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An Emerging Model System: Arabidopsis as a Viral Host Plant

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Viral Transport in Plants

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 7))

Abstract

The model plant Arabidopsis thaliana has been established as a host for representatives of many of the major groups of plant viruses. These viruses use a variety of strategies to replicate and traffic their genomes within compatible host plants. The development of Arabidopsis as a host for these diverse viruses provides opportunities to apply genetic and reverse genetic approaches to the complex interactions that are not feasible or practical in many of their agronomically important hosts. In this chapter, we summarize the amazing array of viruses that have been shown to infect one or more Arabidopsis ecotypes, describe natural variation in the ability of these ecotypes to support systemic infections, and discuss host genes that have been identified through a variety of approaches that are involved in movement or limit virus spread in Arabidopsis.

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References

  • Arce-Johnson P, Medina C, Padgett HS, Huanca W, Espinoza C (2003) Analysis of local and systemic spread of the crucifer-infecting TMV-Cg virus in tobacco and several Arabidopsis thaliana ecotypes. Funct Plant Biol 30:401–408

    Article  Google Scholar 

  • Asano M, Satoh R, Mochizuki A, Tsuda S, Yamanaka T, Nishiguchi M, Hirai K, Meshi T, Naito S, Ishikawa M (2005) Tobamovirus-resistant tobacco generated by RNA interference directed against host genes. FEBS Lett 579:4479–4484

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Callaway AS, Huang Z, Howell SH (2000) Host suppressors in Arabidopsis thaliana of mutations in the movement protein gene of Cauliflower mosaic virus. Mol Plant Microbe Interact 13:512–519

    Article  PubMed  CAS  Google Scholar 

  • Carvalho MF, Lazarowitz SG (2004) Interaction of the movement protein NSP and the Arabidopsis acetyltransferase AtNSI is necessary for Cabbage leaf curl geminivirus infection and pathogenicity. J Virol 78:11161–11171

    Article  PubMed  CAS  Google Scholar 

  • Carvalho MF, Turgeon R, Lazarowitz SG (2006) The geminivirus nuclear shuttle protein NSP inhibits the activity of AtNSI, a vascular-expressed Arabidopsis acetyltransferase regulated with the sink-to-source transition. Plant Physiol 140:1317–1330

    Article  PubMed  CAS  Google Scholar 

  • Chandra-Shekara AC, Gupte M, Navarre D, Raina S, Raina R, Klessig D, Kachroo P (2006) Light-dependent hypersensitive response and resistance signaling against Turnip crinkle virus in Arabidopsis. Plant J 45:320–334

    Article  PubMed  CAS  Google Scholar 

  • Chandra-Shekara AC, Navarre D, Kachroo A, Kang HG, Klessig D, Kachroo P (2004) Signaling requirements and role of salicylic acid in HRT- and rrt-mediated resistance to Turnip crinkle virus in Arabidopsis. Plant J 40:647–659

    Article  PubMed  CAS  Google Scholar 

  • Chisholm ST, Mahajan SK, Whitham SA, Yamamoto ML, Carrington JC (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 

  • Chisholm ST, Parra MA, Anderberg RJ, Carrington JC (2001) Arabidopsis RTM1 and RTM2 genes function in phloem to restrict long-distance movement of Tobacco etch virus. Plant Physiol 127:1667–1675

    Article  PubMed  CAS  Google Scholar 

  • Choi CW, Qu F, Ren T, Ye X, Morris TJ (2004) 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

    Article  PubMed  CAS  Google Scholar 

  • Cooley MB, Pathirana S, Wu HJ, Kachroo P, Klessig DF (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 

  • Cooper B, Eckert D, Andon NL, Yates JR, Haynes PA (2003) Investigative proteomics: identification of an unknown plant virus from infected plants using mass spectrometry. J Am Soc Mass Spectrom 14:736–741

    Article  PubMed  CAS  Google Scholar 

  • Dardick CD, Golem S, Culver JN (2000) Susceptibility and symptom development in Arabidopsis 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 

  • de Assis Filho FM, Sherwood JL (2000) Evaluation of seed transmission of Turnip yellow mosaic virus and Tobacco mosaic virus in Arabidopsis thaliana. Phytopathology 90:1233–1238

    Article  PubMed  Google Scholar 

  • Decroocq V, Sicard O, Alamillo JM, Lansac M, Eyquard JP, Garcia JA, Candresse T, Le Gall O, Revers F (2006) Multiple resistance traits control Plum pox virus infection in Arabidopsis thaliana. Mol Plant Microbe Interact 19:541–549

    Article  PubMed  CAS  Google Scholar 

  • Dempsey DA, Pathirana MS, Wobbe KK, Klessig DF (1997) Identification of an Arabidopsis locus required for resistance to Turnip crinkle virus. Plant J 11:301–311

    Article  PubMed  CAS  Google Scholar 

  • Dempsey DA, Wobbe KK, Klessig D (1993) Resistance and susceptible responses of Arabidopsis thaliana to Turnip crinkle virus. Phytopathology 83:1021–1029

    Article  CAS  Google Scholar 

  • Dorokhov Yu L, Ivanov PA, Novikov VK, Agranovsky AA, Morozov S, Efimov VA, Casper R, Atabekov JG (1994) Complete nucleotide sequence and genome organization of a tobamovirus infecting cruciferae plants. FEBS Lett 350:5–8

    Article  PubMed  Google Scholar 

  • Dunoyer P, Thomas C, Harrison S, Revers F, Maule A (2004) A cysteine-rich plant protein potentiates potyvirus movement through an interaction with the virus genome-linked protein VPg. J Virol 78:2301–2309

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Fujisaki K, Hagihara F, Azukawa Y, Kaido M, Okuno T, 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 17:967–975

    Article  PubMed  CAS  Google Scholar 

  • German TL, Adkins S, Witherell A, Richmond KE, Knaack WR, Willis DK (1995) Infection of Arabidopsis thaliana ecotype Columbia by Tomato spotted wilt virus. Weeds World 2:2–7

    CAS  Google Scholar 

  • Geshi N, Brandt A (1998) Two jasmonate-inducible myrosinase-binding proteins from Brassica napus L. seedlings with homology to jacalin. Planta 204:295–304

    Article  PubMed  CAS  Google Scholar 

  • Hill JE, Strandberg JO, Hiebert E, Lazarowitz SG (1998) Asymmetric infectivity of pseudorecombinants of Cabbage leaf curl virus and Squash leaf curl virus: implications for bipartite geminivirus evolution and movement. Virology 250:283–292

    Article  PubMed  CAS  Google Scholar 

  • Huang Z, Yeakley JM, Garcia EW, Holdridge JD, Fan JB, Whitham SA (2005) Salicylic acid-dependent expression of host genes in compatible Arabidopsis-virus interactions. Plant Physiol 137:1147–1159

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa M, Obata F, Kumagai T, Ohno T (1991) Isolation of mutants of Arabidopsis thaliana in which accumulation of Tobacco mosaic virus coat protein is reduced to low levels. Mol Gen Genet 230:33–38

    Article  PubMed  CAS  Google Scholar 

  • Jimenez I, Lopez L, Alamillo JM, Valli A, Garcia JA (2006) Identification of a Plum pox virus CI-interacting protein from chloroplast that has a negative effect in virus infection. Mol. Plant Microbe Interact 19:350–358

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kang BC, Yeam I, Jahn MM (2005) Genetics of plant virus resistance. Annu Rev Phytopathol 43:581–621

    Article  PubMed  CAS  Google Scholar 

  • Lartey R, Ghoshroy S, Ho J, Citovsky V (1997) Movement and subcellular localization of a tobamovirus in Arabidopsis. Plant J 12:537–545

    Article  PubMed  CAS  Google Scholar 

  • Lartey RT, Ghoshroy S, 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 JM, Hartman GL, Domier LL, Bent AF (1996) Identification and map location of TTR1, a single locus in Arabidopsis thalianathat confers tolerance to Tobacco ringspot nepovirus. Mol Plant Microbe Interact 9:729–735

    Article  PubMed  CAS  Google Scholar 

  • Lee JY, Taoka K, Yoo BC, Ben-Nissan G, Kim DJ, Lucas WJ (2005) Plasmodesmal-associated protein kinase in tobacco and Arabidopsis recognizes a subset of non-cell-autonomous proteins. Plant Cell 17:2817–2831

    Article  PubMed  CAS  Google Scholar 

  • Lee S, Stenger DC, Bisaro DM, Davis KR (1994) Identification of loci in Arabidopsis that confer resistance to geminivirus infection. Plant J 6:525–535

    Article  PubMed  CAS  Google Scholar 

  • Leisner SM, Howell SH (1992) Symptom variations in different Arabidopsis thaliana ecotypes produced by Cauliflower mosaic virus. Phytopathology 82:1042–1046

    Article  Google Scholar 

  • Leisner SM, Turgeon R, Howell SH (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 

  • Loudet O, Chaillou S, Camilleri C, Bouchez D, Daniel-Vedele F (2002) Bay-0 x Shahdara recombinant inbred line population: a powerful tool for the genetic dissection of complex traits in Arabidopsis. Theor Appl Genet 104:1173–1184

    Article  PubMed  CAS  Google Scholar 

  • Love AJ, Yun BW, Laval V, Loake GJ, Milner JJ (2005) Cauliflower mosaic virus, a compatible pathogen of Arabidopsis, engages three distinct defense-signaling pathways and activates rapid systemic generation of reactive oxygen species. Plant Physiol 139:935–948

    Article  PubMed  CAS  Google Scholar 

  • MacFarlane SA, Popovich AH (2000) Efficient expression of foreign proteins in roots from tobravirus vectors. Virology 267:29–35

    Article  PubMed  CAS  Google Scholar 

  • Mahajan SK, Chisholm ST, Whitham SA, Carrington JC (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 Martin A, Cabrera y Poch HL, Martinez Herrera D, Ponz F (1999) Resistances to Turnip mosaic potyvirus in Arabidopsis thaliana. Mol Plant Microbe Interact 12:1016–1021

    Article  PubMed  CAS  Google Scholar 

  • Martin Martin A, Martinez Herrera D, Cabrera y Poch HL, Ponz F (1997) Variability in the interactions between Arabidopsis thalianaecotypes and Oilseed rape mosaic tobamovirus. Aust J Plant Physiology 24:275–281

    Article  Google Scholar 

  • McGarry RC, Barron YD, Carvalho MF, Hill JE, Gold D, Cheung E, Kraus WL, Lazarowitz SG (2003) A novel Arabidopsis acetyltransferase interacts with the geminivirus movement protein NSP. Plant Cell 15:1605–1618

    Article  PubMed  CAS  Google Scholar 

  • Meyerowitz EM, Somerville CR (1994) Arabidopsis. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Nagy PD, Pogany J (2006) Yeast as a model host to dissect functions of viral and host factors in tombusvirus replication. Virology 344:211–220

    Article  PubMed  CAS  Google Scholar 

  • Nemeth M (1994) History and importance of plum pox in stone-fruit production. OEPP/EPPO Bull 24:525–536

    Google Scholar 

  • Noueiry AO, Ahlquist P (2003) Brome mosaic virus RNA replication: revealing the role of the host in RNA virus replication. Annu Rev Phytopathol 41:77–98

    Article  PubMed  CAS  Google Scholar 

  • Noueiry AO, Lucas WJ, Gilbertson RL (1994) Two proteins of a plant DNA virus coordinate nuclear and plasmodesmal transport. Cell 76:925–932

    Article  PubMed  CAS  Google Scholar 

  • Park SH, Hur J, Park J, Lee S, Lee TK, Chang M, Davi KR, Kim J, Lee S (2002) Identification of a tolerant locus on Arabidopsis thaliana to hypervirulent Beet curly top virus CFH strain. Mol Cells 13:252–258

    PubMed  CAS  Google Scholar 

  • Pascal E, Sanderfoot AA, Ward BM, Medville R, Turgeon R, Lazarowitz SG (1994) The geminivirus BR1 movement protein binds single-stranded DNA and localizes to the cell nucleus. Plant Cell 6:995–1006

    Article  PubMed  CAS  Google Scholar 

  • Pazhouhandeh M, Dieterle M, Marrocco K, Lechner E, Berry B, Brault V, Hemmer O, Kretsch T, Richards KE, Genschik P, Ziegler-Graff V (2006) F-box-like domain in the polerovirus protein P0 is required for silencing suppressor function. Proc Natl Acad Sci USA 103:1994–1999

    Article  PubMed  CAS  Google Scholar 

  • Peumans WJ, Van Damme EJM (1995) Lectins as plant defense proteins. Plant Physiol 109:347–352

    Article  PubMed  CAS  Google Scholar 

  • Ren T, Qu F, Morris TJ (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 

  • Ren T, Qu F, Morris TJ (2005) 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

    Article  PubMed  CAS  Google Scholar 

  • Revers F, Guiraud T, Houvenaghel MC, Mauduit T, Le Gall O, Candresse T (2003) Multiple resistance phenotypes to Lettuce mosaic virus among Arabidopsis thaliana accessions. Mol Plant Microbe Interact 16:608–616

    Article  PubMed  CAS  Google Scholar 

  • Sanderfoot AA, Ingham DJ, Lazarowitz SG (1996) A viral movement protein as a nuclear shuttle. The geminivirus BR1 movement protein contains domains essential for interaction with BL1 and nuclear localization. Plant Physiol 110:23–33

    Article  PubMed  CAS  Google Scholar 

  • Sasaki N, Park JW, Maule AJ, Nelson RS (2006) The cysteine-histidine-rich region of the movement protein of Cucumber mosaic virus contributes to plasmodesmal targeting, zinc binding and pathogenesis. Virology 349:396–408

    Article  PubMed  CAS  Google Scholar 

  • Sheng J, Lartey R, Ghoshroy S, Citovsky V (1998) An Arabidopsis thaliana mutant with virus-inducible phenotype. Virology 249:119–128

    Article  PubMed  CAS  Google Scholar 

  • Shirasu K, Schulze-Lefert P (2003) Complex formation, promiscuity and multi-functionality: protein interactions in disease-resistance pathways. Trends Plant Sci 8:252–258

    Article  PubMed  CAS  Google Scholar 

  • Simon AE, Li XH, Lew JE, Stange R, Zhang C, Polacco M, Carpenter CD (1992) Susceptibility and resistance of Arabidopsis thaliana to Turnip crinkle virus. Mol Plant Microbe Interact 5:496–503

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Takahashi H, Miller J, Nozaki Y, Takeda M, Shah J, Hase S, Ikegami M, Ehara Y, Dinesh-Kumar SP (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, Suzuki M, Natsuaki K, Shigyo T, Hino K, Teraoka T, Hosokawa D, Ehara Y (2001) Mapping the virus and host genes involved in the resistance response in Cucumber mosaic virus-infected Arabidopsis thaliana. Plant Cell Physiol 42:340–347

    Article  PubMed  CAS  Google Scholar 

  • Thomas CL, Maule AJ (1995a) Identification of structural domains within the Cauliflower mosaic virus movement protein by scanning deletion mutagenesis and epitope tagging. Plant Cell 7:561–572

    Article  PubMed  CAS  Google Scholar 

  • Thomas CL, Maule AJ (1995b) Identification of the Cauliflower mosaic virus movement protein RNA-binding domain. Virology 206:1145–1149

    Article  PubMed  CAS  Google Scholar 

  • Tomlinson JA (1987) Epidemiology and control of virus diseases of vegetables. Ann Appl Biol 110:661–681

    Article  Google Scholar 

  • Whitham SA, Anderberg RJ, Chisholm ST, Carrington JC (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 SA, Quan S, Chang HS, Cooper B, Estes B, Zhu T, Wang X, Hou YM (2003) Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis thaliana plants. Plant J 33:271–283

    Article  PubMed  CAS  Google Scholar 

  • Whitham SA, Wang Y (2004) Roles for host factors in plant viral pathogenicity. Curr Opin Plant Biol 7:365–371

    Article  PubMed  CAS  Google Scholar 

  • Whitham SA, Yamamoto ML, Carrington JC (1999) Selectable viruses and altered susceptibility mutants in Arabidopsis thaliana. Proc Natl Acad Sci USA 96:772–777

    Article  PubMed  CAS  Google Scholar 

  • Yamanaka T, Imai T, Satoh R, Kawashima A, Takahashi M, Tomita K, Kubota K, Meshi T, Naito S, Ishikawa M (2002) Complete inhibition of tobamovirus multiplication by simultaneous mutations in two homologous host genes. J Virol 76:2491–2497

    Article  PubMed  CAS  Google Scholar 

  • Zambryski P (2004) Cell-to-cell transport of proteins and fluorescent tracers via plasmodesmata during plant development. J Cell Biol 164:165–168

    Article  PubMed  CAS  Google Scholar 

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  1. Department of Plant Pathology, Iowa State University, 351 Bessey Hall, 50011-1020, Ames, IA, USA

    Tyrell Carr & Steven A. Whitham

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  1. Tyrell Carr
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  2. Steven A. Whitham
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Correspondence to Steven A. Whitham .

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Elisabeth Waigmann Manfred Heinlein

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Carr, T., Whitham, S.A. (2007). An Emerging Model System: Arabidopsis as a Viral Host Plant. In: Waigmann, E., Heinlein, M. (eds) Viral Transport in Plants. Plant Cell Monographs, vol 7. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_2006_104

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