Viroid pathogenicity: One process, many faces

Viruses

Volumn 1, Issue 2, 2009, Pages 298-316

  Owens, Robert A ^a   Hammond, Rosemarie W ^a  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Disease induction; RNA silencing; Viroid pathogenicity

Indexed keywords

EID: 73949106627     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v1020298     Document Type: Review

References (92)

1. Diener, T.O. Potato spindle tuber "virus" IV. A replicating, low molecular weight RNA. Virology 1971, 45, 411-428.
2. Gross, H.J.; Domdey, H.; Lossow, C.; Jank, P.; Raba, M.; Alberty, H.; Sänger, H-L. Nucleotide sequence and secondary structure of potato spindle tuber viroid. Nature 1978, 273, 203-208.
3. Dickson, E.; Robertson, H.D.; Niblett, C.L.; Horst, R.K.; Zaitlin, M. Minor differences between nucleotide sequences of mild and severe strains of potato spindle tuber viroid. Nature 1979, 277, 60-62.
4. Keese, P.; Symons, R.H. Domains in viroids: Evidence of intermolecular RNA rearrangements and their contribution to viroid evolution. Proc. Natl. Acad. Sci. USA 1985, 82, 4582-4586.
5. Schnölzer, M.; Haas, B.; Ramm, K.; Hofmann, H.; Sänger, H.-L. Correlation between structure and pathogenicity of potato spindle tuber viroid (PSTV). EMBO J. 1985, 4, 2181-2190.
6. Wang, M-B.; Bian, X.-Y.; Wu, L.-M.; Liu, L.-X.; Smith, N.A.; Isenegger, D.; Wu, R.-M.; Masuta, C.; Vance, V.B.; Watson, J.M.; Rezaian, A.; Dennis, E.S.; Waterhouse, P.M. On the role of RNA silencing in the pathogenicity and evolution of viroids and viral satellites. Proc. Natl. Acad. Sci. USA 2004, 101, 3275-3280.
7. Itaya, A.; Folimonov, A.; Matsuda, Y.; Nelson, R.S.; Ding, B. Potato spindle tuber viroid as inducer of RNA silencing in infected tomato. Mol. Plant-Microbe Interact. 2001, 14, 1332-1334
8. Markarian, N.; Li, H.W.; Ding, S.-W.; Semancik, J.S. RNA silencing as related to viroid induced symptom expression. Arch. Virol. 2004, 149, 397-406.
9. Martínez de Alba, A.E.; Flores, R.; Hernández, C. Two chloroplastic viroids induce the accumulation of the small RNAs associated with post-transcriptional gene silencing. J. Virol. 2002, 76, 13094-13096.
10. Matoušek, J.; Kozlová, P.; Orctová, L.; Schmitz, A.; Pesina, K.; Bannach, O.; Diermann, N.; Steger, G.; Riesner, D. Accumulation of viroid-specific small RNAs and increase in nucleolytic activities linked to viroid-caused pathogenesis. Biol. Chem. 2007, 388, 1-13.
11. Papaefthimiou, I.; Hamilton, A.J.; Denti, M.A.; Baulcombe, D.C.; Tsagris, M.; Tabler, M. Replicating potato spindle tuber viroid RNA is accompanied by short RNA fragments that are characteristic of post-transcriptional gene silencing. Nucleic Acids Res. 2001, 29, 2395-2400.
12. Daros, J.A.; Elena, S.F.; Flores, R. Viroids: An Ariadne's thread into the RNA labyrinth. EMBO Rep. 2006, 7, 593-588.
13. Ding, B.; Itaya, A. Viroid: A useful model for studying the basic principles of infection and RNA biology. Mol. Plant-Microbe Inter. 2007, 20, 7-20.
14. Flores, R.; Hernández, C.; Martinez de Alba, A.E.; Daròs, J.-A.; Di Serio, F. Viroids and viroidhost interactions. Annu. Rev. Phytopathol. 2005, 43, 4.1-4.23.
15. Tabler, M.; Tsagris, M. Viroids: petite RNA pathogens with distinguished talents. Trends Plant Sci. 2004, 9, 339-348.
16. Maniataki, E.; Tabler, M.; Tsagris, M. Viroid RNA systemic spread may depend on the interaction of a 71-nucleotide bulged hairpin with the host protein VIRP1. RNA 2003, 9, 346-354.
17. Visvader, J.E.; Symons, R.H. Eleven new sequence variants of citrus exocortis viroid and the correlation of sequence with pathogencity. Nucleic Acids Res. 1985, 13, 2907-2920.
18. Sano, T.; Candresse, T.; Hammond, R.W.; Diener, T.O.; Owens, R.A. Identification of multiple structural domains regulating viroid pathogenicity. Proc. Natl. Acad. Sci. USA 1992, 89, 10104-10108.
19. Reanwarakom, K.; Semancik, J.S. Regulation of pathogenicity in hop stunt viroid related group II citrus viroids. J. Gen. Virol. 1998, 79, 3581-3584.
20. Reanwarakom, K.; Semancik, J.S. Correlation of hop stunt viroid variants to cachexia and xyloporosis diseases of citrus. Phytopathology 1999, 89, 568-574.
21. Rodriguez, M.J.B.; Randles, J.W. Coconut cadang-cadang viroid (CCCVd) mutants associated with severe disease vary in both the pathogenicity domain and central conserved region. Nuc. Acids Res. 1993, 21, 2771.
22. Semancik, J.S.; Szychowski, J.A. Avocado sunblotch disease: a persistent viroid infection in which variants are associated with differential symptoms. J. Gen. Virol. 1994, 75, 1543-1549.
23. Schnell, R.J.; Kuhn, D.N.; Olano, C.T.; Quintanilla, W.E. Sequence diversity among avocado sunblotch viroid isolated from single avocado trees. Phytoparasitica 2002, 29, 451-460.
24. De la Peña, M.; Navarro, B.; Flores, R. Mapping the molecular determinant of pathogenicity in a hammerhead viroid: a tetraloop within the in vivo branched RNA conformation. Proc. Natl. Acad. Sci. USA 1999, 96, 9960-9965.
25. De la Peña, M.; Flores, R. Chrysanthemum chlorotic mottle viroid RNA: dissection of the pathogenicity determinant and comparative fitness of symptomatic and non-symptomatic variants. J. Mol. Biol. 2002, 321, 411-421.
26. Malfitano, M.; Di Serio, F.; Covelli, L.; Ragozzino, A.; Hernández, C.; Flores, R. Peach latent mosaic viroid variants inducing peach calico (extreme chlorosis) contain a characteristic insertion that is responsible for this symptomatology. Virology 2003, 313, 492-501.
27. Correll, C.C.; Swinger, K. Common and distinctive features of GNRA tetraloops based on a GUAA tetraloop structure at 1.4 Å resolution. RNA 2003, 9, 355-363.
28. Leontis, N.B.; Westhof, E. A common motif organizes the structure of multi-helix loops in 16 S and 23 S ribosomal RNAs. J. Mol. Biol. 1998, 283, 571-583.
29. Branch, A.D.; Benenfeld, B.J.; Robertson, H.D. Ultraviolet light-induced crosslinking reveals a unique region of local tertiary structure in potato spindle tuber viroid and HeLa 5S RNA. Proc. Natl. Acad. Sci. USA 1985, 82, 6590-6594.
30. Wassenegger, M.; Spieker, R.L.; Thalmeir, S.; Gast, F.U.; Riedel L.; Sänger, H.L. A single nucleotide substitution converts potato spindle tuber viroid (PSTVd) from a noninfectious to an infectious RNA for Nicotiana tabacum. Virology 1996, 226, 191-197.
31. Qi, Y.; Ding, B. Inhibition of cell growth and shoot development by a specific nucleotide sequence in a noncoding viroid RNA. Plant Cell 2003a, 15, 1360-1374.
32. Zhong, X.; Leontis, N.; Qian, S.; Itaya, A.; Qi, Y.; Boris-Lawrie, K.; Ding, B. Tertiary structural and functional analyses of a viroid RNA motif by isostericity matrix and mutagenesis reveal its essential role in replication. J. Virol. 2006, 80, 8566-8581.
33. Moazed, D.; Robertson, J.M.; Noller, H.F. Interaction of elongation factors EF-G and EFTu with a conserved loop in 23S RNA. Nature 1988, 372, 68-74.
34. Sharma, N.; Park, S.W.; Vepachedu, R.; Barbieri, L.; Ciani, M.; Stirpe, F.; Savary, B. J; Vivanco, J.M. Isolation and characterization of an RIP (ribosome-inactivating protein)-like protein from tobacco with dual enzymatic activity. Plant Physiol. 2004, 134, 171-181.
35. Wolff, P.; Gilz, R.; Schumacher, J.; Riesner, D. Complexes of viroids with histones and other proteins. Nucleic Acids Res. 1985, 13, 355-367.
36. Klaff, P.; Gruner, R.; Hecker, R.; Sättler, A.; Theissen, G.; Riesner, D. Reconstituted and cellular viroid-protein complexes. J. Gen. Virol. 1989, 70, 2257-2270.
37. Goodman. T.C.; Nagel, L.; Rappold, W.; Klotz, G.; Riesner, D. Viroid replication: equilibrium association constant and comparative activity measurements for the viroid-polymerase interaction. Nucleic Acids Res. 1984, 12, 6231-6246.
38. Kolonko, N.; Bannach, O.; Aschermann, K.; Hu, K.H.; Moors, M.; Schmitz, M.; Steger, G.; Riesner, D. Transcription of potato spindle tuber viroid by RNA polymerase II starts in the left terminal loop. Virology 2006, 347, 392-404.
39. Martínez de Alba, A.E.; Sägesser, R.; Tabler, M.; Tsagris, M. A bromodomain-containing protein from tomato specifically binds potato spindle tuber viroid RNA in vitro and in vivo. J. Virol. 2003, 77, 9685-9694.
40. Gomez, G.; Pallas, V. Identification of an in vitro ribonucleoprotein complex between a viroid RNA and a phloem protein from cucumber plants. Mol. Plant-Microbe Interact. 2001, 14, 910-913.
41. Owens, R.A.; Blackburn, M.; Ding, B. Possible involvement of the phloem lectin in long-distance viroid movement. Mol. Plant-Microbe Interact. 2001, 14, 905-909.
42. Gomez, G.; Pallas, V. A long-distance translocatable phloem protein from cucumber forms a ribonucleoprotein complex in vivo with hop stunt viroid RNA. J. Virol. 2004, 78, 10104-10110.
43. Daròs, J.-A.; Flores, R. A chloroplast protein binds a viroid RNA in vivo and facilitates its hammerhead-mediated self-cleavage. EMBO J. 2002, 21, 749-759.
44. Hiddinga, H.J.; Crum, C.J.; Hu, J.; Roth, D.A. Viroid-induced phosphorylation of a host protein related to a dsRNA-dependent protein kinase. Science 1988, 241, 451-453.
45. Langland, J.O.; Jin, S.; Jacobs, B.L.; Roth, D.A. Identification of a plant-encoded analog of PKR, the mammalian double-stranded RNA-dependent protein kinase. Plant Physiol. 1995, 108, 1259-1267.
46. Diener, T.O.; Hammond, R.W.; Black, T.; Katze, M.G. Mechanism of viroid pathogenesis: differential activation of the interferon-induced, double-stranded RNA-activated, M(r) 68,000 protein kinase by viroid strains of varying pathogenicity. Biochimie 1993, 75, 533-538.
47. Hammond, R.W.; Zhao, Y. Characterization of a tomato protein kinase gene induced by infection by potato spindle tuber viroid. Mol. Plant-Microbe Interact. 2000, 13, 903-910.
48. Hammond, R.W.; Zhao, Y. Modification of tobacco plant development by sense and antisense expression of the tomato viroid-induced AGC VIIIa protein kinase PKV suggests involvement in gibberellin signaling. BMC Plant Biology 2009, 9, 108 (doi:10.1186/1471-2229-9-108).
49. Christensen, S.K.; Dagenais, N.; Chory, J.; Weigel, D. Regulation of auxin response by the protein kinase PINOID. Cell 2000, 100, 469-478.
50. Devarenne, T.P.; Ekengren, S.K.; Pedley, K.F.; Martin, G.B. Adi3 is a Pdk1-interacting AGC kinase that negatively regulates plant cell death. EMBO J. 2006, 25, 255-265.
51. Diener, T.O. Biological properties. In: The Viroids, Diener, T.O., Ed.; Plenum Press: New York, NY, USA, 1987; pp. 9-35.
52. Domingo, C.; Conejero, V.; Vera, P. Genes encoding acidic and basic class III β-1,3-glucanases are expressed in tomato plants upon viroid infection. Plant Mol. Biol. 1994, 24, 725-732.
53. Tornero, P.; Conejero, V.; Vera, P. A gene encoding a novel isoform of the PR-1 protein family from tomato is induced upon viroid infection. Mol. Gen. Genet. 1994, 243, 47-53.
54. Vera, P.; Hernandez-Yago, J.; Conejero, V. "Pathogenesis-related" P1 (p14) protein. Vacuolar and apoplastic localization in leaf tissue from tomato plants infected with citrus exocortis viroid: In vitro synthesis and processing. J. Gen. Virol. 1989, 70, 1933-1942.
55. Vidal, A.M.; Ben-Cheikh, W.; Talón, M.; García-Martínez, J.L. Regulation of gibberellin 20-oxidase gene expression and gibberellin content in citrus by temperature and citrus exocortis viroid. Planta. 2003, 216, 442-448.
56. Fleet, C.M.; Sun, T-P. A DELLAcate balance: the role of gibberellin in plant morphogenesis. Curr. Opin. Plant Biol. 2005, 8, 77-85.
57. Sun, T.P.; Gubler, F. Molecular mechanisms of gibberrellin signaling in plants. Ann. Rev. Plant Biol. 2004, 55, 197-223.
58. Droge-Laser, W.; Kaiser, A.; Lindsay, W.P.; Halkier, B.A.; Loake, G.J.; Doerner, P.; Dixon, R.A.; Lamb, C. Rapid stimulation of a soybean protein-serine kinase that phosphorylates a novel bZIP DNA-binding protein, G/HBF-1, during the induction of early transcription-dependent defenses. EMBO J. 1997, 16, 726-738.
59. Pastori, G.M.; Foyer, C.H. Common components, networks, and pathways of cross-tolerance to stress. The central role of "redox" and abscisic acid-mediated controls. Plant Phys. 2002, 129, 460-468.
60. Itaya, A.; Matsuda, Y.; Gonzales, R.A.; Nelson, R.S.; Ding, B. Potato spindle tuber viroid strains of different pathogenicity induces and suppresses expression of common and unique genes in infected tomato. Mol. Plant-Microbe Interact. 2002, 15, 990-999.
61. Tessitori, M.; Maria, G.; Capasso, C.; Catara, G.; Rizza, S.; De Luca, V.; Catara, A.; Capasso, A.; Carginale, V. Differential display analysis of gene expression in Etrog citron leaves infected by Citrus viroid III. Biochim. Biophys. Acta 2007, 1769, 228-235.
62. Ascencio-Ibáñez, J.T.; Sozzani, R.; Lee, T.-J.; Chu, T.-M.; Wolfinger, R.D.; Cella, R.; Hanley-Bowdoin. L. Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol. 2008, 148, 436-454.
63. Brodersen, P.; Voinnet, O. The diversity of RNA silencing pathways in plants. Trends Genet. 2006, 22, 268-280.
64. Jones-Rhoades, M.W.; Bartel, D.P.; Bartel, B. MicroRNAs and their regulatory roles in plants. Annu. Rev. Plant Biol. 2006, 57, 19-53.
65. Ding, S.W.; Voinnet, O. Antiviral immunity directed by small RNAs. Cell 2007, 130, 413-426.
66. Carthew, R.W.; Sontheimer, E.J. Origin and mechanisms of miRNAs and siRNAs. Cell 2009, 136, 642-655.
67. Ruiz-Ferrer, V.; Voinnet, O. Roles of plant small RNAs in biotic stress responses. Annu. Rev. Plant Biol. 2009, 60, 485-510.
68. Wassenegger, M.; Heimes, S.; Riedel, L.; Sänger, H.L. RNA-directed de novo methylation of genomic sequences in plants. Cell 1994, 76, 567-576.
69. Gómez, G.; Martínez, G.; Pallás, V. Interplay between viroid-induced pathogenesis and RNA silencing pathways. Trends Plant Sci. 2009, 14, 264-269.
70. Machida, S.; Yamahata, N.; Watanuki, H.; Owens, R.A.; Sano, T. Successive accumulation of two size classes of viroid-specific small RNA in potato spindle tuber viroid-infected tomato plants. J. Gen. Virol. 2007, 88, 3452-3457.
71. Itaya, A.; Zhong, X.-H.; Bundschuh, R.; Qi, Y.-J; Wang, Y.; Takeda, R.; Harris, A.R.; Molina, C.; Nelson, R.S.; Ding, B. A structured viroid RNA serves as a substrate for Dicer-like cleavage to produce biologically active small RNAs but is resistant to RNA-induced silencing complexmediated degradation. J. Virol. 2007, 81, 2980-2994.
72. Landry, P.; Perreault, J.P. Identification of a peach latent mosaic viroid hairpin able to act as a Dicer-like substrate. J. Virol. 2005, 79, 6540-6543.
73. Martín, R.; Arenas, C.; Daròs, J.A.; Covarrubias, A.; Reyes, J.L.; Chua, N.H. Characterization of small RNAs derived from Citrus exocortis viroid in infected tomato plants. Virology 2007, 367, 135-146.
74. Schwind, N.; Zweibel, M.; Itaya, A.; Ding, B.; Wang, M-B.; Krczal, G.; Wassenegger, M. RNAimediated resistance to Potato spindle tuber viroid in transgenic tomato expressing a viroid hairpin RNA construct. Mol. Plant Path. 2009, 10, 459-469.
75. Qi, Y.; Ding, B. Differential subnuclear localization of RNA strands of opposite polarity derived from an autonomously replicating viroid. Plant Cell 2003b, 15, 2566-2577.
76. Vogt, U.; Pelissier, T.; Putz, A.; Razvi, F.; Fischer, R.; Wassenegger, M. Viroid-induced RNA silencing of GFP-viroid fusion transgenes does not induce extensive spreading of methylation or transitive silencing. Plant J. 2004, 38, 107-118.
77. Carbonell, A.; Martínez de Alba, A.-E.; Flores, R.; Gago, S. Double-stranded RNA interferes in a sequence-specific manner with the infection of representative members of the two viroid families. Virology 2008, 371, 44-53.
78. Gómez, G.; Martinez, G.; Pallás, V. Viroid-induced symptoms in Nicotiana benthamiana plants are dependent of RDR6 activity. Plant Physiol. 2008, 148, 414-423.
79. Qu, F.; Ye, X.-H.; Hou, G.-C.; Sato, S.; Clemente, T.E.; Morris, T.J. RDR6 has a broad-spectrum but temperature-dependent antiviral defense role in N. benthamiana. J. Virology 2005, 79, 15209-15217.
80. Gas, M.E.; Hernańdez, C.; Flores, R.; Daròs, J.A. Processing of nuclear viroids in vivo: An interplay between RNA conformations. PLoS Pathog. 2007, 3, 1813-1826.
81. Whitham, S.A.; Yang, C.; Goodin, M.M. Global impact: elucidating plant responses to viral infection. Mol. Plant Microbe Interact. 2006, 19, 207-215.
82. Wise, R.P.; Moscou, M.J.; Bogdanove, A.J.; Whitham, S.A. Transcript profiling in host-pathogen interactions. Annu. Rev. Phytopathol. 2007, 45, 329-369.
83. Boller, T.; He, S.Y. Innate immunity in plants: An arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 2009, 324, 742-744.
84. Daròs, J.A.; Flores, R. Arabidopsis thaliana has the enzymatic machinery for replicating representative viroid species of the family Pospiviroidae. Proc. Natl. Acad. Sci. USA 2004, 101, 6792-6797.
85. Harders, J.; Lukacs, N.; Robert-Nicoud, M.; Jovin, T. M.; Riesner, D. Imaging of viroids in nuclei from tomato leaf tissue by in situ hybridization and confocal laser scanning microscopy. EMBO J. 1989, 8, 3941-3949.
86. Hiscox, J.A. RNA viruses: hijacking the dynamic nucleolus. Nature Rev. Microbiol. 2007, 5, 119-127.
87. Senthil, G.; Liu, H.; Puram, V.G.; Clark, A.; Stromberg, A.; Goodin, M.M. Specific and common changes in Nicotiana benthamiana gene expression in response to infection by enveloped viruses. J. Gen. Virol. 2005, 86, 2615-2625.
88. Culver, J.N.; Padmanabhan, M.S. Virus-induced disease: altering host physiology one interaction at a time. Annu. Rev. Phytopathol. 2007, 45, 221-243.
89. Farag, M.A.; Huhman, D.V.; Dixon, R.A.; Sumner, L.W. Metabolomics reveals novel pathways and differential mechanistic and elicitor-specific responses in phenylpropanoid and isoflavonoid biosynthesis in Medicago truncatula cell cultures. Plant Physiol. 2009, 146, 387-402.
90. Marks, F.; Klingmüller, U.; Müller-Decker, K. Cellular signal processing: an introduction to the molecular mechanisms of signal transduction; Garland Science: New York, NY, USA, 2009; p. 634.
91. Dangl, J.L.; Dietrich, R.A.; Thomas, H. Senescence and programmed cell death. In: Biochemistry & Molecular Biology of Plants; Buchanan, B., Gruissem, W., Jones, R., Eds.; Am. Soc. Plant Biol.: Rockville, MD, USA, 2000; pp.1044-1100.
92. Grant, M.R.; Jones, J.D.G. Hormone (dis)harmony moulds plant health and disease. Science 2009, 324, 750-752.