Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Mechanisms of plant resistance to viruses

Key Points

  • Several models that describe plant–virus relationships have been proposed, including compatible and incompatible interactions.

  • Plants contain resistance (R) genes, which confer resistance to pathogens, with each R gene conferring resistance to a particular pathogen. Several R genes have been cloned and some structure/function analyses performed.

  • There are two current models for pathogen recognition by plant R proteins, which are the receptor–ligand model and the guard hypothesis.

  • Several molecules and signalling pathways are induced upon pathogen recognition, and they cooperate to produce a defence response. Some of the best characterized molecules include salicylic acid, nitric oxide and reactive oxygen species, in addition to several plant hormones.

  • RNA silencing is a highly conserved pathway in animals and plants that functions in development and in the maintenance of genome integrity. Plants have adapted this system for antiviral defence, and plant viruses have in turn developed mechanisms to suppress RNA silencing.

  • The two pathways — RNA silencing and R-gene-mediated resistance — might interact to produce an effective defence response in plants.

Abstract

Plants have evolved in an environment rich with microorganisms that are eager to capitalize on the plants' biosynthetic and energy-producing capabilities. There are approximately 450 species of plant-pathogenic viruses, which cause a range of diseases. However, plants have not been passive in the face of these assaults, but have developed elaborate and effective defence mechanisms to prevent, or limit, damage owing to viral infection. Plant resistance genes confer resistance to various pathogens, including viruses. The defence response that is initiated after detection of a specific virus is stereotypical, and the cellular and physiological features associated with it have been well characterized. Recently, RNA silencing has gained prominence as an important cellular pathway for defence against foreign nucleic acids, including viruses. These pathways function in concert to result in effective protection against virus infection in plants.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Local and systemic resistance mediated by resistance (R) genes.
Figure 2: The receptor–ligand hypothesis versus the guard hypothesis.
Figure 3: Recovery.

References

  1. Legg, J. P. & Fauquet, C. M. Cassava mosaic geminiviruses in Africa. Plant Mol. Biol. 56, 585–599 (2004).

    Article  CAS  PubMed  Google Scholar 

  2. Martin, G. B., Bogdanove, A. J. & Sessa, G. Understanding the functions of plant disease resistance proteins. Annu. Rev. Plant Biol. 54, 23–61 (2003).

    Article  CAS  PubMed  Google Scholar 

  3. van der Biezen, E. A. & Jones, J. D. The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr. Biol. 8, R226–R227 (1998).

    Article  CAS  PubMed  Google Scholar 

  4. Tameling, W. I. et al. The tomato R gene products I-2 and MI-1 are functional ATP binding proteins with ATPase activity. Plant Cell 14, 2929–2939 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Bell, J. K. et al. Leucine-rich repeats and pathogen recognition in Toll-like receptors. Trends Immunol. 24, 528–533 (2003).

    Article  CAS  PubMed  Google Scholar 

  6. Inohara, N. & Nunez, G. NODs: intracellular proteins involved in inflammation and apoptosis. Nature Rev. Immunol. 3, 371–382 (2003).

    Article  CAS  Google Scholar 

  7. Whitham, S. et al. The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78, 1101–1115 (1994).

    Article  CAS  PubMed  Google Scholar 

  8. Vidal, S., Cabrera, H., Andersson, R. A., Fredriksson, A. & Valkonen, J. P. Potato gene Y-1 is an N gene homolog that confers cell death upon infection with potato virus Y. Mol. Plant Microbe Interact. 15, 717–727 (2002).

    Article  CAS  PubMed  Google Scholar 

  9. Jebanathirajah, J. A., Peri, S. & Pandey, A. Toll and interleukin-1 receptor (TIR) domain-containing proteins in plants: a genomic perspective. Trends Plant Sci. 7, 388–391 (2002).

    Article  CAS  PubMed  Google Scholar 

  10. Takahashi, H. et al. Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism. Plant J. 32, 655–667 (2002).

    Article  CAS  PubMed  Google Scholar 

  11. Dinesh-Kumar, S. P., Tham, W. -H. & Baker, B. The structure–function analysis of the tobacco mosaic resistance gene N. Proc. Natl Acad. Sci. USA 97, 14789–14794 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Bendahmane, A., Farnham, G., Moffett, P. & Baulcombe, D. C. Constitutive gain-of-function mutants in a nucleotide binding site-leucine rich repeat protein encoded at the Rx locus of potato. Plant J. 32, 195–204 (2002).

    Article  CAS  PubMed  Google Scholar 

  13. Ellis, J. G., Lawrence, G. J., Luck, J. E. & Dodds, P. N. Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 11, 495–506 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Jordan, T., Schornack, S. & Lahaye, T. Alternative splicing of transcripts encoding Toll-like plant resistance proteins — what's the functional relevance to innate immunity? Trends Plant Sci. 7, 392–398 (2002).

    Article  CAS  PubMed  Google Scholar 

  15. Dinesh-Kumar, S. P. & Baker, B. Alternatively spliced N resistance gene transcripts: their possible role in tobacco mosaic virus resistance. Proc. Natl Acad. Sci. USA 97, 1908–1913 (2000). This paper is the first detailed characterization of alternative splicing in TIR-NB-ARC-LRR R genes and the involvement of both transcripts in resistance.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Iwami, K. I. et al. Cutting edge: naturally occurring soluble form of mouse Toll-like receptor 4 inhibits lipopolysaccharide signaling. J. Immunol. 165, 6682–6686 (2000).

    Article  CAS  PubMed  Google Scholar 

  17. Moffett, P., Farnham, G., Peart, J. & Baulcombe, D. C. Interaction between domains of a plant NBS-LRR protein in disease resistance-related cell death. EMBO J. 21, 4511–4519 (2002). In this study, the authors provide evidence for intramolecular interactions within R proteins. These interactions might be disrupted upon pathogen infection, raising many questions regarding R-protein complexes and pathogen detection.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Hwang, C. F. & Williamson, V. M. Leucine-rich repeat-mediated intramolecular interactions in nematode recognition and cell death signaling by the tomato resistance protein Mi. Plant J. 34, 585–593 (2003).

    Article  CAS  PubMed  Google Scholar 

  19. Van der Biezen, E. A. & Jones, J. D. Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23, 454–456 (1998).

    Article  CAS  PubMed  Google Scholar 

  20. Mackey, D., Belkhadir, Y., Alonso, J. M., Ecker, J. R. & Dangl, J. L. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112, 379–389 (2003).

    Article  CAS  PubMed  Google Scholar 

  21. Mackey, D., Holt, B. F., Wiig, A. & Dangl, J. L. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108, 743–754 (2002).

    Article  CAS  PubMed  Google Scholar 

  22. Axtell, M. J. & Staskawicz, B. J. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112, 369–377 (2003).

    Article  CAS  PubMed  Google Scholar 

  23. Shao, F. et al. Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301, 1230–1233 (2003). Experimental evidence in support of the guard hypothesis is provided by references 20–23.

    Article  CAS  PubMed  Google Scholar 

  24. Ren, T., Qu, F. & Morris, T. J. 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 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Ren, T., Qu, F. & Morris, T. J. The nuclear localization of the Arabidopsis transcription factor TIP is blocked by its interaction with the coat protein of Turnip crinkle virus. Virology 331, 316–324 (2005).

    Article  CAS  PubMed  Google Scholar 

  26. Meyers, B. C., Kozik, A., Griego, A., Kuang, H. & Michelmore, R. W. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15, 809–834 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Lu, R. et al. High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J. 22, 5690–5699 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Hubert, D. A. et al. Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. EMBO J. 22, 5679–5689 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Takahashi, A., Casais, C., Ichimura, K. & Shirasu, K. HSP90 interacts with Rar1 and Sgt1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc. Natl Acad. Sci. USA 100, 11777–11782 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Liu, Y., Burch-Smith, T., Schiff, M., Feng, S. & Dinesh-Kumar, S. P. Molecular chaperone Hsp90 associates with resistance protein N and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants. J. Biol. Chem. 279, 2101–2108 (2004).

    Article  CAS  PubMed  Google Scholar 

  31. Rudd, J. J. & Franklin-Tong, V. E. Unravelling response-specificity in Ca2+ signalling pathways in plant cells. New Phytol. 151, 7–33 (2001).

    Article  CAS  PubMed  Google Scholar 

  32. Jin, H. et al. Function of a mitogen-activated protein kinase pathway in N gene-mediated resistance in tobacco. Plant J. 33, 719–731 (2003).

    Article  CAS  PubMed  Google Scholar 

  33. Liu, Y., Schiff, M. & Dinesh-Kumar, S. P. Involvement of MEK1 MAPKK, NTF6 MAPK, WRKY/MYB transcription factors, COI1 and CTR1 in N-mediated resistance to tobacco mosaic virus. Plant J. 38, 800–809 (2004).

    Article  CAS  PubMed  Google Scholar 

  34. Zhang, S. & Klessig, D. F. MAPK cascade in plant defense signaling. Trends Plant Sci. 6, 520–527 (2001).

    Article  CAS  PubMed  Google Scholar 

  35. Kim, C. Y. & Zhang, S. Activation of a mitogen-activated protein kinase cascade induces WRKY family of transcription factors and defense genes in tobacco. Plant J. 38, 142–151 (2004).

    Article  CAS  PubMed  Google Scholar 

  36. Marathe, R., Guan, Z., Anandalakshmi, R., Zhao, H. & Dinesh-Kumar, S. P. Study of Arabidopsis thaliana resistome in response to cucumber mosaic virus infection using whole genome microarray. Plant Mol. Biol. 55, 501–520 (2004).

    Article  CAS  PubMed  Google Scholar 

  37. Vranova, E., Inze, D. & Van Breusegem, F. Signal transduction during oxidative stress. J. Exp. Bot. 53, 1227–1236 (2002).

    Article  CAS  PubMed  Google Scholar 

  38. Mittler, R., Vanderauwera, S., Gollery, M. & Van Breusegem, F. Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490–498 (2004).

    Article  CAS  PubMed  Google Scholar 

  39. Keller, T. et al. A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs. Plant Cell 10, 255–266 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Overmyer, K., Brosche, M. & Kangasjarvi, J. Reactive oxygen species and hormonal control of cell death. Trends Plant Sci. 8, 335–342 (2003).

    Article  CAS  PubMed  Google Scholar 

  41. Ordog, S. H., Higgins, V. J. & Vanlerberghe, G. C. Mitochondrial alternative oxidase is not a critical component of plant viral resistance but may play a role in the hypersensitive response. Plant Physiol. 129, 1858–1865 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Gilliland, A. et al. 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 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Delledonne, M., Xia, Y., Dixon, R. A. & Lamb, C. Nitric oxide functions as a signal in plant disease resistance. Nature 394, 585–588 (1998).

    Article  CAS  PubMed  Google Scholar 

  44. Durner, J., Wendehenne, D. & Klessig, D. F. Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc. Natl Acad. Sci. USA 95, 10328–10333 (1998). The role of NO in plant defence was first identified in references 43 and 44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. del Rio, L. A., Corpas, F. J. & Barroso, J. B. Nitric oxide and nitric oxide synthase activity in plants. Phytochemistry 65, 783–792 (2004).

    Article  CAS  PubMed  Google Scholar 

  46. Guo, F. Q., Okamoto, M. & Crawford, N. M. Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302, 100–103 (2003). In a series of elegant experiments, the authors identify a plant protein that is responsible for the induction of NO synthesis in response to pathogen infection and hormone signals.

    Article  CAS  PubMed  Google Scholar 

  47. Zeidler, D. et al. Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. Proc. Natl Acad. Sci. USA 101, 15811–15816 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Fang, F. C. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nature Rev. Microbiol. 2, 820–832 (2004).

    Article  CAS  Google Scholar 

  49. Turner, J. G., Ellis, C. & Devoto, A. The jasmonate signal pathway. Plant Cell 14, S153–S164 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Guo, H. & Ecker, J. R. The ethylene signaling pathway: new insights. Curr. Opin. Plant Biol. 7, 40–49 (2004).

    Article  CAS  PubMed  Google Scholar 

  51. Durrant, W. E. & Dong, X. Systemic acquired resistance. Annu. Rev. Phytopathol. 42, 185–209 (2004).

    Article  CAS  PubMed  Google Scholar 

  52. Glazebrook, J. et al. Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant J. 34, 217–228 (2003).

    Article  CAS  PubMed  Google Scholar 

  53. Greenberg, J. T. & Yao, N. The role and regulation of programmed cell death in plant–pathogen interactions. Cell. Microbiol. 6, 201–211 (2004).

    Article  CAS  PubMed  Google Scholar 

  54. Lorrain, S., Vailleau, F., Balague, C. & Roby, D. Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci. 8, 263–271 (2003).

    Article  CAS  PubMed  Google Scholar 

  55. Liu, Y. et al. Autophagy regulates programmed cell death during the plant innate immune response. Cell 121, 567–577 (2005).

    Article  CAS  PubMed  Google Scholar 

  56. Lam, E. Controlled cell death, plant survival and development. Nature Rev. Mol. Cell Biol. 5, 305–315 (2004).

    Article  CAS  Google Scholar 

  57. Chichkova, N. V. et al. A plant caspase-like protease activated during the hypersensitive response. Plant Cell 16, 157–171 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Hatsugai, N. et al. A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 305, 855–858 (2004).

    Article  CAS  PubMed  Google Scholar 

  59. Rojo, E. et al. VPEγ exhibits a caspase-like activity that contributes to defense against pathogens. Curr. Biol. 14, 1897–1906 (2004). Plant proteases with a caspase-like activity that is required for the HR PCD are identified in references 57–59.

    Article  CAS  PubMed  Google Scholar 

  60. Bendahmane, A., Kanyuka, K. & Baulcombe, D. C. The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell 11, 781–791 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Lanfermeijer, F. C., Dijkhuis, J., Sturre, M. J., de Haan, P. & Hille, J. Cloning and characterization of the durable tomato mosaic virus resistance gene Tm-22 from Lycopersicon esculentum. Plant Mol. Biol. 52, 1037–1049 (2003).

    Article  CAS  PubMed  Google Scholar 

  62. Smalle, J. & Vierstra, R. D. The ubiquitin 26S proteasome proteolytic pathway. Annu. Rev. Plant Biol. 55, 555–590 (2004).

    Article  CAS  PubMed  Google Scholar 

  63. Holt, B. F., 3rd, Hubert, D. A. & Dangl, J. L. Resistance gene signaling in plants — complex similarities to animal innate immunity. Curr. Opin. Immunol. 15, 20–25 (2003).

    Article  CAS  PubMed  Google Scholar 

  64. Wei, N. & Deng, X. W. The COP9 signalosome. Annu. Rev. Cell Dev. Biol. 19, 261–286 (2003).

    Article  CAS  PubMed  Google Scholar 

  65. Azevedo, C. et al. The Rar1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295, 2073–2076 (2002).

    Article  CAS  PubMed  Google Scholar 

  66. Liu, Y., Schiff, M., Serino, G., Deng, X. -W. & Dinesh-Kumar, S. P. Role of SCF ubiquitin-ligase and the COP9 signalosome in the N gene-mediated resistance response to tobacco mosaic virus. Plant Cell 14, 1483–1496 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Feng, S. et al. The COP9 signalosome interacts physically with SCF COI1 and modulates jasmonate responses. Plant Cell 15, 1083–1094 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Vernooij, B. et al. Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell 6, 959–965 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Kumar, D. & Klessig, D. F. High-affinity salicylic acid-binding protein 2 is required for plant innate immunity and has salicylic acid-stimulated lipase activity. Proc. Natl Acad. Sci. USA 100, 16101–16106 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Maldonado, A. M., Doerner, P., Dixon, R. A., Lamb, C. J. & Cameron, R. K. A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419, 399–403 (2002). For many years, the molecule responsible for signalling SAR has eluded scientists, and this paper identifies a mutation that disrupts SAR while local resistance remains unaffected. A putative lipid-binding protein was identified, indicating that a lipid-derived signal might be the long-sought systemic signal.

    Article  CAS  PubMed  Google Scholar 

  71. Feys, B. J., Moisan, L. J., Newman, M. A. & Parker, J. E. Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO J. 20, 5400–5411 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Baulcombe, D. RNA silencing in plants. Nature 431, 356–363 (2004).

    Article  CAS  PubMed  Google Scholar 

  73. Meister, G. & Tuschl, T. Mechanisms of gene silencing by double-stranded RNA. Nature 431, 343–349 (2004).

    Article  CAS  PubMed  Google Scholar 

  74. Hull, R. Matthews' Plant Virology 4th edn 27–42 (Academic Press, New York, 2002).

    Google Scholar 

  75. Waterhouse, P. M., Graham, M., W. & Wang, M. -B. Virus resistance and gene silencing in plants is induced by double stranded RNA. Proc. Natl Acad. Sci. USA 95, 13959–13964 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Dalmay, T., Hamilton, A., Rudd, S., Angell, S. & Baulcombe, D. C. 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 (2000).

    Article  CAS  PubMed  Google Scholar 

  77. Klumpp, K., Ruigrok, R. W. & Baudin, F. Roles of the influenza virus polymerase and nucleoprotein in forming a functional RNP structure. EMBO J. 16, 1248–1257 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Ahlquist, P. RNA-dependent RNA polymerases, viruses, and RNA silencing. Science 296, 1270–1273 (2002).

    Article  CAS  PubMed  Google Scholar 

  79. Xie, Z. et al. Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2, E104 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  80. Mourrain, P. et al. Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101, 533–542 (2000).

    Article  CAS  PubMed  Google Scholar 

  81. Xie, Z., Fan, B., Chen, C. & Chen, Z. An important role of an inducible RNA-dependent RNA polymerase in plant antiviral defense. Proc. Natl Acad. Sci. USA 98, 6516–6521 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Yang, S. J., Carter, S. A., Cole, A. B., Cheng, N. H. & Nelson, R. S. A natural variant of a host RNA-dependent RNA polymerase is associated with increased susceptibility to viruses by Nicotiana benthamiana. Proc. Natl Acad. Sci. USA 101, 6297–6302 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Yu, D., Fan, B., MacFarlane, S. A. & Chen, Z. Analysis of the involvement of an inducible Arabidopsis RNA-dependent RNA polymerase in antiviral defense. Mol. Plant Microbe Interact. 16, 206–216 (2003).

    Article  CAS  PubMed  Google Scholar 

  84. Chapman, E. J., Prokhnevsky, A. I., Gopinath, K., Dolja, V. V. & Carrington, J. C. Viral RNA silencing suppressors inhibit the microRNA pathway at an intermediate step. Genes Dev. 18, 1179–1186 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Ye, K., Malinina, L. & Patel, D. J. Recognition of small interfering RNA by a viral suppressor of RNA silencing. Nature 426, 874–878 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Vargason, J. M., Szittya, G., Burgyan, J. & Tanaka Hall, T. M. Size selective recognition of siRNA by an RNA silencing suppressor. Cell 115, 799–811 (2003). This paper and reference 85 report the first crystal structures of a viral suppressor bound to siRNAs, clearly showing the importance of the 21-nucleotide length of an siRNA.

    Article  CAS  PubMed  Google Scholar 

  87. Pruss, G., Ge, X., Shi, X. M., Carrington, J. C. & Bowman Vance, V. Plant viral synergism: the potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses. Plant Cell 9, 859–868 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Vance, V. & Vaucheret, H. RNA silencing in plants-defense and counterdefense. Science 292, 2277–2280 (2001).

    Article  CAS  PubMed  Google Scholar 

  89. Kasschau, K. D. & Carrington, J. C. Long-distance movement and replication maintenance functions correlate with silencing suppression activity of potyviral HC-Pro. Virology 285, 71–81 (2001).

    Article  CAS  PubMed  Google Scholar 

  90. Mallory, A. C., Reinhart, B. J., Bartel, D., Vance, V. B. & Bowman, L. H. A viral suppressor of RNA silencing differentially regulates the accumulation of short interfering RNAs and micro-RNAs in tobacco. Proc. Natl Acad. Sci. USA 99, 15228–15233 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Kasschau, K. D. et al. P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev. Cell 4, 205–217 (2003).

    Article  CAS  PubMed  Google Scholar 

  92. Dunoyer, P., Lecellier, C. H., Parizotto, E. A., Himber, C. & Voinnet, O. Probing the microRNA and small interfering RNA pathways with virus-encoded suppressors of RNA silencing. Plant Cell 16, 1235–1250 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Qu, F., Ren, T. & Morris, T. J. The coat protein of turnip crinkle virus suppresses posttranscriptional gene silencing at an early initiation step. J. Virol. 77, 511–522 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Choi, C. W., Qu, F., Ren, T., Ye, X. & Morris, T. J. RNA silencing-suppressor function of Turnip crinkle virus coat protein cannot be attributed to its interaction with the Arabidopsis protein TIP. J. Gen. Virol. 85, 3415–3420 (2004).

    Article  CAS  PubMed  Google Scholar 

  95. Pruss, G. J. et al. The potyviral suppressor of RNA silencing confers enhanced resistance to multiple pathogens. Virology 320, 107–120 (2004). The authors examine how a viral RNA silencing suppressor protein affects R -gene-mediated resistance. This is the first demonstration that these two pathways interact with each other.

    Article  CAS  PubMed  Google Scholar 

  96. Mello, C. C. & Conte, D., Jr. Revealing the world of RNA interference. Nature 431, 338–342 (2004).

    Article  CAS  PubMed  Google Scholar 

  97. Finnegan, E. J. & Matzke, M. A. The small RNA world. J. Cell Sci. 116, 4689–4693 (2003).

    Article  CAS  PubMed  Google Scholar 

  98. Hamilton, A. J. & Baulcombe, D. C. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286, 950–952 (1999).

    Article  CAS  PubMed  Google Scholar 

  99. Bartel, D. P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281–297 (2004).

    Article  CAS  PubMed  Google Scholar 

  100. Mlotshwa, S. et al. RNA silencing and the mobile silencing signal. Plant Cell 14, S289–S301 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Yoo, B. C. et al. A systemic small RNA signaling system in plants. Plant Cell 16, 1979–2000 (2004). The authors provide evidence for the systemic movement of siRNAs through the phloem of a plant. This points to siRNA as the systemic signal for silencing.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Ratcliff, F., Harrison, B. D. & Baulcombe, D. C. A similarity between viral defense and gene silencing in plants. Science 276, 1558–1560 (1997).

    Article  CAS  PubMed  Google Scholar 

  103. Bendahmane, A., Querci, M., Kanyuka, K. & Baulcombe, D. C. Agrobacterium transient expression system as a tool for the isolation of disease resistance genes: application to the Rx2 locus in potato. Plant J. 21, 73–81 (2000).

    Article  CAS  PubMed  Google Scholar 

  104. Cooley, M. B., Pathirana, S., Wu, H.-J., Kachroo, P. & Klessig, D. F. Members of the Arabidopsis HRT/RPP8 family of resistance genes confer resistance to both viral and oomycete pathogens. Plant Cell 12, 663–676 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Spassova, M. I. et al. The tomato gene Sw5 is a member of the coiled coil, nucleotide binding, leucine-rich repeat class of plant resistance genes and confers resistance to TSWV in tobacco. Mol. Breed. 7, 151–161 (2001).

    Article  CAS  Google Scholar 

  106. Voinnet, O., Pinto, Y. M. & Baulcombe, D. C. Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc. Natl Acad. Sci. USA 96, 14147–14152 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Yelina, N. E., Savenkov, E. I., Solovyev, A. G., Morozov, S. Y. & Valkonen, J. P. 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 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Dunoyer, P. et al. Identification, subcellular localization and some properties of a cysteine-rich suppressor of gene silencing encoded by peanut clump virus. Plant J. 29, 555–567 (2002).

    Article  CAS  PubMed  Google Scholar 

  109. Pfeffer, S. et al. P0 of beet Western yellows virus is a suppressor of posttranscriptional gene silencing. J. Virol. 76, 6815–6824 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Reed, J. C. et al. Suppressor of RNA silencing encoded by Beet yellows virus. Virology 306, 203–209 (2003).

    Article  CAS  PubMed  Google Scholar 

  111. Satyanarayana, T. et al. Closterovirus encoded HSP70 homolog and p61 in addition to both coat proteins function in efficient virion assembly. Virology 278, 253–265 (2000).

    Article  CAS  PubMed  Google Scholar 

  112. Lu, R. et al. Three distinct suppressors of RNA silencing encoded by a 20-kb viral RNA genome. Proc. Natl Acad. Sci. USA (2004).

  113. Sambade, A. et al. Polymorphism of a specific region in gene p23 of Citrus tristeza virus allows discrimination between mild and severe isolates. Arch. Virol. 148, 2325–2340 (2003).

    Article  CAS  PubMed  Google Scholar 

  114. Brigneti, G., Voinnet, O., Li, W.-X., Ding, S. W. & Baulcombe, D. C. Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J. 17, 6739–6746 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Ji, L. H. & Ding, S. W. The suppressor of transgene RNA silencing encoded by Cucumber mosaic virus interferes with salicylic acid-mediated virus resistance. Mol. Plant Microbe Interact. 14, 715–724 (2001).

    Article  CAS  PubMed  Google Scholar 

  116. Voinnet, O., Lederer, C. & Baulcombe, D. C. A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 103, 157–167 (2000).

    Article  CAS  PubMed  Google Scholar 

  117. Bucher, E., Sijen, T., De Haan, P., Goldbach, R. & Prins, M. Negative-strand tospoviruses and tenuiviruses carry a gene for a suppressor of gene silencing at analogous genomic positions. J. Virol. 77, 1329–1336 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Anadalakshmi, R. et al. A viral suppressor of gene silencing in plants. Proc. Natl Acad. Sci. USA 95, 13079–13084 (1998).

    Article  Google Scholar 

  119. Ding, X. S. et al. The Tobacco mosaic virus 126-kDa protein associated with virus replication and movement suppresses RNA silencing. Mol. Plant Microbe Interact. 17, 583–592 (2004).

    Article  CAS  PubMed  Google Scholar 

  120. Liu, H., Reavy, B., Swanson, M. & MacFarlane, S. A. Functional replacement of the tobacco rattle virus cysteine-rich protein by pathogenicity proteins from unrelated plant viruses. Virology 298, 232–239 (2002).

    Article  CAS  PubMed  Google Scholar 

  121. Kubota, K., Tsuda, S., Tamai, A. & Meshi, T. Tomato mosaic virus replication protein suppresses virus-targeted posttranscriptional gene silencing. J. Virol. 77, 11016–11026 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Takeda, A. et al. Identification of a novel RNA silencing suppressor, NSs protein of Tomato spotted wilt virus. FEBS Lett. 532, 75–79 (2002).

    Article  CAS  PubMed  Google Scholar 

  123. van Wezel, R. et al. Mutation of three cysteine residues in Tomato yellow leaf curl virus-China C2 protein causes dysfunction in pathogenesis and posttranscriptional gene-silencing suppression. Mol. Plant Microbe Interact. 15, 203–208 (2002).

    Article  CAS  PubMed  Google Scholar 

  124. Thomas, C. L., Leh, V., Lederer, C. & Maule, A. J. Turnip crinkle virus coat protein mediates suppression of RNA silencing in Nicotiana benthamiana. Virology 306, 33–41 (2003).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We apologize to our colleagues whose work we were unable to include owing to space constraints. We thank Dr S. Ekengren and members of the Dinesh-Kumar laboratory for critical reading of the manuscript. The Dinesh-Kumar laboratory is supported by the National Institutes of Health, the National Science Foundation's Plant Genome and 2010 Programs, the Hellman Family Fellowship and Yale University Genomics and Proteomics grants.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Savithramma P. Dinesh-Kumar.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

DATABASES

Entrez

cucumber mosaic virus

peanut clump virus

potato virus X

Pseudomonas syringae pv. tomato

tobacco etch potyvirus

tobacco mosaic virus

tomato bushy stunt virus

turnip crinkle virus

turnip mosaic virus

Swiss-Prot

AvrB

AvrPphB

AvrRpm

RIN4

RPS2

TAIR

DCL2

DIR1

dir1-1

eds1

HRT

pad4

PBS1

RCY1

RDR1

RDR6

RPM1

RPP8

RPS5

FURTHER INFORMATION

The Dinesh-Kumar laboratory

Glossary

INNATE IMMUNITY

The suite of host responses to pathogens that result in rapid defence without requiring prior stimulation.

CHAPERONES

Chaperones are a large group of highly conserved proteins that assist other polypeptides in folding, stabilize large complexes and ensure correct localization of proteins. Although constitutively expressed, they are typically induced to higher levels by stress and are crucial for cell survival under these conditions.

AUTOPHAGY

Autophagy, meaning to eat (phagy) oneself (auto), is the cellular pathway for the degradation of both long-lived proteins and organelles that is involved in cellular development, innate immunity and starvation responses. Substrates are packaged in double-membraned vesicles and targeted to lysosomes and vacuoles for processing and degradation.

DICER

DICER is a member of the RNase III family of nucleases that specifically cleave dsRNAs. DICER processes long dsRNA into siRNAs of 21–23 nucleotides.

SYNERGISTIC INFECTION

An infection by two unrelated viruses during which one virus can replicate to higher-than-normal levels owing to the presence of the other virus.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Soosaar, J., Burch-Smith, T. & Dinesh-Kumar, S. Mechanisms of plant resistance to viruses. Nat Rev Microbiol 3, 789–798 (2005). https://doi.org/10.1038/nrmicro1239

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro1239

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing