The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
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Relationship Between Plant Viral Encoded Suppressor to Post-transcriptional Gene Silencing and Elicitor to R Gene-specific Host Resistance

  • Park, Chang-Won (Department of Biology and Medicinal Science, Pai Chai University) ;
  • Feng Qu (School of Biological Sciences, University of Nebraska) ;
  • Tao Ren (School of Biological Sciences, University of Nebraska) ;
  • T. Jack Morris (School of Biological Sciences, University of Nebraska)
  • Published : 2004.03.01
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Abstract

Many important horticultural and field crops are susceptible to virus infections or may possess a degree of resistance to some viruses, but become infected by others. Plant viruses enter cells through the presence of wounds, and replicate intracellularly small genomes that encode genes required for replication, cell-to-cell movement and encapsidation. There are numerous evidences from specific virus-host interactions to require the involvement of host factors and steps during viral replication cycle. However, viruses should deal with host defense responses either by general or specific mechanisms, targeting viral components or genome itself. On the other hand, the host plants have also adapted to defend themselves against viral attack by operating different lines of resistance responses. The defense-related interactions provide new insights into the complex molecular strategies for hosts for defense and counter-defense employed by viruses.

Keywords

References

  1. Abbink, T. E. M., Tjernberg, P. A., Bol, J. F. and Linthorst, H. J. M. 1998. Tobacco mosaic virus helicase domain induces necrosis in N gene-carrying tobacco in the absence of virus replication. Mol. Plant-Microbe. Interact. 11:1242-1246 https://doi.org/10.1094/MPMI.1998.11.12.1242
  2. Atkinson, R. G., Bieleski, L. R. F., Gleave, A. P., Janssen, B. -J. and Morris, B. A. M. 1998. Post-transcriptional silencing of chalcone synthase in petunia using a geminivirus-based episomal vector. Plant J. 15:593-604 https://doi.org/10.1046/j.1365-313x.1998.00211.x
  3. Baker, B., Zambryski, P, Staskawicz, B. and Dinesh-Kumar, S. P. 1997. Signaling in plant-microbe interactions. Science 276: 726-733 https://doi.org/10.1126/science.276.5313.726
  4. Baulcombe, D. C. 1999. Fast forward genetics based on virusinduced gene silencing. Curr. Opin. Plant Biol. 2: 109-113 https://doi.org/10.1016/S1369-5266(99)80022-3
  5. Baulcombe, D. C. 2002. RNA silencing. Curr. Biol. 12:R82-R84 https://doi.org/10.1016/S0960-9822(02)00665-6
  6. Beclin, C., Berthome, R., Palauqui, J. C., Tepfer, M. and Vercgeret, H. 1998. Infection of tobacco or Arabidopsis plants by CMV counteracts systemic post-transcriptional silencing of nonviral (trans)genes. Virology 252:313-317 https://doi.org/10.1006/viro.1998.9457
  7. Bendahmane, A., Kohn, B. A., Dedi, C. and Baulcombe, D. C. 1995. The coat protein of potato virus X is a strain-specific elicitor of RxI-mediated virus resistance in potato. Plant J. 8:933-941 https://doi.org/10.1046/j.1365-313X.1995.8060933.x
  8. Bendahmane, A., Kanyuka, K. and Baulcombe, D. C. 1999. The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell 11 :781-791 https://doi.org/10.1105/tpc.11.5.781
  9. Bernstein, E., Caudy, A. A., Hammond, S. M. and Hannon, G. J. 2001. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363-366 https://doi.org/10.1038/35053110
  10. Berzal-Herranz, A., de la Cruz, A., Tenllado, F., Diaz-Ruiz, J. R., Lopez, L., Sanz, A. J., Vaquero, C., Serra, M. T. and GarciaLique, I. 1995. The capsicum L3 gene-mediated resistance against the tobamoviruses is elicited by the coat protein. Virology 209:498-505 https://doi.org/10.1006/viro.1995.1282
  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. Carrington, J. C., Kasschau, K. D. and Johansen, L. K. 2001. Activation and suppression of RNA silencing by plant viruses. Virology 281:1-5 https://doi.org/10.1006/viro.2000.0812
  13. Choi, C. W. Qu, F., Ren, T. and Morris, T. J. 2003. Suppression of RNA silencing by the coat protein of turnip crinkle virus is not dependent on the N-terrninal region responsible for eliciting resistance in Arabidopsis. 22nd Annual ASV Meeting, Univ. California, Davis, Abstract p. 266
  14. Chuang, C.-F. and Meyerowitz, E. M. 2000. Specific and heritable genetic interference by double-stranded RNA in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 97:4985-4990 https://doi.org/10.1073/pnas.060034297
  15. 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
  16. Cooley, M., Pathirana, S., Wu, H.-J., Kachroo, P and Klessig, D. F. 2000. Members of the Arabidopsis HRT/RPP8 family of resistance genes confer resistance to both viral and oomycete pathogens. Plant Cell 12:663-676 https://doi.org/10.1105/tpc.12.5.663
  17. Dalmay, T., Hamilton, A., Mueller, E. and Baulcombe, D. C. 2000a. Potato virus X amplicons in Arabidopsis mediate genetic and epigenetic gene silencing. Plant Cell 12:369-379 https://doi.org/10.1105/tpc.12.3.369
  18. Dalmay, T., Hamilton, A., Rudd, S., Angell, S., and Baulcombe, D. C. 2000b. 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 https://doi.org/10.1016/S0092-8674(00)80864-8
  19. Dalmay, T., Horsefield, R., Braunstein, T. H. and Baulcombe, D. C. 2001. SDE3 encodes an RNA helicase required for posttranscriptional gene silencing in Arabidopsis. EMBO J. 20: 2069-2077 https://doi.org/10.1093/emboj/20.8.2069
  20. Dangl, J. L. and Jones, J. D. 2001. Plant pathogens and integrated defense responses to infection. Nature 411 :826-833 https://doi.org/10.1038/35081161
  21. De Serio, F., Schoeb, H., Iglesias, A., Tarina, C., Bouldoires, E and Meins, F. Jr. 2001. Sense-and antisense-mediated gene silencing in tobacco is inhibited by the same viral suppressors and is associated with accumulation of small RNAs. Proc. Natl' Acad. Sci. USA 98:6506-6510 https://doi.org/10.1073/pnas.111423098
  22. Dunoyer, P., Pfeffer, S., Fritsch, C., Hemmer, O, Voinnet, O. and Richards, K.E. 2002. Identification, subcellular localization and some properties of a cysteine-rich suppressor of gene silencing encoded by peanut clump virus. Plant J. 29:555-567 https://doi.org/10.1046/j.0960-7412.2001.01242.x
  23. Elmayan, T., Balzergue, S., Beon, F., Bourdon, V., Daubremet, J., Guenet, Y., Mourrain, P., Palauqui, J.-C., Vernhettes, S., Vialle, T., Wostrikoff, K. and Vaucheret, H. 1998. Arabidopsis mutants impaired in cosuppression. Plant Cell 10: 1747-1757 https://doi.org/10.1105/tpc.10.10.1747
  24. English, J. J., Mueller, E. and Baulcombe, D. C. 1996. Suppression of virus accumulation in transgenic plants exhibiting silencing of nuclear genes. Plant Cell 8: 179-188 https://doi.org/10.1105/tpc.8.2.179
  25. Fagard, M. and Vaucheret, H. 2000. Systemic silencing signal(s). Plant Mol. Biol. 43:285-293 https://doi.org/10.1023/A:1006404016494
  26. Fire, A., Xu. S., Montgomery, M. K., Kostsa, S. A., Driver, S. E. and Mello, C. C. 1998. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391 :806-811 https://doi.org/10.1038/35888
  27. Flor, H. 1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9:275-296 https://doi.org/10.1146/annurev.py.09.090171.001423
  28. Foster, T. M., Lough, T. J., Emerson, S. J., Lee, R. H., Bowman, J. L., Foster, R. S. and Lucas, W. L. 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
  29. Guo, H.-S. Lopez-Maya, J. J. and Garcia, J. A 1999. Mitotic stability of infection induced resistance to plum pox ptyvirus associated with transgene silencing and DNA methylation. Mol. Plant-Microbe Interact. 12: 103-111 https://doi.org/10.1094/MPMI.1999.12.2.103
  30. Guo, H. S. and Ding, S. W. 2002. A viral protein inhibits the long range signaling activity of the gene silencing signal. EMBO J. 21 :398-407 https://doi.org/10.1093/emboj/21.3.398
  31. Hamilton, A J. and Baulcombe, D. C. 1999. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950-952 https://doi.org/10.1126/science.286.5441.950
  32. Hammond, S. M., Bernstein, E., Beach, D. and Hannon, G. J. 2000. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cell extracts. Nature 404: 293-296 https://doi.org/10.1038/35005107
  33. Hammond, S. M., Boettcher, S., Caudy, A. A., Kobayashi, R. and Hannon, G. J. 2001a. Argonaute, a link between genetic and biochemical analyses of RNAi. Science 293:1146-1150 https://doi.org/10.1126/science.1064023
  34. Hunt, M. D. and Ryals, J. A 1996. Systemic acquired resistance signal transduction. Crit. Rev. Plant Sci. 15:583-606 https://doi.org/10.1080/07352689609382371
  35. Jin, Q. and He, S. Y. 2001. Role of the Hrp pilus in type III protein secretionin Pseudomonas syringae. Science 294:2556-2558 https://doi.org/10.1126/science.1066397
  36. Jones, A. L., Thomas, C. L. and Maule, A. J. 1998. De novo methylation and co-suppression induced by a cytoplasmically replicating plant RNA virus. EMBO J. 17:6385-6393 https://doi.org/10.1093/emboj/17.21.6385
  37. Jones, L., Hamilton, A. J., Voinnet, O., Thomas, C. L., Maule, A. J. and Baulcombe, D. C. 1999. RNA-DNA intt;-ractions and DNA methylation in post-transcriptional gene silencing. Plant Cell 11:2291-2302 https://doi.org/10.1105/tpc.11.12.2291
  38. Kasschau, K. D. and Carrington, J. C. 1998. A counterdefense strategy of plant viruses: suppression of post-transcriptional silencing. Cell 95:461-470 https://doi.org/10.1016/S0092-8674(00)81614-1
  39. Kennerdell, J. R. and Carthew, R. W. 1998. Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled 2 act in the wingless pathway. Cell 95: 1017-1026
  40. Kim, C.-H. and Palukatis, P. 1997. The plant defense response to cucumber mosaic virus in cowpea is elicited by the viral polymerase gene and affects virus accumulation in single cells. EMBO J. 16:4060-4068 https://doi.org/10.1093/emboj/16.13.4060
  41. Kjemtrup, S., Sampson, K. S., Peele, C. G., Nguyen, L. V., Conkling, M. A., Thompson, W. F. and Robertson, D. 1998. Gene silencing from plant DNA carried by a geminivirus. Plant J. 14:91-100 https://doi.org/10.1046/j.1365-313X.1998.00101.x
  42. Knight, S. W. and Bass, B. L. 2001. A role for the RNase III enzyme DCR-l in RNA interference and germ line development in Caenorhabditis elegans. Science 293:2269-2271 https://doi.org/10.1126/science.1062039
  43. Kovarik, A., van Houdt, H., Holy, A. and Depicker, A. 2000. Drug-induced hypomethylation of a posttranscriptionally silenced transgene locus of tobacco leads to partial release of silencing. FEBS Letters 467:47-51 https://doi.org/10.1016/S0014-5793(00)01077-2
  44. Lipardi, C., Wei, Q. and Paterson, B. M. 2001. RNAi as random degradative PCR: siRNA primers convert mRNA into dsRNAs that are degraded to generate new siRNAs. Cell 107:297-307 https://doi.org/10.1016/S0092-8674(01)00537-2
  45. Llave, C., Kasschau, K. D. and Carrington, J. C. 2000. Virusencoded suppressor of posttranscriptional gene silencing targets a maintenance step in the silencing pathway. Proc. Natl. Acad. Sci. USA,97:13401-13406 https://doi.org/10.1073/pnas.230334397
  46. Mackey, D., Belkhadir, Y., Alonso, J. M., Ecker, J. R. and Dangl, J. L. 2003. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112:379-389 https://doi.org/10.1016/S0092-8674(03)00040-0
  47. Matthews, R. E. F. 1991. Plant Virology, 3$^{rd}$ ed., Academic Press, New York
  48. Matzke, M., Matzke, A. J. and Kooter, J. M. 2001. RNA: Guiding gene silencing. Science 293: 1080-1083 https://doi.org/10.1126/science.1063051
  49. Mallory, A. C., Ely, L., Smith, T. H., Marathe, R., Anandalakshmi, R., Fagard, M., Vaucheret, H., Pruss, G., Bowman, L, and Vance, V. B. 2001. HC-Pro suppression of transgene silencing eliminates small RNAs but not transgene methylation of the mobile signal. Plant Cell 13:571-583 https://doi.org/10.1105/tpc.13.3.571
  50. Mallory, A. C., Reinhart, B. J., Bartel, D. B., Vance, V. B. and Bowman, L. H. 2002. A viral suppressor of RNA silencing differently regulates the accumulation of short-interfering RNAs and microRNAs in tobacco. Proc. Natl. Acad. Sci. USA 99: 15228-15233 https://doi.org/10.1073/pnas.232434999
  51. Mallory, A. C., Mltoshwa, S., Bowman, L. H. and Vance, V. B. 2003. The capacity of transgenic tobacco to send a systemic RNA silencing signal depends on the nature of the inducing transgene locus. Plant J. 35:82-92 https://doi.org/10.1046/j.1365-313X.2003.01785.x
  52. Meshi, T., Motoyoshi, F., Maeda, T., Yoshiwoka, S., Watanabe, H. and Okada, Y. 1989. Mutations in the tobacco mosaic virus 30-kD protein gene overcome Tm-2 resistance in tomato. Plant Cell 1 :515-522 https://doi.org/10.1105/tpc.1.5.515
  53. Mestre, P. Brigneti, G. and Baulcombe, D. C. 2000. An Ry-mediated resistance response in potato requires the intact active site of the NIa proteinase from potato virus Y. Plant J. 23:653-661 https://doi.org/10.1046/j.1365-313x.2000.00834.x
  54. Morel, J. B., Mourrain, P., Beclin, C. and Vaucheret, H. 2000. DNA methylation and chromatin structure affect transcriptional and posttranscriptional transgene silencing in Arabidopsis. Curr. Biol. 10:1591-1594 https://doi.org/10.1016/S0960-9822(00)00862-9
  55. Mlotshwa, S., Voinnet, O., Mette, M. F, Matzke, M., Vaucheret, H., Ding, S. W, Pruss, G. and Vance, V. B. 2002. RNA silencing and the mobile silencing signal. Plant Cell 14:S289-S301 https://doi.org/10.1105/tpc.140210
  56. Mourrain, P., Beclin, C., Elmayan, T., Feuerbach, F, Godon, C., Morel, J.-B., Jouette, D., Lacombe, A-M., Nikic, S., Picault, N., Remoue, M., Sanial, M., Vo, T.-A. and Vaucheret, H. 2000. Arabidopsis SGS2 and SGS3 genes are required for transcriptional gene silencing and natural virus resistance. Cell 10l :533-542 https://doi.org/10.1016/S0092-8674(00)80863-6
  57. Padgett, H. S., Watanabe, Y. and Beachy, R. N. 1997. Identification of the TMV replicase sequence that activates the N genemediated hypersensitive response. Mol. Plant-Microbe Interact. 10:709-715 https://doi.org/10.1094/MPMI.1997.10.6.709
  58. Peele, C., Jordan, C. V., Muangsan, N., Turnage, M., Egelkrout, E., Eagle, P., Hanley-Bowdoin, L. and Robertson, D. 2001. Silencing of a meristematic gene using geminivirus-derived vectors. Plant J. 27:357-366 https://doi.org/10.1046/j.1365-313x.2001.01080.x
  59. Pelissier, T., Thalmeir, S., Kempe, D., Sanger, H. L. and Wassenegger, M. 1999. Heavy de novo methylation at symmetrical and non-symmetrical sites is a hallmark of RNA-directed DNA methylation. Nucleic acid Res. 27: 1625-1634 https://doi.org/10.1093/nar/27.7.1625
  60. Qu, F., Ren, T. and Morris, T. J. 2003. The coat protein of turnip crinkle virus suppresses posttranscriptional gene silencing at an early initiation step. J. Virol. 77:511-522 https://doi.org/10.1128/JVI.77.1.511-522.2003
  61. Ren, T., Qu, F. and Morris, T. J. 2000. HRT gene function requires interaction between a NAC protein and viral capsid protein to confer resistance to turnip crinkle virus. Plant Cell 12:1917-1926 https://doi.org/10.1105/tpc.12.10.1917
  62. Rodman, M. K., Narendra, S. Y. and Artus, N. N. 2002. Progression of geminivirus-induced transgene silencing is associated with transgene methylation. New Pytol. 155:461-468 https://doi.org/10.1046/j.1469-8137.2002.00467.x
  63. Rossi, M., Goggin, F. L., Milligan, S. B., Kaloshian, I., Ullman, D. E. and Williamson, V. M. 1998. The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc. Natl. Acad. Sci. USA. 95:9750-9754 https://doi.org/10.1073/pnas.95.17.9750
  64. Ruiz, M. T., Voinnet, O. and Baulcombe, D. C. 1998. Initiation and maintenance of virus-induced gene silencing. Plant Cell 10:937-946 https://doi.org/10.1105/tpc.10.6.937
  65. Salmeron, J. M., Oldroyd, G. E. D., Rommen, C. M. T., Scofield, S. R, Kim, H.-S., Lavelle, D. T., Dahlbeck, D. and Staskawicz, B. J. 1996. Tomato Prj is a member of the leucine rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell 86: 123-134 https://doi.org/10.1016/S0092-8674(00)80083-5
  66. Schneid, O. M., Asfar, K. and Paszkowski, J. 1998. Release of epigenetic gene silencing by trans-acting mutations in Arabidopsis. Proc. Natl. Acad. Sci. USA 95:632-637 https://doi.org/10.1073/pnas.95.2.632
  67. Schneider, D. S. 2002. Plant immunity and film noir: what gumshoe detectives can teach us about plant-pathogen interactions. Cell 109:537-540 https://doi.org/10.1016/S0092-8674(02)00764-X
  68. Shao, F, Merritt, P. M., Bao, Z., Innes, R. W. and Dixon, J. E. 2002. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109:575-588 https://doi.org/10.1016/S0092-8674(02)00766-3
  69. Sijen, T., Fleener, A., Simmer, F, Thijssen, L., Parrish, S., Timmons, L., Plasterk, R. H. A and Fire, A. 2001. On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107:465-476 https://doi.org/10.1016/S0092-8674(01)00576-1
  70. Smardon, A., Spoerke, J. M., Stacey, S. C., Klein, M. E., Mackin, N. and Maine, E. M. 2000. EGO-l is related to RNA-directed RNA polymerase and functions in germ-line development and RNA interference in Caenorhabditis elegans. Curr. Biol. 10: 169-178 https://doi.org/10.1016/S0960-9822(00)00323-7
  71. Sonoda, S. and Nishiguchi, M. 2000. Graft transmission of posttranscriptional gene silencing: target specificity for RNA degradation is transmissible between silenced and non-silenced plants, but not between silenced plants. Plant J. 21: 1-8 https://doi.org/10.1046/j.1365-313x.2000.00645.x
  72. Sticher, L., Mauch-Mani, B. and Metraux, J. P. 1997. Systemic acquired resistance. Annu. Rev. Plant Pathol. 35: 235-270
  73. Taraporewala, Z. F. and Culver, J. N. 1996. Identification of an elicitor active site within the three-dimensional structure of the tobacco mosaic tobamovirus coat protein. Plant Cell 8: 169-178 https://doi.org/10.1105/tpc.8.2.169
  74. Thomas, C. L., Leh, V., Lederer, C. and Maule, A. J. 2003. Turnip crinkle virus coat protein mediates suppression of RNA silencing in Nicotiana benthamiana. Virology 306:33-41 https://doi.org/10.1016/S0042-6822(02)00018-1
  75. Turnage, M. A., Muangsan, N., Peele, C. G. and Robertson, D. 2002. Geminivirus-based vectors for gene silencing in Arabidopsis. Plant J. 30:107-114 https://doi.org/10.1046/j.1365-313X.2002.01261.x
  76. van der Biezen, E. A. and Jones, J. D. G. 1998. Plant diseaseresistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23:454-456 https://doi.org/10.1016/S0968-0004(98)01311-5
  77. 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 RNAdependent RNA polymerase.Plant Cell 14:857-867 https://doi.org/10.1105/tpc.010480
  78. Vance, V. and Vaucheret, H. 2001. RNA silencing in plants: defense and counterdefense. Science 292:2277-2280 https://doi.org/10.1126/science.1061334
  79. Voinnet, O., Philippe, V., Angell, S. and Baulcombe, D. C. 1998. Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell 95: 177-187 https://doi.org/10.1016/S0092-8674(00)81749-3
  80. Voinnet, O., Pinto, Y. M. and Baulcombe, D. C. 1999. Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc. Natl. Acad. Sci. USA 96:14147-14152 https://doi.org/10.1073/pnas.96.24.14147
  81. 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 https://doi.org/10.1016/S0092-8674(00)00095-7
  82. Wang, M.-B. and Waterhouse, P. M. 2000. High-efficiency silencing of a beta-glucuronidase gene in rice is correlated with repetitive transgene structure but is independent of DNA methylation. Plant Mol. BioI. 43:67-82 https://doi.org/10.1023/A:1006490331303
  83. Wassenegger, M. 2000. RNA-directed DNA methylation. Plant Mol. BioI. 43:67-82 https://doi.org/10.1023/A:1006490331303
  84. Waterhouse, P. M., Graham, M. W. and Wang, M.-B. 1998. Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA Proc. Natl. Acad. Sci. USA 95:13959-13964 https://doi.org/10.1073/pnas.95.23.13959
  85. Waterhouse, P. M., Wang, M.-B. and Lough, T. 2001. Gene silencing as an adaptive defense against viruses. Nature 411 :834-842 https://doi.org/10.1038/35081168
  86. Weber, H., Schultze, S. and Pfizner, A. J. 1993. Two amino acid substitutions in the tomato mosaic virus 30-kilodalton movement protein confer the ability to overcome the Tm-2(2) resistance gene in the tomato. J. Viral. 67:6432-6438
  87. White, F. F., Yang, B. and Johnson, L. B. 2000. Prospects for understanding avirulence gene function. Curr. Opin. Plant BioI. 3:291-298 https://doi.org/10.1016/S1369-5266(00)00082-0
  88. Whitham, S., Dinesh-Kumar, S. P., Choi, D., Hehl, R., Corr, C. and Baker, B. 1994. The product of the tobacco mosaic virus resistance gene N: similarity to Toll and the interleukin-I receptor. Cell 78:1101-1115 https://doi.org/10.1016/0092-8674(94)90283-6
  89. Zamore, P. D., Tuschl, T., Sharp, P. A. and Bartel, D. P. 2000. RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21- to 23-nucleotide intervals. Cell 101:25-33 https://doi.org/10.1016/S0092-8674(00)80620-0
  90. Zhao, Y., DelGrosso, L., Yigit, E., Dempsey, D. A., Klessig, D. F. and Wobbe, K. K. 2000. The amino terminus of the coat protein of turnip crinkle virus is the avr factor recognized by resistantArabidopsis. Mol. Plant-Microbe Interact. 13:1015-1018 https://doi.org/10.1094/MPMI.2000.13.9.1015

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