNA methylation. Nat Genet 40: 670–675.

21. GaoZ, LiuHL, DaxingerL, PontesO, HeX, et al. (2010) An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation. Nature 465: 106–109.

22. LawJA, AusinI, JohnsonLM, VashishtAA, ZhuJK, et al. (2010) A protein complex required for polymerase V transcripts and RNA- directed DNA methylation in Arabidopsis. Curr Biol 20: 951–956.

23. ZhongX, HaleCJ, LawJA, JohnsonLM, FengS, et al. (2012) DDR complex facilitates global association of RNA polymerase V to promoters and evolutionarily young transposons. Nat Struct Mol Biol 19: 870–875.

24. HeXJ, HsuYF, ZhuS, LiuHL, PontesO, et al. (2009) A conserved transcriptional regulator is required for RNA-directed DNA methylation and plant development. Genes Dev 23: 2717–2722.

25. KannoT, BucherE, DaxingerL, HuettelB, KreilDP, et al. (2010) RNA-directed DNA methylation and plant development require an IWR1-type transcription factor. EMBO Rep 11: 65–71.

26. HaagJR, PikaardCS (2011) Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing. Nat Rev Mol Cell Biol 12: 483–492.

27. Bies-EtheveN, PontierD, LahmyS, PicartC, VegaD, et al. (2009) RNA-directed DNA methylation requires an AGO4-interacting member of the SPT5 elongation factor family. EMBO Rep 10: 649–654.

28. HeXJ, HsuYF, ZhuS, WierzbickiAT, PontesO, et al. (2009) An effector of RNA-directed DNA methylation in arabidopsis is an ARGONAUTE 4- and RNA-binding protein. Cell 137: 498–508.

29. RowleyMJ, AvrutskyMI, SifuentesCJ, PereiraL, WierzbickiAT (2011) Independent chromatin binding of ARGONAUTE4 and SPT5L/KTF1 mediates transcriptional gene silencing. PLoS Genet 7: e1002120.

30. ZhangCJ, NingYQ, ZhangSW, ChenQ, ShaoCR, et al. (2012) IDN2 and its paralogs form a complex required for RNA-directed DNA methylation. PLoS Genet 8: e1002693.

31. AusinI, GreenbergMV, SimanshuDK, HaleCJ, VashishtAA, et al. (2012) INVOLVED IN DE NOVO 2-containing complex involved in RNA-directed DNA methylation in Arabidopsis. Proc Natl Acad Sci U S A 109: 8374–8381.

32. XieM, RenG, ZhangC, YuB (2012) The DNA- and RNA-binding protein FACTOR of DNA METHYLATION 1 requires XH domain-mediated complex formation for its function in RNA-directed DNA methylation. Plant J 72: 491–500.

33. ZhuY, RowleyMJ, BohmdorferG, WierzbickiAT (2013) A SWI/SNF chromatin-remodeling complex acts in noncoding RNA-mediated transcriptional silencing. Mol Cell 49: 298–309.

34. CaoX, JacobsenSE (2002) Role of the arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12: 1138–1144.

35. HendersonIR, DelerisA, WongW, ZhongX, ChinHG, et al. (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.

36. MoissiardG, CokusSJ, CaryJ, FengS, BilliAC, et al. (2012) MORC family ATPases required for heterochromatin condensation and gene silencing. Science 336: 1448–1451.

37. LorkovicZJ, NaumannU, MatzkeAJ, MatzkeM (2012) Involvement of a GHKL ATPase in RNA-directed DNA methylation in Arabidopsis thaliana. Curr Biol 22: 933–938.

38. BrabbsTR, HeZ, HoggK, KamenskiA, LiY, et al. (2013) The stochastic silencing phenotype of Arabidopsis morc6 mutants reveals a role in efficient RNA-directed DNA methylation. Plant J 75(5): 836–46.

39. BaumbuschLO, ThorstensenT, KraussV, FischerA, NaumannK, et al. (2001) The Arabidopsis thaliana genome contains at least 29 active genes encoding SET domain proteins that can be assigned to four evolutionarily conserved classes. Nucleic Acids Res 29: 4319–4333.

40. JacksonJP, LindrothAM, CaoX, JacobsenSE (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416: 556–560.

41. EbbsML, BenderJ (2006) Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell 18: 1166–1176.

42. RajakumaraE, LawJA, SimanshuDK, VoigtP, JohnsonLM, et al. (2011) A dual flip-out mechanism for 5mC recognition by the Arabidopsis SUVH5 SRA domain and its impact on DNA methylation and H3K9 dimethylation in vivo. Genes Dev 25: 137–152.

43. JohnsonLM, BostickM, ZhangX, KraftE, HendersonI, et al. (2007) The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr Biol 17: 379–384.

44. DuJ, ZhongX, BernatavichuteYV, StroudH, FengS, et al. (2012) Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell 151: 167–180.

45. ZilbermanD, CaoX, JacobsenSE (2003) ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299: 716–719.

46. HuettelB, KannoT, DaxingerL, AufsatzW, MatzkeAJ, et al. (2006) Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. EMBO J 25: 2828–2836.

47. JohnsonLM, LawJA, KhattarA, HendersonIR, JacobsenSE (2008) SRA-domain proteins required for DRM2-mediated de novo DNA methylation. PLoS Genet 4: e1000280.

48. KuhlmannM, MetteMF (2012) Developmentally non-redundant SET domain proteins SUVH2 and SUVH9 are required for transcriptional gene silencing in Arabidopsis thaliana. Plant Mol Biol 79: 623–633.

49. ZhangX, HendersonIR, LuC, GreenPJ, JacobsenSE (2007) Role of RNA polymerase IV in plant small RNA metabolism. Proc Natl Acad Sci U S A 104: 4536–4541.

50. MosherRA, SchwachF, StudholmeD, BaulcombeDC (2008) PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis. Proc Natl Acad Sci U S A 105: 3145–3150.

51. LeeTF, GurazadaSG, ZhaiJ, LiS, SimonSA, et al. (2012) RNA polymerase V-dependent small RNAs in Arabidopsis originate from small, intergenic loci including most SINE repeats. Epigenetics 7: 781–795.

52. StroudH, GreenbergMV, FengS, BernatavichuteYV, JacobsenSE (2013) Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152: 352–364.

53. ListerR, O'MalleyRC, Tonti-FilippiniJ, GregoryBD, BerryCC, et al. (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133: 523–536.

54. ReaS, EisenhaberF, O'CarrollD, StrahlBD, SunZW, et al. (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406: 593–599.

55. TrievelRC, BeachBM, DirkLM, HoutzRL, HurleyJH (2002) Structure and catalytic mechanism of a SET domain protein methyltransferase. Cell 111: 91–103.

56. JessbergerR (2002) The many functions of SMC proteins in chromosome dynamics. Nat Rev Mol Cell Biol 3: 767–778.

57. HeXJ, HsuYF, PontesO, ZhuJ, LuJ, et al. (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.

58. LangmeadB, TrapnellC, PopM, SalzbergSL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.

59. TrapnellC, PachterL, SalzbergSL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105–1111.

60. TrapnellC, WilliamsBA, PerteaG, MortazaviA, KwanG, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511–515.