DRD1-Pol V-dependent self-silencing of an exogenous silencer restricts the non-cell autonomous silencing of an endogenous target gene

Plant Journal

Volumn 68, Issue 4, 2011, Pages 633-645

  Dong, Li ^a   Liu, Meng ^a   Fang, Yuan Yuan ^a   Zhao, Jian Hua ^a   He, Xiang Feng ^a   Ying, Xiao Bao ^a   Zhang, Yi Yue ^a   Xie, Qi ^a   Chua, Nam Hai ^b   Guo, Hui Shan ^a  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

exo IR; methylation spreading; non cell autonomous silencing; post transcriptional gene silencing; transcriptional gene silencing

Indexed keywords

DOUBLE-STRANDED RNA; ENDOGENOUS TARGET GENES; EXO-IR; GENERATED FUNCTION; MOBILE SIGNALS; NON-CELL AUTONOMOUS SILENCING; NUCLEAR PROTEINS; PATHWAY COMPONENTS; POST-TRANSCRIPTIONAL GENE SILENCING; PROTEIN-CODING GENES; PROTEIN-ENCODING GENES; SIGNAL SPREADING; SMALL INTERFERING RNA; TARGET CELLS; TRANSCRIPTIONAL GENE SILENCING; TRANSGENE;

ALKYLATION; GENE ENCODING; GENETIC ENGINEERING; METHYLATION; PLANTS (BOTANY); PROTEINS;

CELLS;

ARABIDOPSIS PROTEIN; DNA DIRECTED RNA POLYMERASE; DOUBLE STRANDED RNA; DRD1 PROTEIN, ARABIDOPSIS; PLANT RNA; RNA POLYMERASE V, ARABIDOPSIS; SMALL INTERFERING RNA;

ARABIDOPSIS; ARTICLE; DNA METHYLATION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; MUTATION; SEQUENCE ANALYSIS; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA METHYLATION; DNA-DIRECTED RNA POLYMERASES; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; MUTATION; PLANTS, GENETICALLY MODIFIED; RNA, DOUBLE-STRANDED; RNA, PLANT; RNA, SMALL INTERFERING; SEQUENCE ANALYSIS, RNA;

EID: 80855130737     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04714.x     Document Type: Article

References (77)

1. Allen, E., Xie, Z., Gustafson, A.M., and, Carrington, J.C., (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell, 121, 207-221. (Pubitemid 40546389)
2. Alonso, J.M., Stepanova, A.N., Leisse, T.J., et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653-657. (Pubitemid 36927950)
3. Bartel, D.P., (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281-297.
4. Baulcombe, D., (2004) RNA silencing in plants. Nature, 431, 356-363. (Pubitemid 39265676)
5. Baulcombe, D., (2005) RNA silencing. Trends Biochem. Sci. 30, 290-293. (Pubitemid 40799045)
6. Bouche, N., Lauressergues, D., Gasciolli, V., and, Vaucheret, H., (2006) An antagonistic function for Arabidopsis DCL2 in development and a new function for DCL4 in generating viral siRNAs. EMBO J. 25, 3347-3356. (Pubitemid 44141792)
7. Brodersen, P., Sakvarelidze-Achard, L., Bruun-Rasmussen, M., Dunoyer, P., Yamamoto, Y.Y., Sieburth, L., and, Voinnet, O., (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science, 320, 1185-1190. (Pubitemid 351929501)
8. Cao, X., and, Jacobsen, S.E., (2002) Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr. Biol. 12, 1138-1144. (Pubitemid 34766938)
9. Chan, S.W., Henderson, I.R., Zhang, X., Shah, G., Chien, J.S., and, Jacobsen, S.E., (2006) RNAi, DRD1, and histone methylation actively target developmentally important non-CG DNA methylation in Arabidopsis. PLoS Genet. 2, e83.
10. Chinnusamy, V., and, Zhu, J.K., (2009) RNA-directed DNA methylation and demethylation in plants. Sci. China C, Life Sci. 52, 331-343.
11. Daxinger, L., Kanno, T., and, Matzke, M., (2008) Pol V transcribes to silence. Cell, 135, 592-594.
12. Daxinger, L., Kanno, T., Bucher, E., van, W.J., Naumann, U., Matzke, A.J., and, Matzke, M., (2009) A stepwise pathway for biogenesis of 24-nt secondary siRNAs and spreading of DNA methylation. EMBO J. 28, 48-57.
13. Deleris, A., Gallego-Bartolome, J., Bao, J., Kasschau, K.D., Carrington, J.C., and, Voinnet, O., (2006) Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science, 313, 68-71. (Pubitemid 44051252)
14. Dunoyer, P., and, Voinnet, O., (2008) Mixing and matching: the essence of plant systemic silencing? Trends Genet. 24, 151-154.
15. Dunoyer, P., Himber, C., and, Voinnet, O., (2005) DICER-LIKE 4 is required for RNA interference and produces the 21-nucleotide small interfering RNA component of the plant cell-to-cell silencing signal. Nat. Genet. 37, 1356-1360. (Pubitemid 41722192)
16. Dunoyer, P., Himber, C., Ruiz-Ferrer, V., Alioua, A., and, Voinnet, O., (2007) Intra- and intercellular RNA interference in Arabidopsis thaliana requires components of the microRNA and heterochromatic silencing pathways. Nat. Genet. 39, 848-856. (Pubitemid 47014501)
17. Dunoyer, P., Brosnan, C.A., Schott, G., Wang, Y., Jay, F., Alioua, A., Himber, C., and, Voinnet, O., (2010a) An endogenous, systemic RNAi pathway in plants. EMBO J. 29, 1699-1712.
18. Dunoyer, P., Schott, G., Himber, C., Meyer, D., Takeda, A., Carrington, J.C., and, Voinnet, O., (2010b) Small RNA duplexes function as mobile silencing signals between plant cells. Science, 328, 912-916.
19. Eamens, A., Vaistij, F.E., and, Jones, L., (2008) NRPD1a and NRPD1b are required to maintain post-transcriptional RNA silencing and RNA-directed DNA methylation in Arabidopsis. Plant J. 55, 596-606.
20. Elmayan, T., Adenot, X., Gissot, L., Lauressergues, D., Gy, I., and, Vaucheret, H., (2009) A neomorphic sgs3 allele stabilizing miRNA cleavage products reveals that SGS3 acts as a homodimer. FEBS J. 276, 835-844.
21. Fukunaga, R., and, Doudna, J.A., (2009) dsRNA with 5′ overhangs contributes to endogenous and antiviral RNA silencing pathways in plants. EMBO J. 28, 545-555.
22. Fusaro, A.F., Matthew, L., Smith, N.A., et al. (2006) RNA interference-inducing hairpin RNAs in plants act through the viral defence pathway. EMBO Rep. 7, 1168-1175. (Pubitemid 44660575)
23. Gao, Z., Liu, H.L., Daxinger, L., et al. (2010) An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation. Nature, 465, 106-109.
24. Gasciolli, V., Mallory, A.C., Bartel, D.P., and, Vaucheret, H., (2005) Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr. Biol. 15, 1494-1500. (Pubitemid 41187489)
25. Guo, H.S., Fei, J.F., Xie, Q., and, Chua, N.H., (2003) A chemical-regulated inducible RNAi system in plants. Plant J. 34, 383-392. (Pubitemid 36579862)
26. Haag, J.R., Pontes, O., and, Pikaard, C.S., (2009) Metal A and metal B sites of nuclear RNA polymerases Pol IV and Pol V are required for siRNA-dependent DNA methylation and gene silencing. PLoS One, 4, e4110.
27. He, X.J., Hsu, Y.F., Pontes, O., Zhu, J., Lu, J., Bressan, R.A., Pikaard, C., Wang, C.S., and, Zhu, J.K., (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.
28. Heo, I., and, Kim, V.N., (2009) Regulating the regulators: posttranslational modifications of RNA silencing factors. Cell, 139, 28-31.
29. Herr, A.J., Jensen, M.B., Dalmay, T., and, Baulcombe, D.C., (2005) RNA polymerase IV directs silencing of endogenous DNA. Science, 308, 118-120. (Pubitemid 40471011)
30. Hetzl, J., Foerster, A.M., Raidl, G., and, Mittelsten, S.O., (2007) CyMATE: a new tool for methylation analysis of plant genomic DNA after bisulphite sequencing. Plant J. 51, 526-536. (Pubitemid 47106545)
31. Himber, C., Dunoyer, P., Moissiard, G., Ritzenthaler, C., and, Voinnet, O., (2003) Transitivity-dependent and -independent cell-to-cell movement of RNA silencing. EMBO J. 22, 4523-4533. (Pubitemid 37087205)
32. Huettel, B., Kanno, T., Daxinger, L., Aufsatz, W., Matzke, A.J., and, Matzke, M., (2006) Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. EMBO J. 25, 2828-2836. (Pubitemid 43980389)
33. Huettel, B., Kanno, T., Daxinger, L., Bucher, E., van, W.J., Matzke, A.J., and, Matzke, M., (2007) RNA-directed DNA methylation mediated by DRD1 and Pol IVb: a versatile pathway for transcriptional gene silencing in plants. Biochim. Biophys. Acta 1769, 358-374. (Pubitemid 46855948)
34. Jones, L., Hamilton, A.J., Voinnet, O., Thomas, C.L., Maule, A.J., and, Baulcombe, D.C., (1999) RNA-DNA interactions and DNA methylation in post-transcriptional gene silencing. Plant Cell, 11, 2291-2301. (Pubitemid 30031376)
35. Kanno, T., Mette, M.F., Kreil, D.P., Aufsatz, W., Matzke, M., and, Matzke, A.J., (2004) Involvement of putative SNF2 chromatin remodeling protein DRD1 in RNA-directed DNA methylation. Curr. Biol. 14, 801-805. (Pubitemid 38583716)
36. Kanno, T., Aufsatz, W., Jaligot, E., Mette, M.F., Matzke, M., and, Matzke, A.J., (2005) A SNF2-like protein facilitates dynamic control of DNA methylation. EMBO Rep. 6, 649-655.
37. Kanno, T., Bucher, E., Daxinger, L., Huettel, B., Bohmdorfer, G., Gregor, W., Kreil, D.P., Matzke, M., and, Matzke, A.J., (2008) A structural- maintenance-of-chromosomes hinge domain-containing protein is required for RNA-directed DNA methylation. Nat. Genet. 40, 670-675. (Pubitemid 351601208)
38. Klahre, U., Crete, P., Leuenberger, S.A., Iglesias, V.A., and, Meins, F.J., (2002) High molecular weight RNAs and small interfering RNAs induce systemic posttranscriptional gene silencing in plants. Proc. Natl Acad. Sci. USA 99, 11981-11986. (Pubitemid 34994510)
39. Lahmy, S., Pontier, D., Cavel, E., Vega, D., El-Shami, M., Kanno, T., and, Lagrange, T., (2009) PolV(PolIVb) function in RNA-directed DNA methylation requires the conserved active site and an additional plant-specific subunit. Proc. Natl Acad. Sci. USA 106, 941-946.
40. Li, C.F., Pontes, O., El-Shami, M., Henderson, I.R., Bernatavichute, Y.V., Chan, S.W., Lagrange, T., Pikaard, C.S., and, Jacobsen, S.E., (2006) An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell, 126, 93-106.
41. Matzke, M.A., and, Birchler, J.A., (2005) RNAi-mediated pathways in the nucleus. Nat. Rev. Genet. 6, 24-35. (Pubitemid 39657895)
42. Matzke, M., Aufsatz, W., Kanno, T., Daxinger, L., Papp, I., Mette, M.F., and, Matzke, A.J., (2004) Genetic analysis of RNA-mediated transcriptional gene silencing. Biochim. Biophys. Acta 1677, 129-141. (Pubitemid 38327097)
43. Matzke, M., Kanno, T., Huettel, B., Daxinger, L., and, Matzke, A.J., (2007) Targets of RNA-directed DNA methylation. Curr. Opin. Plant Biol. 10, 512-519. (Pubitemid 47503875)
44. Matzke, M., Kanno, T., Daxinger, L., Huettel, B., and, Matzke, A.J., (2009) RNA-mediated chromatin-based silencing in plants. Curr. Opin. Cell Biol. 21, 367-376.
45. Meister, G., and, Tuschl, T., (2004) Mechanisms of gene silencing by double-stranded RNA. Nature, 431, 343-349. (Pubitemid 39265674)
46. Molnar, A., Melnyk, C.W., Bassett, A., Hardcastle, T.J., Dunn, R., and, Baulcombe, D.C.,. (2010). Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science, 328, 872-875.
47. Mosher, R.A., Schwach, F., Studholme, D., and, Baulcombe, D.C., (2008) PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis. Proc. Natl Acad. Sci. USA 105, 3145-3150. (Pubitemid 351723682)
48. Mourrain, P., Beclin, C., Elmayan, T., et al. (2000) Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell, 101, 533-542.
49. Onodera, Y., Haag, J.R., Ream, T., Nunes, P.C., Pontes, O., and, Pikaard, C.S., (2005) Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell, 120, 613-622. (Pubitemid 40343074)
50. Palauqui, J.C., Elmayan, T., Pollien, J.M., and, Vaucheret, H., (1997) Systemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J. 16, 4738-4745. (Pubitemid 27326611)
51. Parizotto, E.A., Dunoyer, P., Rahm, N., Himber, C., and, Voinnet, O., (2004) In vivo investigation of the transcription, processing, endonucleolytic activity, and functional relevance of the spatial distribution of a plant miRNA. Genes Dev. 18, 2237-2242. (Pubitemid 39209571)
52. Peragine, A., Yoshikawa, M., Wu, G., Albrecht, H.L., and, Poethig, R.S., (2004) SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev. 18, 2368-2379. (Pubitemid 39304684)
53. Pikaard, C.S., Haag, J.R., Ream, T., and, Wierzbicki, A.T., (2008) Roles of RNA polymerase IV in gene silencing. Trends Plant Sci. 13, 390-397.
54. Preuss, S.B., Costa-Nunes, P., Tucker, S., et al. (2008) Multimegabase silencing in nucleolar dominance involves siRNA-directed DNA methylation and specific methylcytosine-binding proteins. Mol. Cell, 32, 673-684.
55. Schwach, F., Vaistij, F.E., Jones, L., and, Baulcombe, D.C., (2005) An RNA-dependent RNA polymerase prevents meristem invasion by potato virus X and is required for the activity but not the production of a systemic silencing signal. Plant Physiol. 138, 1842-1852. (Pubitemid 43733532)
56. Sessions, A., Burke, E., Presting, G., et al. (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell, 14, 2985-2994. (Pubitemid 36029127)
57. Smith, L.M., Pontes, O., Searle, I., Yelina, N., Yousafzai, F.K., Herr, A.J., Pikaard, C.S., and, Baulcombe, D.C., (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. (Pubitemid 47025373)
58. Vaistij, F.E., Jones, L., and, Baulcombe, D.C., (2002) Spreading of RNA targeting and DNA methylation in RNA silencing requires transcription of the target gene and a putative RNA-dependent RNA polymerase. Plant Cell, 14, 857-867. (Pubitemid 34519607)
59. Van, H.H., Bleys, A., and, Depicker, A., (2003) RNA target sequences promote spreading of RNA silencing. Plant Physiol. 131, 245-253. (Pubitemid 36141222)
60. Vaucheret, H., (2005) RNA polymerase IV and transcriptional silencing. Nat. Genet. 37, 659-660. (Pubitemid 41754878)
61. Vazquez, F., Vaucheret, H., Rajagopalan, R., Lepers, C., Gasciolli, V., Mallory, A.C., Hilbert, J.L., Bartel, D.P., and, Crete, P., (2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol. Cell, 16, 69-79. (Pubitemid 39330153)
62. Voinnet, O., (2005) Non-cell autonomous RNA silencing. FEBS Lett. 579, 5858-5871. (Pubitemid 41484131)
63. Voinnet, O., (2008) Post-transcriptional RNA silencing in plant-microbe interactions: a touch of robustness and versatility. Curr. Opin. Plant Biol. 11, 464-470.
64. Voinnet, O., and, Baulcombe, D.C., (1997) Systemic signalling in gene silencing. Nature, 389, 553.
65. Voinnet, O., Lederer, C., and, Baulcombe, D.C., (2000) A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell, 103, 157-167.
66. Wierzbicki, A.T., Haag, J.R., and, Pikaard, C.S., (2008) Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell, 135, 635-648.
67. Wierzbicki, A.T., Ream, T.S., Haag, J.R., and, Pikaard, C.S., (2009) RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat. Genet. 41, 630-634.
68. Xie, Z., Johansen, L.K., Gustafson, A.M., Kasschau, K.D., Lellis, A.D., Zilberman, D., Jacobsen, S.E., and, Carrington, J.C., (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2, E104.
69. Xie, Z., Allen, E., Wilken, A., and, Carrington, J.C., (2005) DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 102, 12984-12989. (Pubitemid 41279476)
70. Yoshikawa, M., Peragine, A., Park, M.Y., and, Poethig, R.S., (2005) A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev. 19, 2164-2175. (Pubitemid 41330318)
71. Zhang, X., Henderson, I.R., Lu, C., Green, P.J., and, Jacobsen, S.E., (2007) Role of RNA polymerase IV in plant small RNA metabolism. Proc. Natl Acad. Sci. USA 104, 4536-4541. (Pubitemid 47186260)
72. Zheng, X., Zhu, J., Kapoor, A., and, Zhu, J.K., (2007) Role of Arabidopsis AGO6 in siRNA accumulation, DNA methylation and transcriptional gene silencing. EMBO J. 26, 1691-1701. (Pubitemid 46480931)
73. Zheng, B., Wang, Z., Li, S., Yu, B., Liu, J.Y., and, 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.
74. Zilberman, D., and, Henikoff, S., (2005) Epigenetic inheritance in Arabidopsis: selective silence. Curr. Opin. Genet. Dev. 15, 557-562. (Pubitemid 41262413)
75. Zilberman, D., and, Henikoff, S., (2007) Genome-wide analysis of DNA methylation patterns. Development, 134, 3959-3965. (Pubitemid 350269413)
76. Zilberman, D., Cao, X., Johansen, L.K., Xie, Z., Carrington, J.C., and, Jacobsen, S.E., (2004) Role of Arabidopsis ARGONAUTE4 in RNA-directed DNA methylation triggered by inverted repeats. Curr. Biol. 14, 1214-1220. (Pubitemid 38893986)
77. Zuo, J., and, Chua, N.H., (2000) Chemical-inducible systems for regulated expression of plant genes. Curr. Opin. Biotechnol. 11, 146-151. (Pubitemid 30182307)