RNA polymerase V-dependent small RNAs in Arabidopsis originate from small, intergenic loci including most SINE repeats

Epigenetics

Volumn 7, Issue 7, 2012, Pages 781-795

  Lee, Tzuu Fen ^a   Gurazada, Sai Guna Ranjan ^a,d   Zhai, Jixian ^a   Li, Shengben ^b   Simon, Stacey A ^a   Matzke, Marjori A ^c   Chen, Xuemei ^b   Meyers, Blake C ^a  

^a UNIVERSITY OF DELAWARE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c GREGOR MENDEL INSTITUTE OF MOLECULAR PLANT BIOLOGY   (Austria)

^d DUPONT COMPANY   (United States)

Author keywords

Arabidopsis; Heterochromatin; RNA polymerase IV; RNA polymerase V; RNA directed DNA methylation; SINE; Small RNA

Indexed keywords

RNA POLYMERASE; RNA POLYMERASE V; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; CONTROLLED STUDY; DEFECTIVE IN MERISTEM SILENCING 3 GENE; DEFECTIVE IN MERISTEM SILENCING 4 GENE; DEFECTIVE IN RNA DIRECTED DNA METHYLATION 1 GENE; GENE LOCUS; GENE SILENCING; HETEROCHROMATIN; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT GENE; PLANT GENOME; RNA DIRECTED DNA METHYLATION 1 GENE; SHORT INTERSPERSED REPEAT; TRANSPOSON; WILD TYPE;

ARABIDOPSIS;

EID: 84863792071     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.20290     Document Type: Article

References (62)

1. Grewal SI, Jia S. Heterochromatin revisited. Nat Rev Genet 2007; 8:35-46. PMID:17173056; http://dx.doi.org/10.1038/nrg2008.
2. Chan SW, Henderson IR, Jacobsen SE. Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 2005; 6:351-360. PMID:15861207; http://dx.doi.org/10.1038/nrg1601.
3. Tamaru H. Confining euchromatin/heterochromatin territory: jumonji crosses the line. Genes Dev 2010; 24:1465-1478. PMID:20634313; http://dx.doi.org/10.1101/gad.1941010.
4. Matzke MA, Birchler JA. RNAi-mediated pathways in the nucleus. Nat Rev Genet 2005; 6:24-35;PMID:15630419; http://dx.doi.org/10.1038/nrg1500.
5. Volpe TA, Kidner C, Hall IM, Teng G, Grewal SI, Martienssen RA. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 2002; 297:1833-1837. PMID:12193640; http://dx.doi.org/10.1126/science.1074973
6. Pilberman D, Cao X, Jacobsen SE. ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 2003; 299:716-719. PMID:12522258; http://dx.doi.org/10.1126/science.1079695.
7. Xie Z, Johansen LK, Gustafson AM, Kasschau KD, Lellis AD, Zilberman D, et al. Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2004; 2:104. PMID:15024409; http://dx.doi.org/10.1371/journal.pbio.0020104.
8. Law JA, Jacobsen SE. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 2010; 11:204-220;PMID:20142834; http://dx.doi.org/10.1038/nrg2719.
9. Matzke M, Kanno T, Daxinger L, Huettel B, Matzke AJM. RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol 2009; 21:367-376;PMID:19243928; http://dx.doi.org/10.1016/j.ceb.2009.01.025.
10. Lahmy S, Bies-Etheve N, Lagrange T. Plant-specific multisubunit RNA polymerase in gene silencing. Epigenetics 2010; 5:4-8. PMID:20173420; http://dx.doi.org/10.4161/epi.5.1.10435.
11. Pikaard CS, Haag JR, Ream T, Wierzbicki AT. Rolesof RNA polymerase IV in gene silencing. Trends Plant Sci 2008; 13:390-397. PMID:18514566; http://dx.doi.org/10.1016/j.tplants.2008.04.008.
12. Ream TS, Haag JR, Wierzbicki AT, Nicora CD, Norbeck AD, Zhu JK, et al. Subunit compositions of the RNA-silencing enzymes Pol IV and Pol V reveal their origins as specialized forms of RNA polymerase II. Mol Cell 2009; 33:192-203. PMID:19110459; http://dx.doi.org/10.1016/j.molcel.2008.12.015.
13. Herr AJ, Jensen MB, Dalmay T, Baulcombe DC. RNA polymerase IV directs silencing of endogenous DNA. Science 2005; 308:118-120. PMID:15692015; http://dx.doi.org/10.1126/science.1106910.
14. Onodera Y, Haag JR, Ream T, Costa Nunes P, Pontes O, Pikaard CS. Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 2005; 120:613-622. PMID:15766525; http://dx.doi.org/10.1016/j.cell.2005.02.007.
15. Kanno T, Huettel B, Mette MF, Aufsatz W, Jaligot E, Daxinger L, et al. Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nat Genet 2005; 37:761-765. PMID:15924141; http://dx.doi.org/10.1038/ng1580.
16. Pontier D, Yahubyan G, Vega D, Bulski A, Saez- Vasquez J, Hakimi MA, et al. Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis. Genes Dev 2005; 19:2030-2040. PMID:16140984; http://dx.doi.org/10.1101/gad.348405.
17. Lahmy S, Pontier D, Cavel E, Vega D, El-Shami M, Kanno T, et al. PolV(PolIVb) function in RNA-directed DNA methylation requires the conserved active site and an additional plant-specific subunit. Proc Natl Acad Sci USA 2009; 106:941-946. PMID:19141635;http://dx.doi.org/10.1073/pnas.0810310106.
18. Li CF, Pontes O, El-Shami M, Henderson IR, Bernatavichute YV, Chan SW, et al. An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell 2006; 126:93-106. PMID:16839879; http://dx.doi.org/10.1016/j.cell.2006.05.032.
19. Mosher RA, Schwach F, Studholme D, Baulcombe DC. PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis. Proc Natl Acad Sci USA 2008; 105:3145-3150. PMID:18287047;http://dx.doi.org/10.1073/pnas.0709632105.
20. Wierzbicki AT, Ream TS, Haag JR, Pikaard CS. RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat Genet 2009; 41:630-634;PMID:19377477; http://dx.doi.org/10.1038/ng.365.
21. Zheng B, Wang Z, Li S, Yu B, Liu JY, Chen X. Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev 2009; 23:2850-2860. PMID:19948763; http://dx.doi.org/10.1101/gad.1868009.
22. Gao Z, Liu HL, Daxinger L, Pontes O, He X, Qian W, et al. An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation. Nature 2010; 465:106-109. PMID:20410883; http://dx.doi.org/10.1038/nature09025.
23. Zhang H, Zhu JK. RNA-directed DNA methylation. Curr Opin Plant Biol 2011; 14:142-147;PMID:21420348; http://dx.doi.org/10.1016/j.pbi.2011.02.003.
24. Zheng X, Zhu J, Kapoor A, Zhu JK. Role of Arabidopsis AGO6 in siRNA accumulation, DNA methylation and transcriptional gene silencing. EMBO J 2007; 26:1691-1701. PMID:17332757; http://dx.doi.org/10.1038/sj.emboj.7601603.
25. Havecker ER, Wallbridge LM, Hardcastle TJ, Bush MS, Kelly KA, Dunn RM, et al. The Arabidopsis RNA-directed DNA methylation argonautes functionally diverge based on their expression and interaction with target loci. Plant Cell 2010; 22:321-334. PMID:20173091; http://dx.doi.org/10.1105/tpc.109.072199.
26. Eun C, Lorkovic ZJ, Naumann U, Long Q, Havecker ER, Simon SA, et al. AGO6 functions in RNAmediated transcriptional gene silencing in shoot and root meristems in Arabidopsis thaliana. PLoS One 2011; 6:25730. PMID:21998686; http://dx.doi.org/10.1371/journal.pone.0025730.
27. Kanno T, Bucher E, Daxinger L, Huettel B, Kreil DP, Breinig F, et al. RNA-directed DNA methylation and plant development require an IWR1-type transcription factor. EMBO Rep 2010; 11:65-71. PMID:20010803;http://dx.doi.org/10.1038/embor.2009.246.
28. Wierzbicki AT, Haag JR, Pikaard CS. Non coding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 2008; 135:635-648. PMID:19013275;http://dx.doi.org/10.1016/j.cell.2008.09.035.
29. Gao Z, Liu HL, Daxinger L, Pontes O, He X, Qian W, et al. An RNA polymerase II- and AGO4-associatedprotein acts in RNA-directed DNA methylation. Nature 2010; 465:106-109. PMID:20410883; http://dx.doi.org/10.1038/nature09025.
30. Kanno T, Bucher E, Daxinger L, Huettel B, Böhmdorfer G, Gregor W, et al. A structural-maintenance- of-chromosomes hinge domain-containing protein is required for RNA-directed DNA methylation. Nat Genet 2008; 40:670-675. PMID:18425128; http://dx.doi.org/10.1038/ng.119.
31. Ausin I, Mockler TC, Chory J, Jacobsen SE. IDN1 and IDN2 are required for de novo DNA methylation in Arabidopsis thaliana. Nat Struct Mol Biol 2009; 16:1325-7. PMID:19915591; http://dx.doi.org/10.1038/nsmb.1690.
32. He XJ, Hsu YF, Zhu S, Wierzbicki AT, Pontes O, Pikaard CS, et al. An effect or of RNA-directed DNA methylation in arabidopsis is an ARGONAUTE 4- and RNA-binding protein. Cell 2009; 137:498-508. PMID:19410546; http://dx.doi.org/10.1016/j.cell.2009.04.028.
33. Bies-Etheve N, Pontier D, Lahmy S, Picart C, Vega D, Cooke R, et al. RNA-directed DNA methylation requires an AGO4-interacting member of the SPT5 elongation factor family. EMBO Rep 2009; 10:649-654. PMID:19343051; http://dx.doi.org/10.1038/embor.2009.31.
34. Cao X, Aufsatz W, Zilberman D, Mette MF, Huang MS, Matzke M, et al. Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation. Curr Biol 2003; 13:2212-2217. PMID:14680640; http://dx.doi.org/10.1016/j.cub.2003.11.052.
35. Cao X, Jacobsen SE. Role of the arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 2002; 12:1138-1144;PMID:12121623; http://dx.doi.org/10.1016/S0960-9822(02)00925-9.1086391.
36. Lindroth AM, Cao X, Jackson JP, Zilberman D, McCallum CM, Henikoff S, et al. Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 2001; 292:2077-2080;PMID:11349138; http://dx.doi.org/10.1126/science.1059745.
37. Johnson LM, Law JA, Khattar A, Henderson IR, Jacobsen SE. SRA-domain proteins required for DRM2-mediated de novo DNA methylation. PLoS Genet 2008; 4:1000280; PMID:19043555; http://dx.doi.org/10.1371/journal.pgen.1000280.
38. Daxinger L, Kanno T, Bucher E, van der Winden J, Naumann U, Matzke AJM, et al. A stepwise pathway for biogenesis of 24-nt secondary siRNAs and spreading of DNA methylation. EMBO J 2009; 28:48-57.PMID:19078964; http://dx.doi.org/10.1038/emboj.2008.260.
39. Zhang X, Henderson IR, Lu C, Green PJ, Jacobsen SE. Role of RNA polymerase IV in plant small RNA metabolism. Proc Natl Acad Sci USA 2007; 104:4536-4541.PMID:17360559; http://dx.doi.org/10.1073/pnas.0611456104.
40. Kanno T, Mette MF, Kreil DP, Aufsatz W, Matzke M, Matzke AJ. Involvement of putative SNF2 chromatin remodeling protein DRD1 in RNA-directedDNA methylation. Curr Biol 2004; 14:801-805.PMID:15120073; http://dx.doi.org/10.1016/j.cub.2004.04.037.
41. Nobuta K, Lu C, Shrivastava R, Pillay M, De Paoli E, Accerbi M, et al. Distinct size distribution of endogeneous siRNAs in maize: Evidence from deep sequencing in the mop1-1 mutant. Proc Natl Acad Sci USA 2008; 105:14958-14963. PMID:18815367; http://dx.doi.org/10.1073/pnas.0808066105.
42. Kasschau KD, Fahlgren N, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, et al. Genome-wide profiling and analysis of Arabidopsis si RNAs. PLoS Biol 2007; 5:57. PMID:17298187; http://dx.doi.org/10.1371/journal.pbio.0050057.
43. Lu C, Kulkarni K, Souret FF, MuthuValliappan R, Tej SS, Poethig RS, et al. MicroRNAs and other small RNAs enriched in the Arabidopsis RNAdependent RNA polymerase-2 mutant. Genome Res 2006; 16:1276-1288. PMID:16954541; http://dx.doi.org/10.1101/gr.5530106.
44. Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, et al. The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 2012; 40:1202-1210;PMID:22140109; http://dx.doi.org/10.1093/nar/gkr1090.
45. Smit A, Hubley R, Green P. Repeat Masker Open-3.0. http://wwwrepeatmaskerorg 1996-2010.
46. Zilberman D, Henikoff S. Silencing of transposons in plant genomes: kick them when they're down. Genome Biol 2004; 5:249. PMID:15575975; http://dx.doi.org/10.1186/gb-2004-5-12-249
47. Lisch D. Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol 2009; 60:43-66; PMID:19007329; http://dx.doi.org/10.1146/annurev.arplant.59.032607.092744.
48. Goodier JL, Kazazian HH Jr. Retrotransposons revisited: the restraint and rehabilitation of parasites. Cell 2008; 135:23-35. PMID:18854152; http://dx.doi.org/10.1016/j.cell.2008.09.022.
49. Law JA, Ausin I, Johnson LM, Vashisht AA, Zhu JK, Wohlschlegel JA, et al. A protein complex required for polymerase V transcripts and RNA-directed DNA methylation in Arabidopsis. Curr Biol 2010; 20:951-956. PMID:20409711; http://dx.doi.org/10.1016/j.cub.2010.03.062.
50. Copenhaver GP, Nickel K, Kuromori T, Benito MI, Kaul S, Lin X, et al. Genetic definition and sequence analysis of Arabidopsis centromeres. Science 1999; 286:2468-474. PMID:10617454; http://dx.doi.org/10.1126/science.286.5449.2468.
51. Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 2000; 408:796-815. PMID:11130711; http://dx.doi.org/10.1038/35048692.
52. Tran RK, Zilberman D, de Bustos C, Ditt RF, Henikoff JG, Lindroth AM, et al. Chromatin and siRNA pathways cooperate to maintain DNA methylation of small transposable elements in Arabidopsis. Genome Biol 2005; 6:90. PMID:16277745; http://dx.doi.org/10.1186/gb-2005-6-11-r90.
53. Ahmed I, Sarazin A, Bowler C, Colot V, Quesneville H. Genome-wide evidence for local DNA methylation spreading from small RNA-targeted sequences in Arabidopsis. Nucleic Acids Res 2011; 39:6919-6931; PMID:21586580; http://dx.doi.org/10.1093/nar/gkr324.
54. Huettel B, Kanno T, Daxinger L, Aufsatz W, Matzke AJ, Matzke M. Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. EMBO J 2006; 25:2828-2836. PMID:16724114; http://dx.doi.org/10.1038/sj.emboj.7601150.
55. Chodavarapu RK, Feng S, Bernatavichute YV, Chen PY, Stroud H, Yu Y, et al. Relationship between nucleosome positioning and DNA methylation. Nature 2010; 466:388-392. PMID:20512117; http://dx.doi.org/10.1038/nature09147.
56. Tran RK, Zilberman D, de Bustos C, Ditt RF, Henikoff JG, Lindroth AM, et al. Chromatin and siRNA pathways cooperate to maintain DNA methylation of small transposable elements in Arabidopsis. Genome Biol 2005; 6:90. PMID:16277745; http://dx.doi.org/10.1186/gb-2005-6-11-r90.
57. Haag JR, Pikaard CS. Multi subunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing. Nat Rev Mol Cell Biol 2011; 12:483-492. PMID:21779025; http://dx.doi.org/10.1038/nrm3152.
58. He XJ, Hsu YF, Zhu S, Liu HL, Pontes O, Zhu J, et al. A conserved transcriptional regulator is required for RNA-directed DNA methylation and plant development. Genes Dev 2009; 23:2717-2722. PMID:19903758;http://dx.doi.org/10.1101/gad.1851809.
59. Lu C, Meyers BC, Green PJ. Construction of small RNA cDNA libraries for deep sequencing. Methods 2007; 43:110-117. PMID:17889797; http://dx.doi.org/10.1016/j.ymeth.2007.05.002.
60. Nobuta K, McCormick K, Nakano M, Meyers BC. Bioinformatics analysis of small RNAs in plants using next generation sequencing technologies. Methods Mol Biol 2010; 592:89-106. PMID:19802591; http://dx.doi.org/10.1007/978-1-60327-005-2_7.
61. McCormick KP, Willmann MR, Meyers BC. Experimental design, preprocessing, normalization and differential expression analysis of small RNA sequencing experiments. Silence 2011; 2:2. PMID:21356093;http://dx.doi.org/10.1186/1758-907X-2-2.
62. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 2003; 301:653-657. PMID:12893945; http://dx.doi.org/10.1126/science.1086391.