The splicing machinery promotes RNA-directed DNA methylation and transcriptional silencing in Arabidopsis

EMBO Journal

Volumn 32, Issue 8, 2013, Pages 1128-1140

  Zhang, Cui Jun ^a   Zhou, Jin Xing ^a   Liu, Jun ^a   Ma, Ze Yang ^a   Zhang, Su Wei ^a   Dou, Kun ^a   Huang, Huan Wei ^a   Cai, Tao ^a   Liu, Renyi ^b   Zhu, Jian Kang ^c,d   He, Xin Jian ^a  

^a NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c PURDUE UNIVERSITY   (United States)

^d INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

Author keywords

DNA methylation; RdDM; splicing; transcriptional silencing; ZOP1

Indexed keywords

PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; ZINC FINGER AND OCRE DOMAIN CONTAINING PROTEIN 1;

ARABIDOPSIS; ARTICLE; COILED BODY; CONTROLLED STUDY; DNA METHYLATION; GENE; GENE MUTATION; GENE REPRESSION; GENE TARGETING; GENETIC SCREENING; IMMUNOFLUORESCENCE; MAC3A3B GENE; MOS12 GENE; MOS14 GENE; MOS4 GENE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA DIRECTED DNA METHYLATION; ROS1 GENE; TRANSCRIPTION TERMINATION; TRANSGENE; ZOP1 GENE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA; DNA METHYLATION; DNA-DIRECTED RNA POLYMERASES; GENE EXPRESSION REGULATION; RNA; RNA POLYMERASE II; RNA SPLICING; TRANSCRIPTION, GENETIC;

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84876419021     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2013.49     Document Type: Article

References (65)

1. Ausin I, Greenberg MV, Li CF, Jacobsen SE (2012) The splicing factor SR45 affects the RNA-directed DNA methylation pathway in Arabidopsis. Epigenetics 7: 29-33
2. Baurle I, Smith L, Baulcombe DC, Dean C (2007) Widespread role for the flowering-time regulators FCA and FPA in RNA-mediated chromatin silencing. Science 318: 109-112
3. Bayne EH, Portoso M, Kagansky A, Kos-Braun IC, Urano T, Ekwall K, Alves F, Rappsilber J, Allshire RC (2008) Splicing factors facilitate RNAi-directed silencing in fission yeast. Science 322: 602-606
4. Bernard P, Drogat J, Dheur S, Genier S, Javerzat JP (2010) Splicing factor Spf30 assists exosome-mediated gene silencing in fission yeast. Mol Cell Biol 30: 1145-1157
5. Buhler M, Verdel A, Moazed D (2006) Tethering RITS to a nascent transcript initiates RNAi-and heterochromatin-dependent gene silencing. Cell 125: 873-886
6. Callebaut I, Mornon JP (2005) OCRE: a novel domain made of imperfect, aromatic-rich octamer repeats. Bioinformatics 21 : 699-702
7. Cao X, Jacobsen SE (2002) Role of the arabidopsis DRM methyl-transferases in de novo DNA methylation and gene silencing. Curr Biol 12: 1138-1144
8. Chinen M, Morita M, Fukumura K, Tani T (2010) Involvement of the spliceosomal U4 small nuclear RNA in heterochromatic gene silencing at fission yeast centromeres. J Biol Chem 285: 5630-5638
9. Christie M, Croft LJ, Carroll BJ (2011) Intron splicing suppresses RNA silencing in Arabidopsis. Plant J 68: 159-167
10. Cioce M, Lamond AI (2005) Cajal bodies: a long history of discovery. Annu Rev Cell Dev Biol 21 : 105-131
11. Gao Z, Liu HL, Daxinger L, Pontes O, He X, Qian W, Lin H, Xie M, Lorkovic ZJ, Zhang S, Miki D, Zhan X, Pontier D, Lagrange T, Jin H, Matzke AJ, Matzke M, Pikaard CS, Zhu JK (2010) An RNA polymerase II-and AGO4-associated protein acts in RNA-directed DNA methylation. Nature 465: 106-109
12. Gong Z, Morales-Ruiz T, Ariza RR, Roldán-Arjona T, David L, Zhu JK (2002) ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell 11 1 : 803-814
13. Grewal SI (2010) RNAi-dependent formation of heterochromatin and its diverse functions. Curr Opin Genet Dev 20: 134-141
14. Hall IM, Shankaranarayana GD, Noma K, Ayoub N, Cohen A, Grewal SI (2002) Establishment and maintenance of a heterochromatin domain. Science 297: 2232-2237
15. He XJ, Hsu YF, Zhu S, Wierzbicki AT, Pontes O, Pikaard CS, Liu HL, Wang CS, Jin H, Zhu JK (2009a) An effector of RNA-directed DNA methylation in arabidopsis is an ARGONAUTE 4-and RNA-binding protein. Cell 137: 498-508
16. He XJ, Hsu YF, Zhu S, Liu HL, Pontes O, Zhu J, Cui X, Wang CS, Zhu JK (2009b) A conserved transcriptional regulator is required for RNA-directed DNA methylation and plant development. Genes Dev 23: 2717-2722
17. He XJ, Hsu YF, Pontes O, Zhu J, Lu J, Bressan RA, Pikaard C, Wang CS, Zhu JK (2009c) NRPD4, a protein related to the RPB4 subunit of RNA polymerase II, is a component of RNA polymerases IVand V and is required for RNA-directed DNA methylation. Genes Dev 23: 318-330
18. Herr AJ, Jensen MB, Dalmay T, Baulcombe DC (2005) RNA poly-merase IV directs silencing of endogenous DNA. Science 308: 118-120
19. Hornyik C, Terzi LC, Simpson GG (2010) The spen family protein FPA controls alternative cleavage and polyadenylation of RNA. Dev Cell 18: 203-213
20. Kaida D, Berg MG, Younis I, Kasim M, Singh LN, Wan L, Dreyfuss G (2010) U1 snRNP protects pre-mRNAs from premature cleavage and polyadenylation. Nature 468: 664-668
21. Kanno T, Bucher E, Daxinger L, Huettel B, Böhmdorfer G, Gregor W, Kreil DP, Matzke M, Matzke AJ (2008) A structural-maintenance-of-chromosomes hinge domain-containing protein is required for RNA-directed DNA methylation. Nat Genet 40: 670-675
22. Kanno T, Bucher E, Daxinger L, Huettel B, Kreil DP, Breinig F, Lind M, Schmitt MJ, Simon SA, Gurazada SG, Meyers BC, Lorkovic ZJ, Matzke AJ, Matzke M (2010) RNA-directed DNA methylation and plant development require an IWR1-type transcription factor. EMBO Rep 11 : 65-71
23. Kanno T, Huettel B, Mette MF, Aufsatz W, Jaligot E, Daxinger L, Kreil DP, Matzke M, Matzke AJ (2005) Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nat Genet 37: 761-765
24. Kanno T, Mette MF, Kreil DP, Aufsatz W, Matzke M, Matzke AJ (2004) Involvement of putative SNF2 chromatin remodeling protein DRD1 in RNA-directed DNA methylation. Curr Biol 14: 801-805
25. Kim YJ, Zheng B, Yu Y, Won SY, Mo B, Chen X (2011) The role of Mediator in small and long noncoding RNA production in Arabidopsis thaliana. EMBO J 30: 814-822
26. Krueger F, Andrews SR (2011) Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 27: 1571-1572
27. Law JA, Ausin I, Johnson LM, Vashisht AA, Zhu JK, Wohlschlegel JA, Jacobsen SE (2010) A protein complex required for polymer-ase V transcripts and RNA-directed DNA methylation in Arabidopsis. Curr Biol 20: 951-956
28. Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11 : 204-220
29. Law JA, Vashisht AA, Wohlschlegel JA, Jacobsen SE (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
30. Li CF, Henderson IR, Song L, Fedoroff N, Lagrange T, Jacobsen SE (2008) Dynamic regulation of ARGONAUTE4 within multiple nuclear bodies in Arabidopsis thaliana. PLoS Genet 4: e27
31. Li CF, Pontes O, El-Shami M, Henderson IR, Bernatavichute YV, Chan SW, Lagrange T, Pikaard CS, Jacobsen SE (2006) An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell 126: 93-106
32. 0 processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327: 94-97
33. Liu J, Bai G, Zhang C, Chen W, Zhou J, Zhang S, Chen Q, Deng X, He XJ, Zhu JK (2011) An atypical component of RNA-directed DNA methylation machinery has both DNA methylation-dependent and-independent roles in locus-specific transcrip-tional gene silencing. Cell Res 21 : 1691-1700
34. Makarov EM, Makarova OV, Achsel T, Luhrmann R (2000) The human homologue of the yeast splicing factor prp6p contains multiple TPR elements and is stably associated with the U5 snRNP via protein-protein interactions. J Mol Biol 298: 567-575
35. Matlin AJ, Moore MJ (2007) Spliceosome assembly and composition. Adv Exp Med Biol 623: 14-35
36. Matzke M, Kanno T, Daxinger L, Huettel B, Matzke AJ (2009) RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol 21 : 367-376
37. Moazed D (2009) Small RNAs in transcriptional gene silencing and genome defence. Nature 457: 413-420
38. Monaghan J, Xu F, Gao M, Zhao Q, Palma K, Long C, Chen S, Zhang Y, Li X (2009) Two Prp19-like U-box proteins in the MOS4-associated complex play redundant roles in plant innate immunity. PLoS Pathog 5: e1000526
39. Morris GE (2008) The Cajal body. Biochim Biophys Acta 1783: 2108-2115
40. Mosher RA, Schwach F, Studholme D, Baulcombe DC (2008) PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis. Proc Natl Acad Sci USA 105 : 3145-3150
41. Motamedi MR, Verdel A, Colmenares SU, Gerber SA, Gygi SP, Moazed D (2004) Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell 119: 789-802
42. Onodera Y, Haag JR, Ream T, Costa Nunes P, Pontes O, Pikaard CS (2005) Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 120: 613-622
43. Pikaard CS (2006) Cell biology of the Arabidopsis nuclear siRNA pathway for RNA-directed chromatin modification. Cold Spring Harb Symp Quant Biol 71: 473-480
44. Pontes O, Li CF, Costa Nunes P, Haag J, Ream T, Vitins A, Jacobsen SE, Pikaard CS (2006) The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell 126: 79-92
45. Pontier D, Yahubyan G, Vega D, Bulski A, Saez-Vasquez J, Hakimi MA, Lerbs-Mache S, Colot V, Lagrange T (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
46. Qi Y, He X, Wang XJ, Kohany O, Jurka J, Hannon GJ (2006) Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-direc-ted DNA methylation. Nature 443: 1008-1012
47. Ream TS, Haag JR, Wierzbicki AT, Nicora CD, Norbeck AD, Zhu JK, Hagen G, Guilfoyle TJ, Pasa-Tolić L, Pikaard CS (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
48. Reyes-Turcu FE, Zhang K, Zofall M, Chen E, Grewal SI (2011) Defects in RNA quality control factors reveal RNAi-independent nucleation of heterochromatin. Nat Struct Mol Biol 18: 1132-1138
49. Sharp PA (1994) Split genes and RNA splicing. Cell 77: 805-815
50. Shukla S, Kavak E, Gregory M, Imashimizu M, Shutinoski B, Kashlev M, Oberdoerffer P, Sandberg R, Oberdoerffer S (2011) CTCF-promoted RNA polymerase II pausing links DNA methyla-tion to splicing. Nature 479: 74-79
51. Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8: 272-285
52. Smith LM, Pontes O, Searle I, Yelina N, Yousafzai FK, Herr AJ, Pikaard CS, Baulcombe DC (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
53. Tang W, Kannan R, Blanchette M, Baumann P (2012) Telomerase RNA biogenesis involves sequential binding by Sm and Lsm complexes. Nature 484: 260-264
54. Verdel A, Jia S, Gerber S, Sugiyama T, Gygi S, Grewal SI, Moazed D (2004) RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303: 672-676
55. Volpe TA, Kidner C, Hall IM, Teng G, Grewal SI, Martienssen RA (2002) Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297: 1833-1837
56. Wierzbicki AT, Haag JR, Pikaard CS (2008) Non-coding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135: 635-648
57. Wierzbicki AT, Ream TS, Haag JR, Pikaard CS (2009) RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat Genet 41: 630-634
58. Wierzbicki AT, Cocklin R, Mayampurath A, Lister R, Rowley MJ, Gregory BD, Ecker JR, Tang H, Pikaard CS (2012) Spatial and functional relationships among Pol V-associated loci, Pol IV-dependent siRNAs, and cytosine methylation in the Arabidopsis epigenome. Genes Dev 26: 1825-1836
59. Xie Z, Johansen LK, Gustafson AM, Kasschau KD, Lellis AD, Zilberman D, Jacobsen SE, Carrington JC (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2: e104
60. Xu F, Xu S, Wiermer M, Zhang Y, Li X (2012) The cyclin L homolog MOS12 and the MOS4-associated complex are required for the proper splicing of plant resistance genes. Plant J 70: 916-928
61. Xu S, Zhang Z, Jing B, Gannon P, Ding J, Xu F, Li X, Zhang Y (2011) Transportin-SR is required for proper splicing of resistance genes and plant immunity. PLoS Genet 7: e1002159
62. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565-1572
63. Zheng B, Wang Z, Li S, Yu B, Liu JY, Chen X (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
64. Zhou Z, Licklider LJ, Gygi SP, Reed R (2002) Comprehensive proteomic analysis of the human spliceosome. Nature 419: 182-185
65. Zofall M, Yamanaka S, Reyes-Turcu FE, Zhang K, Rubin C, Grewal SI (2012) RNA elimination machinery targeting meiotic mRNAs promotes facultative heterochromatin formation. Science 335: 96-100