RNA-dependent RNA polymerase 6 delays accumulation and precludes meristem invasion of a viroid that replicates in the nucleus

Journal of Virology

Volumn 84, Issue 5, 2010, Pages 2477-2489

  Di Serio, Francesco ^a   De Alba, Angel Emilio Martínez ^b,d   Navarro, Beatriz ^a   Gisel, Andreas ^c   Flores, Ricardo ^b  

^a INSTITUTE FOR SUSTAINABLE PLANT PROTECTION   (Italy)

^b Ciudad Politécnica de la Innovación   (Spain)

^c CNR   (Italy)

^d INSTITUT JEAN PIERRE BOURGIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC RNA; NUCLEOTIDE; RNA DIRECTED RNA POLYMERASE; RNA DIRECTED RNA POLYMERASE 6; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANGIOSPERM; ARTICLE; CELL INVASION; CELL NUCLEUS; CONTROLLED STUDY; DNA HYBRIDIZATION; GENE EXPRESSION; GENE MAPPING; GENE SEQUENCE; IN SITU HYBRIDIZATION; MERISTEM; NICOTIANA BENTHAMIANA; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT LEAF; POTATO SPINDLE TUBER; PRIORITY JOURNAL; RNA VIRUS; TRANSGENIC PLANT; VIROID; VIRUS ENTRY; VIRUS REPLICATION;

BASE SEQUENCE; ISOENZYMES; MERISTEM; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PHENOTYPE; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; RNA INTERFERENCE; RNA REPLICASE; RNA, SMALL INTERFERING; SEQUENCE ANALYSIS, DNA; TOBACCO; VIROIDS;

NICOTIANA BENTHAMIANA; POSPIVIROIDAE; POTATO SPINDLE TUBER VIROID; RNA VIRUSES; VIROIDS;

EID: 77649205597     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02336-09     Document Type: Article

References (90)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. Mol. Biol. 215:403-410.
2. Bernstein, E., A. A. Caudy, S. M. Hammond, and G. J. Hannon. 2001. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363-366.
3. Branch, A. D., B. J. Benenfeld, and H. D. Robertson. 1988. Evidence for a single rolling circle in the replication of potato spindle tuber viroid. Proc. Natl. Acad. Sci. U. S. A. 85:9128-9132.
4. Branch, A. D., and H. D. Robertson. 1984. A replication cycle for viroids and other small infectious RNAs. Science 223:450-455.
5. Carbonell, A., A. E. Martínez de Alba, R. Flores, and S. Gago. 2008. Doubl-estranded RNA interferes in a sequence-specific manner with infection of representative members of the two viroid families. Virology 371:44-53.
6. Dalmay, T., A. Hamilton, S. Rudd, S. Angell, and D. C. Baulcombe. 2000. An RNA-dependent RNA polymerase gene in Arabidopsis is required for post-transcriptional gene silencing mediated by a transgene but not by a virus. Cell 101:543-553.
7. Dalmay, T., L. Rubino, J. Burgyan, A. Kollár, and M. Russo. 1993. Functional analysis of cymbidium ringspot virus genome. Virology 194:697-704.
8. Daròs, J. A., and R. Flores. 2002. A chloroplast protein binds a viroid RNA in vivo and facilitates its hammerhead-mediated self-cleavage. EMBO J. 21:749-759.
9. Daròs, J. A., J. F. Marcos, C. Hernández, and R. Flores. 1994. Replication of avocado sunblotch viroid: Evidence for a symmetric pathway with two rolling circles and hammerhead ribozyme processing. Proc. Natl. Acad. Sci. U. S. A. 91:12813-12817.
10. Deleris, A., J. Gallego-Bartolomé, J. Bao, K. D. Kasschau, J. C. Carrington, and O. Voinnet. 2006. Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 313:68-71.
11. De Paoli, E., A. Dorantes-Acosta, J. Zhai, M. Accerbi, D.-H. Jeong, S. Park, B. C. Meyers, R. A. Jorgensen, and P. J. Green. 2009. Distinct extremely abundant siRNAs associated with cosuppression in petunia. RNA. 15:1965-1970.
12. Díaz-Pendón, J. A., and S. W. Ding. 2008. Direct and indirect roles of viral suppressors of RNA silencing in pathogenesis. Annu. Rev. Phytopathol. 46:303-326.
13. Díaz-Pendón, J. A., F. Li, W. X. Li, and S. W. Ding. 2007. Suppression of antiviral silencing by cucumber mosaic virus 2b protein in Arabidopsis is associated with drastically reduced accumulation of three classes of viral small interfering RNAs. Plant Cell 19:2053-2063.
14. Diener, T. O. 2003. Discovering viroids - a personal perspective. Nature Rev. Microbiol. 1:75-80.
15. Ding, B. 2009. The biology of viroid-host interactions. Annu. Rev. Phytopathol. 47:105-131.
16. Ding, B., and A. Itaya. 2007. Viroid: a useful model for studying the basic principles of infection and RNA biology. Mol. Plant Microbe Interact. 20:7-20.
17. Di Serio, F., A. Gisel, B. Navarro, S. Delgado, A. E. Martínez de Alba, G. Donvito, and R. Flores. 2009. Deep sequencing of the small RNAs derived from two symptomatic variants of a chloroplastic viroid: implications for their genesis and for pathogenesis. PLoS One 4:e7539.
18. Donaire, L., Y. Wang, D. Gonzalez-Ibeas, K. F. Mayer, M. A. Aranda, and C. Llave. 2009. Deep-sequencing of plant viral small RNAs reveals effective and widespread targeting of viral genomes. Virology 392:203-214.
19. Donaire, L., D. Barajas, B. Martínez-García, L. Martínez-Priego, I. Pagan, and C. Llave. 2008. Structural and genetic requirements for the biogenesis of tobacco rattle virus-derived small interfering RNAs. J. Virol. 82:5167-5177.
20. Fagard, M., and H. Vaucheret. 2000. Systemic silencing signal(s). Plant Mol. Biol. 43:285-293.
21. Feldstein, P. A., Y. Hu, and R. A. Owens. 1998. Precisely full length, circularizable, complementary RNA: an infectious form of potato spindle tuber viroid. Proc. Natl. Acad. Sci. U. S. A. 95:6560-6565.
22. Flores, R., C. Hernández, A. E. Martínez de Alba, J. A. Daròs, and F. Di Serio. 2005. Viroids and viroid-host interactions. Annu. Rev. Phytopathol. 43:117-139.
23. Flores, R., J. A. Daròs, and C. Hernández. 2000. The Avsunviroidae family: viroids with hammerhead ribozymes. Adv. Virus Res. 55:271-323.
24. Foster, T. M., T. J. Lough, S. J. Emerson, R. H. Lee, J. L. Bowman, R. L. Forster, and W. J. Lucas. 2002. A surveillance system regulates selective entry of RNA into the shoot apex. Plant Cell 14:1497-1508.
25. Fusaro, A. F., L. Matthew, N. A. Smith, S. J. Curtin, J. Dedic-Hagan, G. A. Ellacott, J. M. Watson, M. B. Wang, C. Brosnan, B. J. Carroll, and P. M. Waterhouse. 2006. RNA interference-inducing hairpin RNAs in plants act through the viral defence pathway. EMBO Rep. 7:1168-1175.
26. Gas, M. E., C. Hernández, R. Flores, and J. A. Daròs. 2007. Processing of nuclear viroids in vivo: an interplay between RNA conformations. PLoS Pathog. 3:e182.
27. Gómez, G., G. Martínez, and V. Pallás. 2009. Interplay between viroidinduced pathogenesis and RNA silencing pathways. Trends Plant Sci. 14: 264-269.
28. Gómez, G., G. Martínez, and V. Pallás. 2008. Viroid-induced symptoms in Nicotiana benthamiana plants are dependent on RDR6 activity. Plant Physiol. 148:414-423.
29. Gross, H. J., H. Domdey, C. Lossow, P. Jank, M. Raba, H. Alberty, and H. L. Sänger. 1978. Nucleotide sequence and secondary structure of potato spindle tuber viroid. Nature 273:203-208.
30. Hamilton, A. J., and D. C. Baulcombe. 1999. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950-952.
31. Hammond, S. M., E. Bernstein, D. Beach, and G. J. Hannon. 2000. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404:293-296.
32. Harders, J., N. Lukacs, M. Robert-Nicoud, J. M. Jovin, and D. Riesner. 1989. Imaging of viroids in nuclei from tomato leaf tissue by in situ hybridization and confocal laser scanning microscopy. EMBO J. 8:3941-3949.
33. Hernández, C., and R. Flores. 1992. Plus and minus RNAs of peach latent mosaic viroid self-cleave in vitro through hammerhead structures. Proc. Natl. Acad. Sci. U. S. A. 89:3711-3715.
34. Howell, M. D., N. Fahlgren, E. J. Chapman, J. S. Cumbie, C. M. Sullivan, S. A. Givan, K. D. Kasschau, and J. C. Carrington. 2007. Genome-wide analysis of the RNA-DEPENDENT RNA POLYMERASE6/DICERLIKE4 pathway in Arabidopsis reveals dependency on miRNA- and tasiRNA-directed targeting. Plant Cell 19:926-942.
35. Itaya, A., X. Zhong, R. Bundschuh, Y. Qi, Y. Wang, R. Takeda, A. R. Harris, C. Molina, R. S. Nelson, and B. Ding. 2007. A structured viroid RNA is substrate for Dicer-like cleavage to produce biologically active small RNAs but is resistant to RISC-mediated degradation. J. Virol. 81:2980-2994.
36. Itaya, A., A. Folimonov, Y. Matsuda, R. S. Nelson, and B. Ding. 2001. Potato spindle tuber viroid as inducer of RNA silencing in infected tomato. Mol. Plant Microbe. Interact. 14:1332-1334.
37. Jackson, D. P. 1992. In situ hybridization in plants, p. 163-174. In D. J. Bowles, S. J. Gurr, and M. J. McPherson (ed.), Molecular plant pathology: a practical approach. Oxford University Press, Oxford.
38. Kalantidis, K., H. T. Schumacher, T. Alexiadis, and J. M. Helm. 2008. RNA silencing movement in plants. Biol. Cell 100:13-26.
39. Keese, P., and R. H. Symons. 1985. Domains in viroids: evidence of intermolecular RNA rearrangements and their contribution to viroid evolution. Proc. Natl. Acad. Sci. U. S. A. 82:4582-4586.
40. Lindbo, J. A., L. Silva-Rosales, W. M. Proebsting, and W. G. Dougherty. 1993. Induction of a highly specific antiviral state in transgenic plants: implications for regulation of gene expression and virus resistance. Plant Cell 5:1749-1759.
41. Machida, S., N. Yamahata, H. Watanuki, R. A. Owens, and T. Sano. 2007. Successive accumulation of two size classes of viroid-specific small RNA in potato spindle tuber viroid-infected tomato plants. J. Gen. Virol. 88:3452-3457.
42. Margis, R., A. F. Fusaro, N. A. Smith, S. J. Curtin, J. M. Watson, E. J. Finnegan, and P. M. Waterhouse. 2006. The evolution and diversification of Dicers in plants. FEBS Lett. 580:2442-2450.
43. Markarian, N., H. W. Li, S. W. Ding, and J. S. Semancik. 2004. RNA silencing as related to viroid induced symptom expression. Arch. Virol. 149:397-406.
44. Martín, R., C. Arenas, J. A. Daròs, A. Covarrubias, J. L. Reyes, and N. H. Chua. 2007. Characterization of small RNAs derived from citrus exocortis viroid (CEVd) in infected tomato plants. Virology 367:135-146.
45. Martínez de Alba, A. E., R. Sagesser, M. Tabler, and M. Tsagris. 2003. A bromodomain-containing protein from tomato specifically binds potato spindle tuber viroid RNA in vitro and in vivo. J. Virol. 77:9685-9694.
46. Martínez de Alba, A. E., R. Flores, and C. Herná ndez. 2002. Two chloroplastic viroids induce the accumulation of the small RNAs associated with post-transcriptional gene silencing. J. Virol. 76:13094-13096.
47. Matousek, J., P. Kozlová, L. Orctová, A. Schmitz, K. Pesina, O. Bannach, N. Diermann, G. Steger, and D. Riesner. 2007. Accumulation of viroid-specific small RNAs and increase of nucleolytic activities linked to viroid-caused pathogenesis. Biol. Chem. 388:1-13.
48. Mi, S., T. Cai, Y. Hu, Y. Chen, E. Hodges, F. Ni, L. Wu, S. Li, H. Zhou, C. Long, S. Chen, G. J. Hannon, and Y. Qi. 2008. Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133:116-127.
49. Montgomery, T. A., M. D. Howell, J. T. Cuperus, D. Li, J. E. Hansen, A. L. Alexander, E. J. Chapman, N. Fahlgren, E. Allen, and J. C. Carrington. 2008. Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133:128-141.
50. Morel, J. B., C. Godon, P. Mourrain, C. Beclin, S. Boutet, F. Feuerbach, F. Proux, and H. Vaucheret. 2002. Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in posttranscriptional gene silencing and virus resistance. Plant Cell 14:629-639.
51. Mourrain, P., C. Beclin, T. Elmayan, F. Feuerbach, C. Godon, J. B. Morel, D. Jouette, A. M. Lacombe, S. Nikic, N. Picault, K. Remoue, M. Sanial, T. A. Vo, and H. Vaucheret. 2000. Arabidopsis SGS2 and SGS3 genes are required for post-transcriptional gene silencing and natural virus resistance. Cell 101: 533-542.
52. Navarro, B., V. Pantaleo, A. Gisel, S. Moxon, T. Dalmay, G. Bisztray, F. Di Serio, and J. Burgyán. 2009. Deep sequencing of viroid-derived small RNAs from grapevine provides new insights on the role of RNA silencing in plantviroid interaction. PLoS One 4:e7686.
53. Navarro, J. A., J. A. Daròs, and R. Flores. 1999. Complexes containing both polarity strands of avocado sunblotch viroid: Identification in chloroplasts and characterization. Virology 253:77-85.
54. Omarov, R. T., J. J. Cioperlik, and H. B. Sholthof. 2007. RNAi-associated ssRNA-specific ribonucleases in tombusvirus P19 mutant-infected plants and evidence for a discrete siRNA-containing effector complex. Proc. Natl. Acad. Sci. U. S. A. 104:1714-1719.
55. Owens, R. A. 2007. Potato spindle tuber viroid: The simplicity paradox resolved? Mol. Plant Pathol. 8:549-560.
56. Pak, J., and A. Fire. 2007. Distinct populations of primary and secondary effectors during RNAi in C. elegans. Science 315:241-244.
57. Palauqui, J. C., T. Elmayan, J. M. Pollien, and H. Vaucheret. 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.
58. Pantaleo, V., G. Szittya, and J. Burgyán. 2007. Molecular bases of viral RNA targeting by viral small interfering RNA-programmed RISC. J. Virol. 81: 3797-3806.
59. Papaefthimiou, I., A. J. Hamilton, M. A. Denti, D. C. Baulcombe, M. Tsagris, and M. Tabler. 2001. Replicating potato spindle tuber viroid RNA is accompanied by short RNA fragments that are characteristic of post-transcriptional gene silencing. Nucleic Acids Res. 29:2395-2400.
60. Qi, Y., A. M. Denli, and G. J. Hannon. 2005. Biochemical specialization within Arabidopsis RNA silencing pathways. Mol. Cell 19:421-428.
61. Qi, Y., T. Pelissier, A. Itaya, E. Hunt, M. Wassenegger, and B. Ding. 2004. Direct role of a viroid RNA motif in mediating directional RNA trafficking across a specific cellular boundary. Plant Cell 16:1741-1752.
62. Qi, Y., and B. Ding. 2003. Differential subnuclear localization of RNA strands of opposite polarity derived from an autonomously replicating viroid. Plant Cell 15:2566-2577.
63. Qi, Y., and B. Ding. 2003. Inhibition of cell growth and shoot development by a specific nucleotide sequence in a noncoding viroid RNA. Plant Cell 15:1360-1374.
64. Qi, Y., and B. Ding. 2002. Replication of potato spindle tuber viroid in cultured cells of tobacco and Nicotiana benthamiana: the role of specific nucleotides in determining replication levels for host adaptation. Virology 302:445-456.
65. Qu, F., X. Ye, and T. J. Morris. 2008. Arabidopsis DRB4, AGO1, AGO7, and RDR6 participate in a DCL4-initiated antiviral RNA silencing pathway negatively regulated by DCL1. Proc. Natl. Acad. Sci. U. S. A. 105:14732-14737.
66. Qu, F., X. Ye, G. Hou, S. Sato, T. E. Clemente, and T. J. Morris. 2005. RDR6 has a broad-spectrum but temperature-dependent antiviral defense role in Nicotiana benthamiana. J. Virol. 79:15209-15217.
67. Ramachandran, V., and X. M. Chen. 2008. Small RNA metabolism in Arabidopsis. Trends Plant Sci. 13:368-374.
68. Riesner, D., K. Henco, U. Rokohl, G. Klotz, A. K. Kleinschmidt, H. Domdey, P. Jank, H. J. Gross, and H. Sänger. 1979. Structure and structure formation of viroids. J. Mol. Biol. 133:85-115.
69. Rodio, M. E., S. Delgado, A. De Stradis, M. D. Gómez, R. Flores, and F. Di Serio. 2007. A viroid RNA with a specific structural motif inhibits chloroplast development. Plant Cell 19:3610-3616.
70. Schiebel, W., T. Pelissier, L. Riedel, S. Thalmeir, R. Schiebel, D. Kempe, F. Lottspeich, H. L. Sänger, and M. Wassenegger. 1998. Isolation of an RNA-Directed RNA polymerase-specific cDNA clone from tomato. Plant Cell 10:2087-2101.
71. Schiebel, W., B. Haas, S. Marinkovic, A. Klanner, and H. L. Sänger. 1993. RNA-directed RNA polymerase from tomato leaves. 1. Purification and physical-properties. J. Biol. Chem. 268:11851-11857.
72. Schnolzer, M., B. Haas, K. Ramm, H. Hofmann, and H. L. Sänger. 1985. Correlation between structure and pathogenicity of potato spindle tuber viroid (PSTV). EMBO J. 4:2181-2190.
73. Schwach, F., F. E. Vaistij, L. Jones, and D. C. Baulcombe. 2005. An RNAdependent 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.
74. Schwind, N., M. Zwiebel, A. Itaya, B. Ding, M. B. Wang, G. Krczal, and M. Wassenegger. 2009. RNAi-mediated resistance to potato spindle tuber viroid in transgenic tomato expressing a viroid hairpin RNA construct. Mol. Plant Pathol. 10:459-469.
75. Sijen, T., F. A. Steiner, K. L. Thijssen, and R. H. Plasterk. 2007. Secondary siRNAs result from unprimed RNA synthesis and form a distinct class. Science 315:244-247.
76. Singh, R. P. 2006. Reassessment of the presence of viroid species of the genus Pospiviroid in infected floral parts, using reverse transcription-polymerase chain reaction and infectivity assays. Can. J. Plant Pathol. 28:242-249.
77. St-Pierre, P., F. Hassen, D. Thompson, and J. P. Perreault. 2009. Characterization of the siRNAs associated with peach latent mosaic viroid infection. Virology 383:178-182.
78. Takeda, A., S. Iwasaki, T. Watanabe, M. Utsumi, and Watanabe, Y. 2008. The mechanism selecting the guide strand from small RNA duplexes is different among Argonaute proteins. Plant Cell Physiol. 49:493-500.
79. Takeda, A., M. Tsukuda, H. Mizumoto, K. Okamoto, M. Kaido, K. Mise, and T. Okuno. 2005. A plant RNA virus suppresses RNA silencing through viral RNA replication. EMBO J. 24:3147-3157.
80. Tournier, B., M. Tabler, and K. Kalantidis. 2006. Phloem flow strongly influences the systemic spread of silencing in GFP Nicotiana benthamiana plants. Plant J. 47:383-394.
81. Tsagris, E. M., A. E. Martínez de Alba, M. Gozmanova, and K. Kalantidis. 2008. Viroids. Cell Microbiol. 10:2168-2179.
82. Vaistij, F. E., and L. Jones. 2009. Compromised virus-induced gene silencing in RDR6-deficient plants. Plant Physiol. 149:1399-1407.
83. Voinnet, O. 2008. Use, tolerance and avoidance of amplified RNA silencing by plants. Trends Plant Sci. 13:317-328.
84. Voinnet, O., P. Vain, S. Angell, and D. C. Baulcombe. 1998. Systemic spread of sequence-specific transgene RNA degradation is initiated by localised introduction of ectopic promoterless DNA. Cell 95:177-187.
85. Wang, M. B., X. Y. Bian, L. M. Wu, L. X. Liu, N. A. Smith, D. Isenegger, R. M. Wu, C. Masuta, V. B. Vance, J. M. Watson, A. Rezaian, E. S. Dennis, and P. M. Waterhouse. 2004. On the role of RNA silencing in the pathogenicity and evolution of viroids and viral satellites. Proc. Natl. Acad. Sci. U. S. A. 101:3275-3280.
86. Wassenegger, M., and G. Krczal. 2006. Nomenclature and functions of RNA-directed RNA polymerases. Trends Plant Sci. 11:142-151.
87. Yang, S. J., S. A. Carter, A. B. Cole, N. H. Cheng, and R. S. Nelson. 2004. A natural variant of a host RNA-dependent RNA polymerase is associated with increased susceptibility to viruses by Nicotiana benthamiana. Proc. Natl. Acad. Sci. U. S. A. 101:6297-6302.
88. Yang, Z., Y. W. Ebright, B. Yu, and X. Chen. 2006. HEN1 recognizes 21-24 nt small RNA duplexes and deposits a methyl group onto the 2′ OH of the 3′ terminal nucleotide. Nucleic Acids Res. 34:667-675.
89. Zhu, Y., Y. Qi, Y. Xun, R. Owens, and B. Ding. 2002. Movement of potato spindle tuber viroid reveals regulatory points of phloem-mediated RNA traffic. Plant Physiol. 130:138-146.
90. Zhu, Y., L. Green, Y. M. Woo, R. Owens, and B. Ding. 2001. Cellular basis of potato spindle tuber viroid systemic movement. Virology 279:69-77.