Viroid-induced symptoms in Nicotiana benthamiana plants are dependent on RDR6 activity

Plant Physiology

Volumn 148, Issue 1, 2008, Pages 414-423

  Gómez, Gustavo ^a   Martínez, Germán ^a   Pallás, Vicente ^a  

^a Ciudad Politécnica de la Innovación   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

HOP STUNT VIROID; HUMULUS; NICOTIANA BENTHAMIANA; VIROIDS;

VEGETABLE PROTEIN;

ARTICLE; COLD; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; RNA INTERFERENCE; TOBACCO; VIROID;

COLD; HOST-PATHOGEN INTERACTIONS; PLANT DISEASES; PLANT PROTEINS; RNA INTERFERENCE; TOBACCO; VIROIDS;

EID: 55549113227     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.108.120808     Document Type: Article

References (60)

1. Adenot X, Elmayan T, Lauressergues D, Boutet S, Bouché N, Gasciolli V, Vaucheret H (2006) DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr Biol 16: 927-932
2. Allen E, Xie Z, Gustafson AM, Carrington JC (2005) MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121: 207-221
3. Baulcombe DC (2002) RNA silencing. Curr Biol 12: 82-84
4. Brodersen P, Voinnet O (2006) The diversity of RNA silencing pathways in plants. Trends Genet 22: 268-280
5. Carbonell A, Martínez de Alba AE, Flores R, Gago S (2008) Double-stranded RNA interferes in a sequence-specific manner with the infection of representative members of the two viroid families. Virology 371: 44-53
6. Chapman EJ, Carrington JC (2007) Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8: 884-896
7. Chellappan P, Vanitharani R, Ogbe F, Fauquet CM (2005) Effect of temperature on geminivirus-induced RNA silencing in plants. Plant Physiol 138: 1828-1841
8. Conejero V (2003) Viroids and gene silencing. In A Hadidi, R Flores, JW Randles, JS Semancik, eds, Viroids. CSIRO Publishing, Collingwood, Australia, pp 67-70
9. Dalmay T, Hamilton A, Rudd S, Angell S, Baulcombe DC (2000) An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell 101: 543-553
10. Daròs JA, Elena SF, Flores R (2006) Viroids: an Ariadne's thread into the RNA labyrinth. EMBO Rep 7: 593-598
11. Daròs JA, Flores R (2002) A chloroplast protein binds a viroid RNA in vivo and facilitates its hammerhead-mediated self-cleavage. EMBO J 21: 749-759
12. Diener TO (1971) Potato spindle tuber "virus": replicating low molecular weight RNA. Virology 45: 411-428
13. Diener TO (1999) Viroids and the nature of viroid diseases. Arch Virol 15: 203-220
14. Diener TO, Smith D, Hammond R, Albanese G, La Rosa R, Davino M (1988) Citrus B viroid identified as a strain of hop stunt viroid. Plant Dis 72: 691-693
15. Ding B, Itaya A (2007) Viroid: a useful model for studying the basic principles of infection and RNA biology. Mol Plant Microbe Interact 20: 7-20
16. Ding SW, Voinnet O (2007) Antiviral immunity directed by small RNAs. Cell 130: 413-426
17. Flores R, Delgado S, Gas ME, Carbonell A, Molina D, Gago S, de la Peña M (2004) Viroids: the minimal non-coding RNAs with autonomous replication. FEBS Lett 567: 42-48
18. Flores R, Hernández C, Martínez de Alba AE, Daròs JA, Di Serio F (2005) Viroids and viroid-host interactions. Annu Rev Phytopathol 43: 117-139
19. Flores R, Pallás V (2006) Viroids. In JA Khan, J Dijkstra, eds, Handbook of Plant Virology. Haworth Press, New York, pp 93-104
20. Gómez G, Pallás V (2001) Identification of an in vitro ribonucleoprotein complex between a viroid RNA and a phloem protein from cucumber plants. Mol Plant Microbe Interact 14: 910-913
21. Gómez G, Pallás V (2004) A long-distance translocatable phloem protein from cucumber forms a ribonucleoprotein complex in vivo with Hop stunt viroid RNA. J Virol 78: 10104-10110
22. Gómez G, Pallás V (2006) Hop stunt viroid is processed and translocated in transgenic N. benthamiana plants. Mol Plant Pathol 7: 511-517
23. Gómez G, Pallás V (2007a) Mature monomeric forms of Hop stunt viroid resist RNA silencing in transgenic plants. Plant J 51: 1041-1049
24. Gómez G, Pallás V (2007b) A peptide derived from a single-modified viroid-RNA can be used as an "in vivo" nucleolar marker. J Virol Methods 144: 169-171
25. Gómez G, Torres H, Pallás V (2005) Identification of translocatable RNA-binding phloem proteins from melon, potential components of the longdistance RNA transport system. Plant J 41: 107-116
26. Gora A, Candresse T, Zagorski W (1996) Use of intramolecular chimeras to map molecular determinants of symptom severity of Potato spindle tuber viroid. Arch Virol 141: 2045-2055
27. Gruner R, Fels A, Qu F, Zimmat R, Steger G, Riesner D (1995) Interdependence of pathogenicity and replicability with Potato spindle tuber viroid. Virology 209: 60-69
28. Hamilton CM, Frary A, Lewis C, Tanksley SD (1996) Stable transfer of intact high molecular weight DNA into plant chromosomes. Proc Natl Acad Sci USA 93: 9975-9979
29. Himber C, Dunoyer P, Moissiard G, Ritzenthaler C, Voinnet O (2003) Transitivity-dependent and -independent cell-to-cell movement of RNA silencing. EMBO J 22: 4523-4533
30. Hull R (2002) Virus movement through the plant. In Matthews' Plant Virology, Ed 4. Academic Press, San Diego
31. Itaya A, Folimonov A, Matsuda Y, Nelson RS, Ding B (2001) Potato spindle tuber viroid as inducer of RNA silencing in infected tomato. Mol Plant Microbe Interact 14: 1332-1334
32. Itaya A, Zhong X, Bundschuh R, Qi Y, Wang Y, Takeda R, Harris AR, Molina C, Nelson RS, Ding B (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
33. Llave C, Kasschau KD, Rector MA, Carrington JC (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14: 1605-1619
34. Markarian N, Li HW, Ding SW, Semancik JS (2004) RNA silencing as related to viroid induced symptom expression. Arch Virol 149: 397-406
35. Martín R, Arenas C, Daròs JA, Covarrubias A, Reyes JL, Chua N (2007) Characterization of small RNAs derived from Citrus exocortis viroid in infected tomato plants. Virology 367: 135-146
36. Martinez G, Pallás V, Gómez G (2008) Analysis of the symptoms developed in N. benthamiana plants expressing dimeric forms of the Hop stunt viroid. J Plant Pathol 90: 121-124
37. Martínez de Alba AE, Flores R, Hernández C (2002) Two chloroplastic viroids induce the accumulation of the small RNAs associated with post-transcriptional gene silencing. J Virol 76: 13094-13096
38. Matoušek J, Kozlová P, Orctová L, Schmitz A, Pesina K, Bannach O, Diermann N, Steger G, Riesner D (2007) Accumulation of viroid-specific small RNAs and increase in nucleolytic activities linked to viroid-caused pathogenesis. Biol Chem 388: 1-13
39. Mourrain P, Beclin C, Elmayan T, Feuerbach F, Godon C, Morel JB, Jouette D, Lacombe AM, Nikic S, Picault N, et al (2000) Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101: 533-542
40. Owens RA, Blackburn M, Ding B (2001) Possible involvement of the phloem lectin in long-distance viroid movement. Mol Plant Microbe Interact 14: 905-909
41. Pallás V, Navarro A, Flores R (1987) Isolation of a viroid-like RNA from Hop different to HSVd. J Gen Virol 68: 3201-3205
42. Papaefthimiou I, Hamilton AJ, Denti MA, Baulcombe DC, Tsagris M, Tabler M (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
43. Peragine A, Yoshikawa M, Wu G, Albrecht HL, Poethig RS (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
44. Qu F, Ye XH, Hou GC, Sato S, Clemente TE, Morris TJ (2005) RDR6 has a broad-spectrum but temperature-dependent antiviral defense role in N. benthamiana. J Virol 79: 15209-15217
45. Remington DL, Vision TJ, Guilfoyle TJ, Reed JW (2004) Contrasting modes of diversification in the Aux/IAA and ARF gene families. Plant Physiol 135: 1738-1752
46. Rodio ME, Delgado S, Flores R, Di Serio F (2006) Variants of Peach latent mosaic viroid inducing peach calico: uneven distribution in infected plants and requirements of the insertion containing the pathogenicity determinant. J Gen Virol 87: 231-240
47. Sano T, Matsuura Y (2004) Accumulation of short interfering RNAs characteristics of RNA silencing precedes recovery of tomato plants from severe symptoms of Potato spindle tuber viroid infection. J Gen Plant Pathol 70: 50-53
48. Schnölzer M, Haas B, Ramm K, Hofmann H, Sänger HL (1985) Correlation between structure and pathogenicity of Potato spindle tuber viroid (PSTV). EMBO J 4: 2181-2190
49. Schwach F, Vaistij FE, Jones L, Baulcombe DC (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
50. Shikata E (1990) New viroids from Japan. Semin Virol 1: 107-115
51. Skoric D, Conerly M, Szychowski JA, Semancik JS (2001) CEVd-induced symptom modification as a response to a host-specific temperature-sensitive reaction. Virology 280: 115-123
52. Szittya G, Silhavy D, Molnar A, Havelda Z, Lovas A, Lakatos L, Banfalvi Z, Burgyan J (2003) Low temperature inhibits RNA silencing-mediated defence by the control of siRNA generation. EMBO J 22: 633-640
53. Tabler M, Tsagris M (2004) Viroids: petite RNA pathogens with distinguished talents. Trends Plant Sci 9: 339-348
54. Vaistij FE, Jones L, Baulcombe DC (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
55. Vance V, Vaucheret H (2001) RNA silencing in plants: defense and counterdefense. Science 292: 2277-2280
56. Vaucheret H (2006) Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev 20: 759-771
57. Vazquez F, Vaucheret H, Rajagopalan R, Lepers C, Gasciolli V, Mallory AC, Hilbert JL, Bartel DP, Crété P (2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol Cell 16: 69-79
58. Vogt U, Pelissier T, Putz A, Razvi F, Fischer R, Wassenegger M (2004) Viroid-induced RNA silencing of GFP-viroid fusion transgenes does not induce extensive spreading of methylation or transitive silencing. Plant J 38: 107-118
59. Wang MB, Bian XY, Wu LM, Liu LX, Smith NA, Isenegger D, Wu RM, Masuta C, Vance VB, Watson JM, et al (2004) On the role of RNA silencing in the pathogenicity and evolution of viroids and viral satellites. Proc Natl Acad Sci USA 101: 3275-3280
60. Xu L, Yang L, Pi L, Liu Q, Ling Q, Wang H, Poethig RS, Huang H (2006) Genetic interaction between the AS1-AS2 and RDR6-SGS3-AGO7 pathways for leaf morphogenesis. Plant Cell Physiol 47: 853-863