Specific but interdependent functions for Arabidopsis AGO4 and AGO6 in RNA-directed DNA methylation

EMBO Journal

Volumn 34, Issue 5, 2015, Pages 581-592

  Duan, Cheng Guo ^a   Zhang, Huiming ^a   Tang, Kai ^a   Zhu, Xiaohong ^a   Qian, Weiqiang ^b   Hou, Yueh Ju ^a   Wang, Bangshing ^a   Lang, Zhaobo ^a   Zhao, Yang ^a,b   Wang, Xingang ^a   Wang, Pengcheng ^a   Zhou, Jianping ^c   Liang, Gaimei ^d   Liu, Na ^e   Wang, Chunguo ^f   Zhu, Jian Kang ^a,b  

^a PURDUE UNIVERSITY   (United States)

^b Chinese Academy of Sciences   (China)

^c UNIVERSITY OF ELECTRONIC SCIENCE AND TECHNOLOGY OF CHINA   (China)

^d Shanxi Academy of Agricultural Sciences   (China)

^e ZHEJIANG UNIVERSITY   (China)

^f NANKAI UNIVERSITY   (China)

Author keywords

argonautes; DNA methylation; epigenetics; RdDM; RNA polymerases

Indexed keywords

ARABIDOPSIS ARGONAUTE 4 PROTEIN; ARABIDOPSIS ARGONAUTE 6 PROTEIN; ARABIDOPSIS PROTEIN; RNA; RNA POLYMERASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; AGO4 PROTEIN, ARABIDOPSIS; AGO6 PROTEIN, ARABIDOPSIS; ARGONAUTE PROTEIN; DNA DIRECTED RNA POLYMERASE;

ARTICLE; CHROMATIN; DNA METHYLATION; GENE INTERACTION; GENETIC ASSOCIATION; IMMUNOFLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; RNA DIRECTED DNA METHYLATION; ARABIDOPSIS; CHROMATIN IMMUNOPRECIPITATION; DNA SEQUENCE; FLUORESCENT ANTIBODY TECHNIQUE; GENE SILENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOPRECIPITATION; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ARABIDOPSIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ARGONAUTE PROTEINS; BASE SEQUENCE; CHROMATIN IMMUNOPRECIPITATION; DNA METHYLATION; DNA-DIRECTED RNA POLYMERASES; FLUORESCENT ANTIBODY TECHNIQUE; GENE SILENCING; IMMUNOPRECIPITATION; MOLECULAR SEQUENCE DATA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SEQUENCE ANALYSIS, DNA;

EID: 84923902334     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201489453     Document Type: Article

References (59)

1. Ausin I, Greenberg MV, Simanshu DK, Hale CJ, Vashisht AA, Simon SA, Lee TF, Feng S, Espanola SD, Meyers BC, Wohlschlegel JA, Patel DJ, Jacobsen SE, (2012) INVOLVED IN DE NOVO 2-containing complex involved in RNA-directed DNA methylation in Arabidopsis. Proc Natl Acad Sci USA 109: 8374-8381
2. Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C, (1998) AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J 17: 170-180
3. Castel SE, Martienssen RA, (2013) RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat Rev Genet 14: 100-112
4. Dunoyer P, Schott G, Himber C, Meyer D, Takeda A, Carrington JC, Voinnet O, (2010) Small RNA duplexes function as mobile silencing signals between plant cells. Science 328: 912-916
5. El-Shami M, Pontier D, Lahmy S, Braun L, Picart C, Vega D, Hakimi MA, Jacobsen SE, Cooke R, Lagrange T, (2007) Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes Dev 21: 2539-2544
6. Eun C, Lorkovic ZJ, Naumann U, Long Q, Havecker ER, Simon SA, Meyers BC, Matzke AJ, Matzke M, (2011) AGO6 functions in RNA-mediated transcriptional gene silencing in shoot and root meristems in Arabidopsis thaliana. PLoS One 6: e25730
7. Fagard M, Boutet S, Morel JB, Bellini C, Vaucheret H, (2000) AGO1, QDE-2, and RDE-1 are related proteins required for post-transcriptional gene silencing in plants, quelling in fungi, and RNA interference in animals. Proc Natl Acad Sci USA 97: 11650-11654
8. Farazi TA, Juranek SA, Tuschl T, (2008) The growing catalog of small RNAs and their association with distinct Argonaute/Piwi family members. Development 135: 1201-1214
9. Frank F, Sonenberg N, Nagar B, (2010) Structural basis for 5?-nucleotide base-specific recognition of guide RNA by human AGO2. Nature 465: 818-822
10. 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
11. Ghildiyal M, Zamore PD, (2009) Small silencing RNAs: an expanding universe. Nat Rev Genet 10: 94-108
12. Harris EY, Ponts N, Le Roch KG, Lonardi S, (2012) BRAT-BW: efficient and accurate mapping of bisulfite-treated reads. Bioinformatics 28: 1795-1796
13. Harvey JJ, Lewsey MG, Patel K, Westwood J, Heimstadt S, Carr JP, Baulcombe DC, (2011) An antiviral defense role of AGO2 in plants. PLoS One 6: e14639
14. Havecker ER, Wallbridge LM, Hardcastle TJ, Bush MS, Kelly KA, Dunn RM, Schwach F, Doonan JH, Baulcombe DC, (2010) The Arabidopsis RNA-directed DNA methylation argonautes functionally diverge based on their expression and interaction with target loci. Plant Cell 22: 321-334
15. He XJ, Hsu YF, Zhu S, Wierzbicki AT, Pontes O, Pikaard CS, Liu HL, Wang CS, Jin H, Zhu JK, (2009) An effector of RNA-directed DNA methylation in Arabidopsis is an ARGONAUTE 4- and RNA-binding protein. Cell 137: 498-508
16. Huettel B, Kanno T, Daxinger L, Aufsatz W, Matzke AJ, Matzke M, (2006) Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. EMBO J 25: 2828-2836
17. Jaubert M, Bhattacharjee S, Mello AF, Perry KL, Moffett P, (2011) ARGONAUTE2 mediates RNA-silencing antiviral defenses against Potato virus X in Arabidopsis. Plant Physiol 156: 1556-1564
18. Law JA, Jacobsen SE, (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11: 204-220
19. 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
20. 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
21. Li X, Qian W, Zhao Y, Wang C, Shen J, Zhu JK, Gong Z, (2012) Antisilencing role of the RNA-directed DNA methylation pathway and a histone acetyltransferase in Arabidopsis. Proc Natl Acad Sci USA 109: 11425-11430
22. Lingel A, Simon B, Izaurralde E, Sattler M, (2004) Nucleic acid 3?-end recognition by the Argonaute 2 PAZ domain. Nat Struct Mol Biol 11: 576-577
23. Ma JB, Ye K, Patel DJ, (2004) Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature 429: 318-322
24. Ma JB, Yuan YR, Meister G, Pei Y, Tuschl T, Patel DJ, (2005) Structural basis for 5?-end-specific recognition of guide RNA by the A. fulgidus Piwi protein. Nature 434: 666-670
25. Mallory A, Vaucheret H, (2010) Form, function, and regulation of ARGONAUTE proteins. Plant Cell 22: 3879-3889
26. Martinez-Macias MI, Qian W, Miki D, Pontes O, Liu Y, Tang K, Liu R, Morales-Ruiz T, Ariza RR, Roldan-Arjona T, Zhu JK, (2012) A DNA 3? phosphatase functions in active DNA demethylation in Arabidopsis. Mol Cell 45: 357-370
27. 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
28. Matzke MA, Mosher RA, (2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15: 394-408
29. Mi S, Cai T, Hu Y, Chen Y, Hodges E, Ni F, Wu L, Li S, Zhou H, Long C, Chen S, Hannon GJ, Qi Y, (2008) Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5? terminal nucleotide. Cell 133: 116-127
30. Montgomery TA, Howell MD, Cuperus JT, Li D, Hansen JE, Alexander AL, Chapman EJ, Fahlgren N, Allen E, Carrington JC, (2008) Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133: 128-141
31. Morel JB, Godon C, Mourrain P, Beclin C, Boutet S, Feuerbach F, Proux F, Vaucheret H, (2002) Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell 14: 629-639
32. 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
33. Olmedo-Monfil V, Duran-Figueroa N, Arteaga-Vazquez M, Demesa-Arevalo E, Autran D, Grimanelli D, Slotkin RK, Martienssen RA, Vielle-Calzada JP, (2010) Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464: 628-632
34. Pikaard CS, Haag JR, Ream T, Wierzbicki AT, (2008) Roles of RNA polymerase IV in gene silencing. Trends Plant Sci 13: 390-397
35. Pikaard CS, Haag JR, Pontes OM, Blevins T, Cocklin R, (2012) A transcription fork model for Pol IV and Pol V-dependent RNA-directed DNA methylation. Cold Spring Harb Symp Quant Biol 77: 205-212
36. 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
37. Pontier D, Picart C, Roudier F, Garcia D, Lahmy S, Azevedo J, Alart E, Laudie M, Karlowski WM, Cooke R, Colot V, Voinnet O, Lagrange T, (2012) NERD, a plant-specific GW protein, defines an additional RNAi-dependent chromatin-based pathway in Arabidopsis. Mol Cell 48: 121-132
38. Qi Y, He X, Wang XJ, Kohany O, Jurka J, Hannon GJ, (2006) Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature 443: 1008-1012
39. Rivas FV, Tolia NH, Song JJ, Aragon JP, Liu J, Hannon GJ, Joshua-Tor L, (2005) Purified Argonaute 2 and an siRNA form recombinant human RISC. Nat Struct Mol Biol 12: 340-349
40. Saleh A, Alvarez-Venegas R, Avramova Z, (2008) An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants. Nat Protoc 3: 1018-1025
41. Song JJ, Smith SK, Hannon GJ, Joshua-Tor L, (2004) Crystal structure of Argonaute and its implications for RISC slicer activity. Science 305: 1434-1437
42. Stroud H, Greenberg MV, Feng S, Bernatavichute YV, Jacobsen SE, (2013) Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152: 352-364
43. Tolia NH, Joshua-Tor L, (2007) Slicer and the argonautes. Nat Chem Biol 3: 36-43
44. Vannini A, Cramer P, (2012) Conservation between the RNA polymerase I, II, and III transcription initiation machineries. Mol Cell 45: 439-446
45. Wang Y, Juranek S, Li H, Sheng G, Tuschl T, Patel DJ, (2008) Structure of an argonaute silencing complex with a seed-containing guide DNA and target RNA duplex. Nature 456: 921-926
46. Wei W, Ba Z, Gao M, Wu Y, Ma Y, Amiard S, White CI, Rendtlew Danielsen JM, Yang YG, Qi Y, (2012) A role for small RNAs in DNA double-strand break repair. Cell 149: 101-112
47. Wierzbicki AT, Haag JR, Pikaard CS, (2008) Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135: 635-648
48. Wierzbicki AT, Ream TS, Haag JR, Pikaard CS, (2009) RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat Genet 41: 630-634
49. Wu L, Mao L, Qi Y, (2012) Roles of dicer-like and argonaute proteins in TAS-derived small interfering RNA-triggered DNA methylation. Plant Physiol 160: 990-999
50. Yan KS, Yan S, Farooq A, Han A, Zeng L, Zhou MM, (2003) Structure and conserved RNA binding of the PAZ domain. Nature 426: 468-474
51. Zhang X, Henderson IR, Lu C, Green PJ, Jacobsen SE, (2007) Role of RNA polymerase IV in plant small RNA metabolism. Proc Natl Acad Sci USA 104: 4536-4541
52. Zheng X, Zhu J, Kapoor A, Zhu JK, (2007) Role of Arabidopsis AGO6 in siRNA accumulation, DNA methylation and transcriptional gene silencing. EMBO J 26: 1691-1701
53. 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
54. Zhang H, Zhu JK, (2011) RNA-directed DNA methylation. Curr Opin Plant Biol 14: 142-147
55. Zhang H, Ma ZY, Zeng L, Tanaka K, Zhang CJ, Ma J, Bai G, Wang P, Zhang SW, Liu ZW, Cai T, Tang K, Liu R, Shi X, He XJ, Zhu JK, (2013) DTF1 is a core component of RNA-directed DNA methylation and may assist in the recruitment of Pol IV. Proc Natl Acad Sci USA 110: 8290-8295
56. Zhang H, Tang K, Qian W, Duan CG, Wang B, Zhang H, Wang P, Zhu X, Lang Z, Yang Y, Zhu JK, (2014) An Rrp6-like protein positively regulates noncoding RNA levels and DNA methylation in Arabidopsis. Mol Cell 54: 418-430
57. Zhong X, Du J, Hale CJ, Gallego-Bartolome J, Feng S, Vashisht AA, Chory J, Wohlschlegel JA, Patel DJ, Jacobsen SE, (2014) Molecular mechanism of action of plant DRM de novo DNA methyltransferases. Cell 157: 1050-1060
58. Zhu H, Hu F, Wang R, Zhou X, Sze SH, Liou LW, Barefoot A, Dickman M, Zhang X, (2011) Arabidopsis Argonaute 10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 145: 242-256
59. Zilberman D, Cao X, Jacobsen SE, (2003) ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299: 716-719