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Host Gene-mediated Virus Resistance Mechanisms and Signaling in Arabidopsis

  • Chapter
Natural Resistance Mechanisms of Plants to Viruses

Abstract

Plants resist viral infections either via an active mechanism, involving the participation of resistance (R) genes and subsequent signal transduction pathways, or in a passive manner, which entails the absence of essential host factors required for replication or movement of the virus. An active resistance response involves strain-specific recognition of a virus-encoded elicitor, through direct or indirect interaction with the corresponding R gene product. This in turn activates downstream signaling, which leads to prevention of viral spread and confers resistance against the pathogen. An R gene-mediated recognition of virus often turns on defense responses such as the accumulation of salicylic acid (SA), the expression of pathogenesisrelated (PR) genes, and the development of a hypersensitive response (HR) on the inoculated leaves. The HR is defined by necrotic lesion formation at the site of infection and is thought to help prevent multiplication and movement by confining the virus to the region immediately surrounding the necrotic lesions.

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References

  • Aarts, N., Metz, M., Holub, E., Staskawicz, B.J., Daniels, M.J. and Parker, J.E. 1998. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc. Natl. Acad. Sci. USA. 95: 10306–10311.

    Article  PubMed  CAS  Google Scholar 

  • Austin, M.J., Muskett, P., Kahn, K., Feys, B.J., Jones, J.D. and Parker, J.E. 2002. Regulatory role of SGT1 in early R gene-mediated plant defenses. Science 295: 2077–2080.

    Article  PubMed  CAS  Google Scholar 

  • Azevedo, C., Sadanandom, A., Kitagawa, K., Freialdenhoven, A., Shirasu, K. and Schulze-Lefert, P. 2002. The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science, 295: 2073–2076.

    Article  PubMed  CAS  Google Scholar 

  • Callaway, A., Liu, W., Andrianov, V., Stenzler, L., Zhao, J., Wettlaufer, S., Jayakumar, P. and Howell, S.H. 1996. Characterization of cauliflower mosaic virus (CaMV) resistance in virus-resistant ecotypes of Arabidopsis. Mol. Plant-Microbe Interact. 9: 810–818.

    PubMed  CAS  Google Scholar 

  • Cao, H., Glazebrook, J., Clarke, J.D., Volko, S. and Dong, X. 1997. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88: 57–63.

    Article  PubMed  CAS  Google Scholar 

  • Chandra-Shekara, A.C., Navarre, D., Kachroo, A., Kang, H-G., Klessig, D., and Kachroo, P. 2004. Signaling requirements and role of salicylic acid in HRT-and rrt-mediated resistance to turnip crinkle virus in Arabidopsis. Plant J. In press

    Google Scholar 

  • Chisholm, S.T., Mahajan, S.K, Whitham, S.A., Yamamoto, M and. Carrington, J.C. 2000. Cloning of the Arabidopsis RTM1 gene, which controls restriction of long-distance movement of tobacco etch virus. Proc. Natl. Acad. Sci. USA. 97: 489–494.

    Article  PubMed  CAS  Google Scholar 

  • Chivasa, S. and Carr, J.P. 1998. Cyanide restores N gene-mediated resistance to tobacco mosaic virus in transgenic tobacco expressing salicylic acid hydroxylase. Plant Cell 10: 1489–1498.

    Article  PubMed  CAS  Google Scholar 

  • Chivasa, S., Murphy, A.M., Naylor, M. Carr, J.P. 1997. Salicylic acid interferes with tobacco mosaic virus replication via a novel salicylhydroxamic acid-sensitive mechanism. Plant Cell 9: 547–557.

    Article  PubMed  CAS  Google Scholar 

  • Cooley, M.B., 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.

    Article  PubMed  CAS  Google Scholar 

  • Dangl, J.L. and Jones J.D. 2001. Defence responses to infection. Nature 411: 826–833.

    Article  PubMed  CAS  Google Scholar 

  • Dardick, C.D., Golem, S. and Culver, J.N. 2000. Susceptibility and symptom development in Arabidosis thaliana to Tobacco mosaic virus is influenced by virus cell-to-cell movement. Mol. Plant-Microbe. Interact. 13: 1139–1144.

    Article  PubMed  CAS  Google Scholar 

  • Dempsey, D.A., Pathirana, M.S., Wobbe, K.K. and Klessig, D.F. 1997. Identification of an Arabidopsis locus required for resistance to turnip crinkle virus. Plant J. 2: 301–311.

    Article  Google Scholar 

  • Dempsey, D.A., Wobbe, K.K. and Klessig, D.F. 1993. Resistance and susceptible responses of Arabidopsis thaliana to turnip crinkle virus. Phytopathology 83: 1021–1029.

    Article  CAS  Google Scholar 

  • Dzianott, A. and Bujarski, J.J. 2004. Infection and RNA recombination of Brome mosaic virus in Arabidopsis thaliana. Virology 318: 482–492.

    Article  PubMed  CAS  Google Scholar 

  • Falk, A., Feys, B.J., Frost, L.N., Jones, J.D., Daniels, M.J. and Parker, J.E. 1999. EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc. Natl. Acad. Sci. USA. 96: 3292–3297.

    Article  PubMed  CAS  Google Scholar 

  • Fujisaki, K., Hagihara, F., Azukawa, Y., Kaido, M., Okuno, T. and Mise, K. 2004. Identification and characterization of the SSB1 locus involved in symptom development by spring beauty latent virus infection in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 9: 967–975.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Golem, S. and Culver, J.N. 2003. Tobacco mosaic virus induced alterations in the gene expression profile of Arabidopsis thaliana. Mol. Plant-Microbe. Interact. 16: 681–688.

    Article  PubMed  CAS  Google Scholar 

  • Hubert, D. A., Tornero, P., Belkhadir, Y., Krishna, P., Takahashi, A., Shirasu, K. and Dangl, J.L. 2003. Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. EMBO J. 22: 5679–5689.

    Article  PubMed  CAS  Google Scholar 

  • Ishihara, T., Sakurai, N., Sekine, K. T., Hase, S., Ikegami, M., Shibata, D. and Takahashi, H. 2004. Comparative analysis of expressed sequence tags in resistant and susceptible ecotypes of Arabidopsis thaliana infected with cucumber mosaic virus. Plant Cell Physiol. 45: 470–480.

    Article  PubMed  CAS  Google Scholar 

  • Jirage, D., Tootle, T.L., Reuber, T.L., Frost, L.N., Feys, B.J., Parker, J.E., Ausubel, F.M. and Glazebrook, J. 1999. Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc. Natl. Acad. Sci. USA. 96: 13583–13588.

    Article  PubMed  CAS  Google Scholar 

  • Kachroo, P., Kachroo, A., Lapchyk, L., Hildebrand D. and Klessig, D. 2003a. Restoration of defective cross talk in ssi2 mutants; Role of salicylic acid, jasmonic acid and fatty acids in SSI2-mediated signaling. Mol. Plant-Microbe Interact. 11: 1022–1029.

    Article  Google Scholar 

  • Kachroo, A., Lapchyk, L., Fukushigae, H., Hildebrand, D., Klessig, D. and Kachroo, P. 2003b. Plastidial fatty acid signaling modulates salicylic acid-and jasmonic acid-mediated defense pathways in the Arabidopsis ssi2 mutant. Plant cell, 15: 2952–2965.

    Article  PubMed  CAS  Google Scholar 

  • Kachroo, A., Srivathsa C. V., Lapchyk, L., Falcone, D., Hildebrand, D. and Kachroo, P. 2004. Oleic acid levels regulated by glycerolipid metabolism modulate defense gene expression in Arabidopsis. Proc. Natl. Acad. Sci. USA. 101: 5152–5157.

    Article  PubMed  CAS  Google Scholar 

  • Kachroo, P., Shanklin, J., Shah, J., Whittle, E.J. and Klessig, D.F. 2001. A Fatty acid desaturase modulates the activation of defense signaling pathways in Plants. Proc. Natl. Acad. Sci. USA. 98: 9448–9453.

    Article  PubMed  CAS  Google Scholar 

  • Kachroo, P., Yoshioka, K., Shah, J., Dooner, H.K. and Klessig, D.F. 2000. Resistance to turnip crinkle virus in Arabidopsis is regulated by two host genes, is salicylic acid dependent but NPR1, ethylene and jasmonate independent. Plant Cell, 12: 677–690.

    Article  PubMed  CAS  Google Scholar 

  • Kunkel, B.N. and Brooks D.M. 2002. Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol. 5: 325–331.

    Article  PubMed  CAS  Google Scholar 

  • Köhm, B.A., Goulden, M.G., Gilbert, J.E., Kavanagh, T.A. and Baulcombe, D.C. 1993. A potato virus X resistance gene mediates an induced, nonspecific resistance in protoplasts. Plant Cell 8: 913–920.

    Article  Google Scholar 

  • Lartey, R.T., Ghoshroy, S. and Citovsky, V. 1998. Identification of an Arabidopsis thaliana mutation (vsm1) that restricts systemic movement of tobamoviruses. Mol. Plant-Microbe Interact. 11: 706–709.

    Article  PubMed  CAS  Google Scholar 

  • Lee, S., Stenger, D.C., Bisaro, D.M. and Davis, K.R. 1994. Identification of loci in Arabidopsis that confer resistance to geminivirus infection. Plant J. 6: 525–535.

    Article  PubMed  CAS  Google Scholar 

  • Lee, J.M., Hartman, G.L., Domier, L.L. and Bent, A.F. 1996. Identification and map location of TTR1, a single locus in Arabidopsis thaliana that confers tolerance to tobacco ringspot nepovirus. Mol. Plant-Microbe Interact. 9: 729–735.

    PubMed  CAS  Google Scholar 

  • Lee, W-M, Ishikawa, M. and Ahlquist, P. 2001. Mutations of host Δ9 fatty acid desaturase inhibits brome mosaic virus RNA replication between template recognition and RNA synthesis. J. Virol. 75: 2097–2106.

    Article  PubMed  CAS  Google Scholar 

  • Leisner, S.M., Turgeon, R. and Howell, S.H. 1993. Effects of host plant development and genetic determinants on the long-distance movement of cauliflower mosaic virus in Arabidopsis. Plant Cell 5: 191–202.

    Article  PubMed  CAS  Google Scholar 

  • Liu, Y., Schiff, M., Marathe, R. and Dinesh-Kumar, S.P. 2002 Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J. 30: 415–429.

    Article  PubMed  CAS  Google Scholar 

  • Liu, Y., Burch-Smith, T., Schiff, M., Feng, S. and Dinesh-Kumar, S. P. 2004. 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.

    Article  PubMed  CAS  Google Scholar 

  • Luderer, R. and Joosten, M.H.A.J. 2001. Avirulence proteins of plant pathogens: determinants of victory and defeat. Mol. Plant Pathol. 2, 355–364.

    Article  CAS  Google Scholar 

  • Lund, S.T., Stall, R.E. and Klee, H.J. 1998. Ethylene regulates the susceptible response to pathogen infection in tomato. Plant Cell 10: 371–382.

    Article  PubMed  CAS  Google Scholar 

  • Mahajan, S.K., Chisholm, S.T., Whitham, S.A. and Carrington, J.C. 1998. Identification and characterization of a locus (RTM1) that restricts long-distance movement of tobacco etch virus in Arabidopsis thaliana. Plant J. 14: 177–186.

    Article  PubMed  CAS  Google Scholar 

  • Martin, A., Cabrera, Y., Poch, H. L., Martinez-Herrera, D., Ponz, F. 1999. Resistance to turnip mosaic potyvirus in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 12: 1016–1021.

    Article  CAS  Google Scholar 

  • McDowell, J.M., Cuzick, A., Can, C., Beynon, J., Dangl, J.L. and Holub, E.B. 2000. Downy mildew (Peronospora parasitica) resistance genes in Arabidopsis vary in functional requirements for NDR1, EDS1, NPR1 and salicylic acid accumulation. Plant J. 6: 523–529.

    Article  Google Scholar 

  • McDowell, J.M., Dhandaydham, M., Long, T.A., Aarts, M.G., Goff, S., Holub, E.B. and Dangl J.L. 1998. Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell, 10: 1861–1874.

    Article  PubMed  CAS  Google Scholar 

  • Muskett, P.R., Kahn, K., Austin, M.J., Moisan, L.J., Sadanandom, A., Shirasu, K., Jones J.D. and Parker, J.E. 2002. Arabidopsis RAR1 exerts rate-limiting control of R genemediated defenses against multiple pathogens. Plant Cell, 14: 979–992.

    Article  PubMed  CAS  Google Scholar 

  • Nawrath, C. and Métraux, J.P. 1999. Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell, 11: 1393–1404.

    Article  PubMed  CAS  Google Scholar 

  • Nawrath, C., Heck, S., Parinthawong, N. and Métraux, J.P. 2002. EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell 14: 275–286.

    Article  PubMed  CAS  Google Scholar 

  • Naylor, M., Murphy, A.M., Berry, J.O. and Carr, J.P. 1998. Salicylic acid can induce resistance to plant virus movement. Mol. Plant-Microbe. Interact. 11: 860–868.

    Article  CAS  Google Scholar 

  • O’Donnell, P.J., Jones, J.B., Antoine, F.R., Ciardi, J. and Klee, H.J. 2003. Ethylenedependent salicylic acid regulates an expanded cell death response to a plant pathogen. Plant J. 25: 315–323.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Ryals, J., Weymann, K., Lawton, K., Friedrich, L., Ellis, D., Steiner, H.Y., Johnson, J., Delaney, T.P., Jesse, T., Vos, P. and Uknes, S. 1997. The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor I kappa B. Plant Cell 9: 425–439.

    Article  PubMed  CAS  Google Scholar 

  • Sekine, K.T, Nandi, A., Ishihara, T., Hase, S., Ikegami, M., Shah, J., Takahashi, H. 2004. Enhanced resistance to Cucumber mosaic virus in the Arabidopsis thaliana ssi2 mutant is mediated via an SA-independent mechanism. Mol Plant-Microbe Interact. 17: 623–632.

    Article  PubMed  CAS  Google Scholar 

  • Simon, A.E., Li, X.H., Lew, J.E., Srange, R., Zhang, C., Polacco, M. and Carpenter, C.D. 1992. Susceptibility and resistance of Arabidopsis thaliana to turnip crinkle virus. Mol. Plant-Microbe Interact. 5, 496–503.

    Google Scholar 

  • Singh, D.P., Moore, C.A., Gilliland, A. and Carr, J.P. 2004. Activation of multiple antiviral defence mechanisms by salicylic acid. Mol. Plant Pathol. 5: 57–63.

    Article  CAS  Google Scholar 

  • Takahashi, H., Goto, N. and Ehara, Y. 1994. Hypersensitive response in cucumber mosaic virus-inoculated Arabidopsis thaliana. Plant J. 6: 369–377.

    Article  Google Scholar 

  • Takahashi, H., Suzuki, M., Natsuaki, K., Shigyo, T., Hino, K., Teaoka, T., Hosokawa, D. and Ehara, Y. 2001. Mapping the virus and host genes involved in resistance response in Cucumber mosaic virus-infected Arabidopsis thaliana. Plant Cell Physiol. 42: 340–347.

    Article  PubMed  CAS  Google Scholar 

  • Takahashi, H., Miller, J., Nozaki, Y., Takeda, M., Shah, J., Hase, S., Ikegami, M., Ehara, Y. and Dinesh-Kumar, S.P. 2002. RCY1, an 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.

    Article  PubMed  CAS  Google Scholar 

  • Takahashi, H., Kanayama, Y., Zheng, M. S., Kusano, T., Hase, S., Ikegami. and Shah J. 2004. Antagonistic interactions between the SA and JA signaling pathways in Arabidopsis modulate expression of defense genes and gene-for-gene resistance to cucumber mosaic virus. Plant Cell Physiol. 45: 803–809.

    Article  PubMed  CAS  Google Scholar 

  • Takahashi, A., Casais, C., Ichimura, K. and Shirasu, K. 2003. HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc. Natl. Acad. Sci. USA. 100: 11777–11782.

    Article  PubMed  CAS  Google Scholar 

  • Tör, M., Gordon, P., Cuzick, A., Eulgem, T., Sinapidou, E., Mert-Turk, F., Can, C., Dangl, J.L. and Holub, E.B. 2002. Arabidopsis SGT1b is required for defense signaling conferred by several downy mildew resistance genes. Plant Cell 14: 993–1003.

    Article  PubMed  Google Scholar 

  • Tsujimoto, Y., Numaga, T., Ohshima, K., Yano, M-A., Ohsawa, R., Goto, D. B. Naito, S. and Ishikawa, M. 2003. Arabidopsis Tobamovirus multiplication (TOM) 2 locus encodes a transmembrane protein that interacts with TOM1. EMBO J. 22: 335–343.

    Article  PubMed  CAS  Google Scholar 

  • Whitham, S.A., Anderberg, R.J., Chisholm, S.T. Carrington, J.C. 2000. Arabidopsis RTM2 gene is necessary for specific restriction of Tobacco etch virus and encodes an unusual small heat shock-like protein. Plant Cell 12: 569–582.

    Article  PubMed  CAS  Google Scholar 

  • Whitham, S.A., Quan, S., Chang, H.-S., Cooper, B., Estees, B., Zhu, T., Wang, X. and Hou, Y.-M. 2003. Diverse RNA viruses elicit the expression of common set of genes in susceptible Arabidopsis thaliana plants. Plant J. 33: 271–283.

    Article  PubMed  CAS  Google Scholar 

  • Wildermuth, M.C., Dewdney, J., Wu, G. and Ausubel, F.M. 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defense. Nature, 414: 562–565.

    Article  PubMed  CAS  Google Scholar 

  • Wong, C.E., Carson, R.A.J. and Carr J.P. 2002. Chemically induced virus resistance in Arabidopsis thaliana is independent of pathogenesis-related protein expression and the NPR1 gene. Mol. Plant-Microbe Interact. 15: 75–81.

    Article  PubMed  CAS  Google Scholar 

  • 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. USA. 98: 6516–6521.

    Article  PubMed  CAS  Google Scholar 

  • Yamanaka, T., Ohta, T., Takahashi, M., Meshi, T., Schmidt, R., Dean, C., Naito, S., Ishikawa, M. 2000. TOM1, an Arabidopsis gene required for efficient multiplication of a tobamovirus, encodes a putative transmembrane protein. Proc. Natl. Acad. Sci. USA. 97: 10107–10112.

    Article  PubMed  CAS  Google Scholar 

  • Yoshii, M., Yoshioka, N., Ishikawa, M., Naito, S. 1998. Isolation of an Arabidopsis thaliana mutant in which the multiplication of both Cucumber mosaic virus and Turnip crinkle virus is affected. J. Virol. 72: 8731–8737.

    PubMed  CAS  Google Scholar 

  • Yoshii, M., Nishikiori, M., Tomita, K., Yoshioka, N., Kozuka, R., Naito, S. and Ishikawa, M. 2004. The Arabidopsis cucumovirus multiplication 1 and 2 loci encode translation initiation factors 4E and 4G. J. Virol. 78: 6102–6111.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 resistant Arabidopsis. Mol. Plant-Microbe Interact. 13: 1015–1018.

    Article  PubMed  CAS  Google Scholar 

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  1. Department of Plant Pathology, University of Kentucky, Lexington, KY, 40546

    Pradeep Kachroo

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  1. Agricultural Research Organisation, Bet Dagan, Israel

    Gad Loebenstein

  2. University of Cambridge, UK

    John Peter Carr

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Kachroo, P. (2006). Host Gene-mediated Virus Resistance Mechanisms and Signaling in Arabidopsis. In: Loebenstein, G., Carr, J.P. (eds) Natural Resistance Mechanisms of Plants to Viruses. Springer, Dordrecht. https://doi.org/10.1007/1-4020-3780-5_7

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