The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
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The Road to RNA Silencing is Paved with Plant-Virus Interactions

  • Received : 2011.05.11
  • Accepted : 2011.05.24
  • Published : 2011.09.01
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Abstract

RNA silencing has had a large impact on biology in general, as well as on our understanding of plant-pathogen interactions, especially interactions between plants and viruses. While most of what we know about the mechanism of RNA silencing was deduced in the last 12 years, many of the interactions between plants and viruses, as well as virus-virus interactions in plants, which we now know are manifestations of RNA silencing, were the subject of decades of work from numerous laboratories. These laboratories were examining the nature and extent of phenomena such as recovery from infection, the formation of dark green islands resistant to re-infection, synergy between unrelated viruses and cross-protection between related viruses, all first described in the late 1920s. In this review, the relationships between these phenomena and their place in the defense mechanism we call RNA silencing will be described, to show how they are all linked.

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References

  1. Al-Kaff, N. and Covey, S.N. Biological diversity of cauliflower mosaic virus isolates expressed from two Brassica species. Plant Pathol. 44:516-526.
  2. Allard, H. A. 1914. The mosaic disease of tobacco. U. S. Dept. Agr. Bull. 40:1-33.
  3. Anandalakshmi, R., Pruss, G. J., Ge, X., Marathe, R., Mallory, A. C., Smith, T. H. and Vance, V. B. 1998. A viral suppressor of gene silencing in plants. Proc. Natl. Acad. Sci. USA 95: 13079-13084. https://doi.org/10.1073/pnas.95.22.13079
  4. Asurmendi, S., Berg, R. H., Smith, T. J., Bendahmane, M. and Beachy, R. N. 2007. Aggregation of TMV CP plays a role in CP functions and in coat-protein-mediated resistance. Virology 366:98-106. https://doi.org/10.1016/j.virol.2007.03.014
  5. Bendahmane, M. and Beachy, R. N. 1999. Control of tobamovirus infections via pathogen-derived resistance. Adv. Virus Res. 53:369-386. https://doi.org/10.1016/S0065-3527(08)60357-7
  6. Bivalkar-Mehla, S., Vakharia, J., Mehla, R., Abreha, M., Kanwar, J. R., Tikoo, A. and Chauhan, A. 2011. Viral RNA silencing suppressors (RSS): novel strategy of viruses to ablate the host RNA interference (RNAi) defense system. Virus Res. 155:1-9. https://doi.org/10.1016/j.virusres.2010.10.003
  7. Blood, H. L. 1928. A "streak" of tomatoes produced by a disturbing principle by apparently healthy potatoes in combination with tomato mosaic virus. Phytopathology 18:311-315.
  8. Boccardo, G. and Accotto, G. P. 1988. RNA-dependent RNA polymerase activity in two morphologically different white clover cryptic viruses. Virology 163:413-419. https://doi.org/10.1016/0042-6822(88)90282-6
  9. Boccardo, G., Lisa, V., Luisoni, E. and Milne, R. G. 1987. Cryptic plant viruses. Adv. Virus Res. 32:171-214. https://doi.org/10.1016/S0065-3527(08)60477-7
  10. Boller, T. and Felix, G. 2009. A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Ann. Rev. Plant Biol. 60:379-406. https://doi.org/10.1146/annurev.arplant.57.032905.105346
  11. Brigneti, G., Voinnet, O., Li, W.X., Ji, L. H., Ding, S. W. and Baulcombe, D. C. 1998. Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J. 17:6739-6746. https://doi.org/10.1093/emboj/17.22.6739
  12. Brodersen, P. and Voinnet, O. 2006. The diversity of RNA silencing pathways in plants. Trends Genet. 22:268-280. https://doi.org/10.1016/j.tig.2006.03.003
  13. Cadman, C. H. and Harrison, B. D. 1959. Studies on the properties of soil-borne viruses of the tobacco-rattle type occurring in Scotland. Ann. Appl. Biol. 47:542-556. https://doi.org/10.1111/j.1744-7348.1959.tb07286.x
  14. Canizares, M. C., Navas-Castillo, J. and Moriones, E. 2008. Multiple suppressors of RNA silencing encoded by both genomic RNAs of a crinivirus, Tomato chlorosis virus. Virus Res. 379:168-174.
  15. Carr, J. P., Lewsey, M. G. and Palukaitis, P. 2010. Signaling in induced resistance. Adv. Virus Res. 76:57-121. https://doi.org/10.1016/S0065-3527(10)76003-6
  16. Chan, S. W.-L., Zilberman, D., Xie, Z., Johansen, L. K., Carrington, J. C. and Jacobsen, S. E. 2004. RNA silencing genes control de novo DNA methylation. Science 303:1336. https://doi.org/10.1126/science.1095989
  17. Chisholm, S. T., Coaker, G., Day, B. and Staskawicz, B. J. 2006. Host-microbe interactions: Shaping the evolution of the plant immune response. Cell 124:803-814. https://doi.org/10.1016/j.cell.2006.02.008
  18. Chitwood, D. H. and Timmermans, M. C. P. 2010. Small RNAs are on the move. Nature 467:415-419. https://doi.org/10.1038/nature09351
  19. Choi, S. K., Yoon, J. Y., Ryu, K. H., Choi, J. K., Palukaitis, P. and Park, W. M. 2002. Systemic movement of a movement-deficient strain of Cucumber mosaic virus in zucchini squash is facilitated by a cucurbit-infecting potyvirus. J. Gen. Virol. 83:3173-3178. https://doi.org/10.1099/0022-1317-83-12-3173
  20. Cogoni C. and Macino G. 1999. Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature 399:166-169. https://doi.org/10.1038/20215
  21. Covey, S. N., Al-Kaff, N. S., Langara, A. and Turner, D. S. 1997. Plants combat infection by gene silencing. Nature 385:781-782. https://doi.org/10.1038/385781a0
  22. Csorba, T., Pantaleo, V. and Burgyan, J. 2009. RNA silencing: an antiviral mechanism. Adv. Virus Res. 75:35-71. https://doi.org/10.1016/S0065-3527(09)07502-2
  23. Cuellar, W. J., Kreuze, J. F., Rajamaki, M.-L., Cruzado, K. R., Untiveros, M. and Valkonen, J. P. T. 2009. Elimination of antiviral defense by viral RNase III. Proc. Natl. Acad. Sci. U.S.A. 106:10354-10358. https://doi.org/10.1073/pnas.0806042106
  24. Dalmay, T., Hamilton, A., Rudd, S., Angell, S. and Baulcombe, D. C. 2000. An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not a virus. Cell 101:543-553.
  25. Damirdagh, I. S. and Ross, A. F. 1967. A marked synergistic interaction of potato viruses X and Y in inoculated leaves of tobacco. Virology 31:296-307. https://doi.org/10.1016/0042-6822(67)90174-2
  26. de Zoeten, G. A. and Fulton, R. W. 1975. Understanding generates possibilities. Phytopathology 65:221-222.
  27. Ding, B. 2009. The biology of viroid-host interactions. Annu. Rev. Phytopathol. 47:105-131.
  28. Ding, S.-W. and Voinnet, O. 2007. Antiviral immunity directed by small RNAs. Cell 130:413-426. https://doi.org/10.1016/j.cell.2007.07.039
  29. Di Serio, F., Martinez de Alba, A.-E., Navarro, B., Gisel, A. and Flores, R. 2010. RNA-dependent RNA polymerase 6 delays accumulation and precludes meristem invasion of a viroid that replicates in the nucleus. J. Virol. 84:2477-2489. https://doi.org/10.1128/JVI.02336-09
  30. Dodds, J. A. 1982. Cross-protection and interference between electrophoretically distinct strains of cucumber mosaic virus in tomato. Virology 118:235-240. https://doi.org/10.1016/0042-6822(82)90338-5
  31. Eamens, A., Wang, M.-B., Smith, N. A. and Waterhouse, P. W. 2008. RNA silencing ion plants: yesterday, today and tomorrow. Plant Physiol. 147:456-468. https://doi.org/10.1104/pp.108.117275
  32. Edwards, M. C. 1995. Mapping of the seed transmission determinants of barley stripe mosaic virus. Mol. Plant-Microbe Ineract. 8:906-915. https://doi.org/10.1094/MPMI-8-0906
  33. Ferguson, A. and Matthews, R. E. F. 1993. Mosaic disease induced by turnip yellow mosaic tymovirus. Biochemie 75:555-559. https://doi.org/10.1016/0300-9084(93)90061-V
  34. Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E. and Mello, C. C. 1998. Potent and specific interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806-811. https://doi.org/10.1038/35888
  35. Flores, R., Hernandez, C., Martinez de Alba, A. E., Daros, J.-A. and Di Serio F. 2005. Viroids and viroid-host interactions. Annu. Rev. Phytopathol. 43:117-139. https://doi.org/10.1146/annurev.phyto.43.040204.140243
  36. Foster, T. M., Lough, T. J., Emerson, S. J., Lee, R. H., Bowman, J. L., Forster, R. L. S. and Lucas, W. J. 2002. A surveillance system regulates selective entry of RNA into the shoot apex. Plant Cell 14:1497-1508. https://doi.org/10.1105/tpc.001685
  37. Fraenkel-Conrat, H. 1983. RNA-dependent RNA polymerases of plants. Proc. Natl. Acad. Sci. U.S.A. 80:422-424. https://doi.org/10.1073/pnas.80.2.422
  38. Fukuzawa, N., Itchoda, N., Ishihara, T., Goto, K., Masuta, C. and Matsumura, T. 2010. Hc-Pro, a potyvirus RNA silencing suppressor, cancels cycling of Cucumber mosaic virus in Nicotiana benthamiana plants. Virus Genes 40:440-446. https://doi.org/10.1007/s11262-010-0460-0
  39. Fulton, R. W. 1951. Superinfection by strains of tobacco mosaic virus. Phytopathology 41:579-592.
  40. Fulton, R. W. 1986. Practices and precautions in the use of cross protection for plant virus disease control. Annu. Rev. Phytopathol. 24:67-81. https://doi.org/10.1146/annurev.py.24.090186.000435
  41. Gal-On, A. and Shiboleth, Y. M. 2006. Cross-Protection. In "Natural Resistance Mechanisms of Plants to Viruses". (G. Loebenstein and J.P. Carr, eds.), Springer, The Netherlands, pp. 261-288.
  42. Gal-On, A., Kaplan, I. and Palukaitis, P. 1995. Differential effects of satellite RNA on the accumulation of cucumber mosaic virus RNAs and the encoded proteins in tobacco vs. zucchini squash with two strains of CMV helper virus. Virology 208:58-66. https://doi.org/10.1006/viro.1995.1129
  43. Garcia-Cano, E., Resende, R. O., Fernandez-Munoz, R. and Moriones, E. 2006. Synergistic interactions between Tomato chlorosis virus and Tomato spotted wilt virus results in breakdown of resistance in tomato. Phytopathology 96:1263-1269. https://doi.org/10.1094/PHYTO-96-1263
  44. Garcia-Ruiz, H., Takeda, A., Chapman, E. J., Sullivan, C. M., Fahlgren, N., Brempelis, K. J. and Carrington, J. C. 2010. Arabidopsis RNA-dependent RNA polymerases and Dicer-like proteins in antiviral defense and small interfering RNA biogenesis during Turnip mosaic virus infection. Plant Cell 22:481-496. https://doi.org/10.1105/tpc.109.073056
  45. Gilliland, A., Singh, D. P., Hayward, J. M., Moore, C. A., Murphy, A. M., York, C. J., Slator, J. and Carr, J. P. 2003. Genetic modification of alternative respiration has differential effects on antimycin A-induced versus salicylic acid-induced resistance to Tobacco mosaic virus. Plant Physiol. 132:1518-1528. https://doi.org/10.1104/pp.102.017640
  46. Gonzales-Jara, P., Tenllado, F., Martinez-Garcia, B., Atencio, F. A., Barajas, D., Vargas, M., Diaz-Ruiz, J and Diaz-Ruiz, J. R. 2004. Host-dependent differences during synergistic infection by potyviruses with PVX. Mol. Plant Pathol. 5:29-35. https://doi.org/10.1111/j.1364-3703.2004.00202.x
  47. Goodman, R. M. and Ross, A. F. 1974a. Enhancement by potato virus Y of potato virus X synthesis in doubly infected tobacco depends on the timing of invasion by the viruses. Virology 58:263-271. https://doi.org/10.1016/0042-6822(74)90160-3
  48. Goodman, R. M. and Ross, A. F. 1974b. Enhancement of potato virus X synthesis in doubly infected tobacco occurs in double infected cells. Virology 58:16-24. https://doi.org/10.1016/0042-6822(74)90137-8
  49. Goodwin, J., Chapman, K., Swaney, S., Parks, T. D., Wernsman, E. A. and Dougherty, W. G. 1996. Genetic and biochemical dissection of transgenic RNA-mediated virus resistance. Plant Cell 8:95-105. https://doi.org/10.1105/tpc.8.1.95
  50. Gottula, J. and Fuchs, M. 2009. Towards a quarter century of pathogen-derived resistance and practical approaches to plant disease control. Adv. Virus Res. 75:161-183. https://doi.org/10.1016/S0065-3527(09)07505-8
  51. Hamilton, A. J. and Baulcombe, D. C. 1999. A species of small antisense RNA in post-transcripional gene silencing in plants. Science 286:950-952. https://doi.org/10.1126/science.286.5441.950
  52. Harrison, B. D. 1958. Relationship between beet ringspot, potato bouquet and tomato black ring viruses. J. Gen. Microbiol. 18:450-460. https://doi.org/10.1099/00221287-18-2-450
  53. Holmes, F. O. 1928. Accuracy in quantitative work with tobacco mosaic virus. Bot. Gazette 86:66-81. https://doi.org/10.1086/333873
  54. Johansen, I. E., Dougherty, W. G., Keller, K. E., Wang, D. and Hampton, R. O. 1996. Multiple determinants affect seed transmission of pea seedborne mosaic virus in Pisum sativum. J. Gen. Virol. 77:3149-3154. https://doi.org/10.1099/0022-1317-77-12-3149
  55. Jorgensen, R. A., Cluster, P. D., English, J., Que, Q. and Napoli, C. A. 1996. Chalcone synthase cosuppression phenotypes in petunia flowers: comparison of sense vs. antisense constructs and single copy vs. complex T-DNA sequences. Plant Mol. Biol. 31:957−973.
  56. Kasschau, K. D. and Carrington, J. C. 1998. A counterdefensive strategy of plant viruses: suppression of post-transcriptional gene silencing. Cell 95: 461-470. https://doi.org/10.1016/S0092-8674(00)81614-1
  57. Kreuze, J. F., Savenkov, E. I., Cuellar, W., Li, X. and Valkonen, J. P. T. 2005. Viral class 1 RNase III involved in suppression of RNA silencing. J. Virol. 79:7227-7238. https://doi.org/10.1128/JVI.79.11.7227-7238.2005
  58. Kurihara, Y. and Watanabe, Y. 2003. Cross-protection in Arabidopsis against crucifer tobamovirus Cg by an attenuated strain of the virus. Mol. Plant Pathol. 4:259-269. https://doi.org/10.1046/j.1364-3703.2003.00174.x
  59. Lakatos, L., Csorba, T., Pantaleo, V., Chapman, E. J., Carrington, J. C., Liu, Y.-P., Dolja, V. V., Fernández Calvino, L., Lopez-Moya, J. J. and Burgyan, J. 2006. Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors. EMBO J. 25:2768-2780. https://doi.org/10.1038/sj.emboj.7601164
  60. Lewsey, M., Palukaitis, P. and Carr, J. P. 2009. Plant-virus interactions: Defence and counter-defence. In "Annual Plant Reviews, Volume 34, Molecular Aspects of Plant Disease Resistance." (J. Parker, ed.), Wiley-Blackwell, Oxford, pp. 134-176.
  61. Li, F. and Ding, S.-W. 2006. Virus counterdefense: diverse strategies for evading the RNA-silencing immunity. Annu. Rev. Microbiol. 60:503-531. https://doi.org/10.1146/annurev.micro.60.080805.142205
  62. Lindbo, J. A., Silva-Rosales, L., Proebsting, W. M. and Dougherty, W. G. 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. https://doi.org/10.1105/tpc.5.12.1749
  63. Lippman, Z. and Martienssen, R. 2004. The role of RNA interference in heterochromatin silencing. Nature 431:364-370. https://doi.org/10.1038/nature02875
  64. Lister, R. M. and Murant, A. F. 1967. Seed transmission of nematode- borne viruses. Ann. Appl. Biol. 59:49-62. https://doi.org/10.1111/j.1744-7348.1967.tb04416.x
  65. Loebenstein, G., Cohen, J., Shabtai, S., Coutts, R. H. A. and Wood, K. R. 1977. Distribution of cucumber mosaic virus in systemically infected tobacco leaves. Virology 81:117-125. https://doi.org/10.1016/0042-6822(77)90063-0
  66. Lu, R., Folimonov, A., Shintaku, M., Li, W-X., Falk, B. W., Dawson, W. O. and Ding, S.-W. 2004. Three distinct suppressors of RNA silencing encoded by a 20-kb viral RNA genome. Proc. Natl. Acad. Sci. U.S.A. 101:15742-15747. https://doi.org/10.1073/pnas.0404940101
  67. Maule, A. J. and Wang, D. 1996. Seed transmission of plant viruses: a lesson in biological complexity. Trends Microbiol. 4:153-158. https://doi.org/10.1016/0966-842X(96)10016-0
  68. McKinney, H. H. 1929. Mosaic diseases in the canary Islands, West Africa and Gibraltar. J. Agric. Res. 39:557-578.
  69. Merai, Z., Kerenyi, Z., Kertesz, S., Magna, M., Lakatos, L. and Silhavny, D. 2006. Double-stranded RNA binding may be a general plant RNA viral strategy to suppress RNA silencing. J. Virol. 80:5747-5756. https://doi.org/10.1128/JVI.01963-05
  70. Mette, M. F., Aufsatz, W., van der Winden, J., Matzke, M. A. and Matzke, A. J. M. 2000. Transcriptional silencing and promoter methylation triggered by double-stranded RNA. EMBO J. 19:5194-5201. https://doi.org/10.1093/emboj/19.19.5194
  71. Mink, G. I. 1993. Pollen-transmitted and seed-transmitted viruses and viroids. Ann. Rev. Phytopathol. 31:375-402.
  72. Moazed, D. 2009. Small RNAs in transcriptional gene silencing and genome defence. Nature 457:413-420. https://doi.org/10.1038/nature07756
  73. Moore, C. J. and MacDiarmid, R. M. 2006. Dark Green Islands: the Phenomenon. In: "Natural Resistance Mechanisms of Plants to Viruses". (G. Loebenstein and J.P. Carr, eds.), Springer, The Netherlands, pp. 187-209.
  74. Moore, C. J., Sutherland, P. W., Forster, R. L. S., Gardner, R. C. and MacDiarmid, R. M. 2001. Dark green islands in plant virus infection ar the result of posttranscriptional gene silencing. Mol. Plant-Microbe Interact. 14:939-946. https://doi.org/10.1094/MPMI.2001.14.8.939
  75. Mourrain, P., Beclin, C., Elmayan, T., Feuerbach, F., Godon, C., Morel, J. B., Jouette, D., Lacombe, A. M., Nikic, S., Picault, N., Remoue, K., Sanial, M., Vo, T. A. and Vaucheret, H. 2000. Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101:533-542. https://doi.org/10.1016/S0092-8674(00)80863-6
  76. Murphy, J. F. and Kyle, M. M. 1995. Alleviation of restricted systemic spread of pepper mottle potyvirus in Capsicum annum cv. Avelar by coinfection with a cucumovirus. Phytopathology 85:561-566. https://doi.org/10.1094/Phyto-85-561
  77. Napoli, C., Lemieux, C. and Jorgensen, R. 1990. Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279-289. https://doi.org/10.1105/tpc.2.4.279
  78. Nelson, R. S., Powell-Abel, P. and Beachy, R. N. 1987. Lesions and virus accumulation in inoculated transgenic tobacco plants expressing the coat protein gene of tobacco mosaic virus. Virology 158:126-132. https://doi.org/10.1016/0042-6822(87)90245-5
  79. Niblett, C. L., Dickson, E., Fernow, K. H., Horst, R. K. and Zaitlin, M. 1978. Cross protection among four viroids. Virology 91:198-203. https://doi.org/10.1016/0042-6822(78)90368-9
  80. Qu, F., Ye, X., Hou, G., Sato, S., Clemente, T. E. and Morris, T. J. 2005. RDR6 has a broad-spectrum but temperature dependent antiviral defense role in Nicotiana benthamiana. J. Virol. 79:15209-15217. https://doi.org/10.1128/JVI.79.24.15209-15217.2005
  81. Palukaitis, P. and Kaplan, I. B. 1997. Synergy of virus accumulation and pathology in transgenic plants expressing viral sequences. In: "Virus-resistant Transgenic Plants: Potential Ecological Impact." (M. Tepfer and E. Balázs, eds.), Springer, Berlin. pp. 77-84.
  82. Palukaitis, P. and MacFarlane, S. 2006. Viral Counter-Defense Molecules. In "Natural Resistance Mechanisms of Plants to Viruses". (G. Loebenstein and J.P. Carr, eds.), Springer, The Netherlands, pp. 165-185.
  83. Palukaitis, P. and Zaitlin, M. 1984. A model to explain the "cross protection" phenomenon shown by plant viruses and viroids. In: "Plant-Microbe Interactions - Molecular and Genetic Perspectives". (E.W. Nester and T. Kosuge, eds.), MacMillan, New York. Volume 1. pp. 420-429.
  84. Pandey, S. P. and Baldwin, I. T. 2007. RNA-directed RNA polymerase 1 (RdR1) mediates the resistance of Nicotiana attenuata to herbivore attack in nature. Plant J. 50:40-53. https://doi.org/10.1111/j.1365-313X.2007.03030.x
  85. Pandey, S. P., Priyanka, P., Gase, K. and Baldwin, I. T. 2008. Herbivory- induced changes in the small-RNA transcriptome and phytohormone signaling in Nicotiana attenuata. Proc. Natl. Acad. Sci. U.S.A. 105:4559-4564. https://doi.org/10.1073/pnas.0711363105
  86. Poolpol, P. and Inouye, T. 1986. Enhancement of cucumber mosaic virus multiplication by zucchini yellow mosaic virus in doubly infected cucumber plants. Ann. Phytopath. Soc. Japan 52:22-30. https://doi.org/10.3186/jjphytopath.52.22
  87. Powell-Abel, P., Nelson, R. S., De, B., Hoffmann, N., Rogers, S. G., Fraley, R. T. and Beachy, R. N. 1986. Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science 232:738-743. https://doi.org/10.1126/science.3457472
  88. Powell-Abel, P., Sanders, P. R., Tumer, N., Fraley, R. T. and Beachy, R. N. 1990. Protection against tobacco mosaic virus infection in transgenic plants requires accumulation of coat protein rather than coat protein RNA sequences. Virology 175:124-130. https://doi.org/10.1016/0042-6822(90)90192-T
  89. Pruss, G., Ge, X., Shi, X. M., Carrington, J. C. and Vance, V. B. 1997. Plant viral synergism: the potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses. Plant Cell 9:859-868. https://doi.org/10.1105/tpc.9.6.859
  90. Rashid, U. J., Hoffmann, J., Brutschy, B., Piehler, J. and Chen, J. C-H. 2008. Multiple targets for suppression of RNA interference by Tomato aspermy virus protein 2B. Biochemistry 47:12655-12657. https://doi.org/10.1021/bi801281h
  91. Ratcliff, F., Harrison, B. D. and Baulcombe, D. C. 1997. A similarity between viral defense and gene silencing in plants. Science 276:1558-1560. https://doi.org/10.1126/science.276.5318.1558
  92. Ratcliff, F. G., MacFarlane, S. A. and Baulcombe, D. C. 1999. Gene silencing without DNA: RNA-mediated cross-protection between viruses. Plant Cell 11:1207-1215. https://doi.org/10.1105/tpc.11.7.1207
  93. Rochow, W. F. and Ross, A. F. 1955. Virus multiplication in plants doubly infected by potato viruses X and Y. Virology 1:10-27. https://doi.org/10.1016/0042-6822(55)90003-9
  94. Ross, A. F. 1941. The concentration of alfalfa-mosaic virus in tobacco plants at different periods of time after inoculation. Phytopathology 31:410-421.
  95. Ruiz, M. T., Voinnet, O. and Balucombe, D. C. 1998. Initiation and maintenance if virus-induced gene silencing. Plant Cell 10:937-946. https://doi.org/10.1105/tpc.10.6.937
  96. Saenz, P., Salvador, B., Simón-Mateo, B., Kasschau, K. D., Carrington, J. C. and García, J. A. 2002. Host-specific involvement of the HC protein in the long-distance movement of potyviruses. J. Virol. 76:1922-1931. https://doi.org/10.1128/JVI.76.4.1922-1931.2002
  97. Salaman, R. N. 1933. Protective inoculation against a plant virus. Nature 131:468.
  98. Schiebel W., Pélissier T., Riedel L., Thalmeir S., Schiebel R., Kempe D., Lottspeich F., Sänger H. L. and Wassenegger M. 1998. Isolation of an RNA-directed RNA polymerase-specific cDNA clone from tomato. Plant Cell 10:2087-2101.
  99. Schmardon, A., Spoerke, J. M., Stacey, S. C., Klein, M. E., Mackin, N. and Maine, E. M. 2000. EGO-1 is related to RDNA-directed RNA polymerase and functions in germ-line development and RNA interference in C. elegans. Curr. Biol. 10:169-178. https://doi.org/10.1016/S0960-9822(00)00323-7
  100. 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. https://doi.org/10.1104/pp.105.063537
  101. Shams-Bakhsh, M., Canto, T. and Palukaitis, P. 2007. Enhanced resistance and neutralization of defense responses by suppressors of RNA silencing. Virus Res. 130:103-109.
  102. Sherwood, J. L. 1987. Demonstration of the specific involvement of coat protein in tobacco mosaic virus (TMV) cross protection using a TMV coat protein mutant. J. Phytopathol. 118:358-362. https://doi.org/10.1111/j.1439-0434.1987.tb00467.x
  103. Sherwood, J. L. and Fulton, R. W. 1982. The specific involvement of coat protein in Tobacco mosaic virus cross protection. Virology 119:150-158. https://doi.org/10.1016/0042-6822(82)90072-1
  104. Shi, X. M., Miller, H., Verchot, J., Carrington, J. C. and Vance, V. B. 1997. Mutations in the region encoding the central domain of helper component-proteinase (HC-Pro) eliminate potato virus X/potyviral synergism. Virology 231:35-42. https://doi.org/10.1006/viro.1997.8488
  105. Smith, J. H. 1928. The transmission of potato mosaic to tomato. Ann. Appl. Biol. 15:517-528. https://doi.org/10.1111/j.1744-7348.1928.tb07774.x
  106. Smith, C. J. S., Watson, C. F., Morris, P. C., Bird, C. R., Seymour, G. B., Gray, J. E., Arnold, C., Tucker, G. A., Schuch, W., Harding, S. and Grierson, D. 1990. Inheritance and effect on ripening of antisense polygalacturonase genes in transgenic tomatoes, Plant Mol. Biol. 14:369-379. https://doi.org/10.1007/BF00028773
  107. Smith, H. A., Swaney, S. L., Parks, T. D., Wernsman, E. A. and Dougherty, W. G. 1994. Transgenic plant virus resistance mediated by untranslatable sense RNAs: expression, regulation, and fate of nonessential RNAs. Plant Cell 6:1441-1453. https://doi.org/10.1105/tpc.6.10.1441
  108. Sunpapao, A., Nakai, T., Dong, F., Mochizuki, T. and Ohki, S. T. 2009. The 2b protein of cucumber mosaic virus is essential for viral infection of the shoot apical mesistem and for efficient invasion of leaf primordia in infected tobacco plants. J. Gen. Virol. 90:3015-3021. https://doi.org/10.1099/vir.0.013219-0
  109. Vance, V. B. 1991. Replication of potato virus X RNA is altered in coinfections with potato virus Y. Virology 182:486-494. https://doi.org/10.1016/0042-6822(91)90589-4
  110. Vance, V. B., Berger, P. H., Carrington, J. C., Hunt, A. G. and Shi, X. M. 1995. 5 proximal potyviral sequences mediate potato virus X/potyviral synergistic disease in transgenic tobacco. Virology 206:583−590.
  111. van der Krol, A. R., Mur, L. A., Beld, M., Mol, J. N. M. and Stuitje, A. R. 1990. Flavonoid genes in petunia: addition of a limited number of gene copies may lead to suppression of gene expression. Plant Cell 2:291-299. https://doi.org/10.1105/tpc.2.4.291
  112. van Rij, R. P. and Andino, R. 2006. The silent treatment: RNAi as a defense against virus infection in mammals. Trends Biotechnol. 24:186-193. https://doi.org/10.1016/j.tibtech.2006.02.006
  113. Vanterpool, T. C. 1926. Streak or winter blight of tomato in Quebec. Phytopathology 16:311-331.
  114. Vaucheret, H. 2006. Post-transcriptional small RNA pathways in plants: mecvhanisms and regulations. Genes Dev. 20:759-771. https://doi.org/10.1101/gad.1410506
  115. Voinnet, O. 2005a. Induction and suppression of RNA silencing: insights from viral infections. Nature Rev. Genet. 6:206-221. https://doi.org/10.1038/nrg1555
  116. Voinnet, O. 2005b. Non-cell autonomous RNA silencing. FEBS Lett. 579:5858-5871. https://doi.org/10.1016/j.febslet.2005.09.039
  117. Wang, D., MacFarlane, S. A. and Maule, A. J. 1997. Viral determinants of pea early browning virus seed transmission in pea. Virology 234:112-117. https://doi.org/10.1006/viro.1997.8637
  118. Wang, Y., Gaba, V., Yang, J., Palukaitis, P. and Gal-On, A. 2002. Characterization of synergy between Cucumber mosaic virus and potyviruses in cucurbit hosts. Phytopathology 92:51-58. https://doi.org/10.1094/PHYTO.2002.92.1.51
  119. Wang, Y., Lee, K. C., Gaba, V., Wong, S. M., Palukaitis, P. and Gal-On, A. 2004. Breakage of resistance to Cucumber mosaic virus by co-infection with Zucchini yellow mosaic virus: enhancement of CMV accumulation independent of symptom expression. Arch. Virol. 149:379-396. https://doi.org/10.1007/s00705-003-0240-4
  120. Wang, X.-B., Wu, Q., Ito, T., Cillo, F., Li, W.-X., Chen, X., Yu, J.- L. and Ding, S.-W. 2010. RNAi-mediated viral immunity requires amplification of virus-derived siRNAs in Arabidopsis thaliana. Proc. Natlt. Acad. Sci. USA 107:484-489. https://doi.org/10.1073/pnas.0904086107
  121. Wassenegger, M. 2005. The role of RNAi machinery in heterochromatin formation. Cell 122:13-16. https://doi.org/10.1016/j.cell.2005.06.034
  122. Wassenegger, M. and Krczal, G. 2006. Nomenclature and functions of RNA-directed RNA polymerases. Trends Plant Sci. 11:142-151. https://doi.org/10.1016/j.tplants.2006.01.003
  123. Webb, R. E., Larson, R. H. and Walker, J. C. 1952. Relationships of potato leaf roll virus strains. Res. Bull. Agric. Ex. Stat. Coll. Agric. Univ. Wisconsin. 178:1-38.
  124. Wingard, S. A. 1928. Hosts and symptoms of ring spot, a virus disease of plants. J. Agric. Res. 37:127-153.
  125. Xie, Z., Fan, B., Chen, C. and Chen, Z. 2001. An important role of an inducible RNA-dependent RNA polymerase in plant antiviral defense. Proc. Natl. Acad. Sci. U.S.A. 98:6516-21. https://doi.org/10.1073/pnas.111440998
  126. Yang, S. J., Carter, S. A., Cole, A. B., Cheng, N. H. and Nelson, R. S. 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. 101:6297-302. https://doi.org/10.1073/pnas.0304346101
  127. Yelina, N. E., Savenkov, E. I., Solovyev, A. G., Morozov, S. Y. and Valkonen, J. P. T. 2002. Long-distance movement, virulence, and RNA silencing suppression controlled by a single protein in hordei- and potyviruses: complementary functions between virus families. J. Virol. 76:12981-12991. https://doi.org/10.1128/JVI.76.24.12981-12991.2002
  128. Yu, D., Fan, B., MacFarlane, S. A. and Chen, Z. 2003. Analysis of the involvement of an inducible Arabidopsis RNA-dependent RNA polymerase in antiviral defense. Mol. Plant-Microbe Interact. 16:206-216. https://doi.org/10.1094/MPMI.2003.16.3.206
  129. Zhang, X., Du, P., Lu, L., Xiao, Q., Wang, W., Cao, X., Ren, B., Wei, C. and Li, Y. 2008. Contrasting effects of HC-Pro and 2b viral suppressors from Sugarcane mosaic virus and Tomato aspermy cucumovirus on the accumulation of siRNAs. Virology 374:351-360. https://doi.org/10.1016/j.virol.2007.12.045
  130. Ziebell, H. and Carr, J. P. 2009. Effects of Dicer-like endoribonucleases 2 and 4 on infection of Arabidopsis thaliana by cucumber mosaic virus and a mutant virus lacking the 2b counter-defence protein gene. J. Gen. Virol. 90:2288-2292. https://doi.org/10.1099/vir.0.012070-0
  131. Ziebell, H. and Carr, J. P. 2010. Cross-protection: a century of mystery. Adv. Virus Res. 76:211-264. https://doi.org/10.1016/S0065-3527(10)76006-1

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