Journal of General Plant Pathology

, Volume 80, Issue 4, pp 327–336 | Cite as

Breakdown of plant virus resistance: can we predict and extend the durability of virus resistance?

  • Kappei Kobayashi
  • Ken-Taro Sekine
  • Masamichi Nishiguchi
REVIEW FOR THE 100TH ANNIVERSARY

Abstract

Cultivars with introgressed natural resistance genes have been widely used for plant disease control, especially in the control of virus diseases, for which no effective chemical control agent is available. However, we often encounter virus mutants that break down or overcome the resistance. In this review, recent studies will be discussed with respect to breakdown of plant virus resistance.

Keywords

Plant virus Resistance gene Breakdown Durability Prediction Genetic background 

Notes

Acknowledgments

This work was supported in part by JSPS KAKENHI Grant Number 24658044 (KK); JSPS KAKENHI Grant Number 24780043 and Yamazaki Spice Promotion Foundation (KTS); and the Program for Promotion of Basic and Applied Researches in Bio-oriented Industry, and JSPS KAKENHI Grant Number 24580065 (MN).

References

  1. Abdul-Razzak A, Guiraud T, Peypelut M, Walter J, Houvenaghel MC, Candresse T, Le Gall O, German-Retana S (2009) Involvement of the cylindrical inclusion (CI) protein in the overcoming of an eIF4E-mediated resistance against Lettuce mosaic potyvirus. Mol Plant Pathol 10:109–113PubMedGoogle Scholar
  2. Ali ME, Kobayashi K, Yamaoka N, Ishikawa M, Nishiguchi M (2013) Graft transmission of RNA silencing to non-transgenic scions for conferring cvirus resistance in tobacco. PLoS ONE 8:e63257Google Scholar
  3. Antignus Y, Lachman O, Pearlsman M, Maslenin L, Rosner A (2008) A new pathotype of Pepper mild mottle virus (PMMoV) overcomes the L 4 resistance genotype of pepper cultivars. Plant Dis 92:1033–1037Google Scholar
  4. 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 579:4479–4484PubMedGoogle Scholar
  5. Ashby JA, Stevenson CEM, Jarvis GE, Lawson DM, Maule AJ (2011) Structure-based mutational analysis of eIF4E in relation to sbm1 resistance to pea seed-borne mosaic virus in pea. PLoS ONE 6:e15873PubMedCentralPubMedGoogle Scholar
  6. Atsumi G, Kagaya U, Kitazawa H, Nakahara KS, Uyeda I (2009) Activation of the salicylic acid signaling pathway enhances Clover yellow vein virus virulence in susceptible pea cultivars. Mol Plant Microbe Interact 22:166–175PubMedGoogle Scholar
  7. Bendahmane A, Kanyuka K, Baulcombe DC (1999) The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell 11:781–792PubMedCentralPubMedGoogle Scholar
  8. Bendahmane A, Querci M, Kanyuka K, Baulcombe DC (2000) Agrobacterium transient expression system as a tool for the isolation of disease resistance genes: application to the Rx2 locus in potato. Plant J 21:73–81PubMedGoogle Scholar
  9. Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742–744PubMedCentralPubMedGoogle Scholar
  10. Boukema IW (1980) Allelism of genes controlling resistance to TMV in Capsicum L. Euphytica 29:433–439Google Scholar
  11. Boukema IW (1982) Resistance to a new strain of TMV in Capsicum chacoense Hunz. Capsicum Newsl 1:49–51Google Scholar
  12. Boukema IW (1984) Resistance to TMV in Capsicum chacoense Hunz. is governed by allele of the L-locus. Capsicum Newsl 3:47–48Google Scholar
  13. Brun H, Chèvre AM, Fitt BDL, Powers S, Besnard AL, Ermel M, Huteau V, Marquer B, Eber F, Renard M, Andrivon D (2010) Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytol 185:285–299PubMedGoogle Scholar
  14. Calder VL, Palukaitis P (1992) Nucleotide sequence analysis of the movement genes of resistance breaking strains of tomato mosaic virus. J Gen Virol 73:165–168PubMedGoogle Scholar
  15. Caplan JL, Mamillapalli P, Burch-Smith TM, Czymmek K, Dinesh-Kumar SP (2008) Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector. Cell 132:449–462PubMedCentralPubMedGoogle Scholar
  16. Charron C, Nicolaï M, Gallois JL, Robaglia C, Moury B, Palloix A, Caranta C (2008) Natural variation and functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg. Plant J 54:56–68PubMedGoogle Scholar
  17. 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 97:489–494PubMedCentralPubMedGoogle Scholar
  18. 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 127:1667–1675PubMedCentralPubMedGoogle Scholar
  19. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host–microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814PubMedGoogle Scholar
  20. Collier SM, Moffett P (2009) NB-LRRs work a “bait and switch” on pathogens. Trends Plant Sci 14:521–529PubMedGoogle Scholar
  21. 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 12:663–676PubMedCentralPubMedGoogle Scholar
  22. Cosson P, Schurdi-Levraud V, Le QH, Sicard O, Caballero M, Roux F, Le Gall O, Candresse T, Revers F (2012) The RTM resistance to potyviruses in Arabidopsis thaliana: natural variation of the RTM genes and evidence for the implication of additional genes. PLoS ONE 7:e39169PubMedCentralPubMedGoogle Scholar
  23. Csorba T, Pantaleo V, Burgyán J (2009) RNA silencing: an antiviral mechanism. Adv Virus Res 75:35–71PubMedGoogle Scholar
  24. Culver JN (2002) Tobacco mosaic virus assembly and disassembly: determinants in pathogenicity and resistance. Annu Rev Phytopathol 40:287–308PubMedGoogle Scholar
  25. Culver JN, Dawson WO (1989) Tobacco mosaic virus coat protein: an elicitor of the hypersensitive reaction but not required for the development of mosaic symptoms in Nicotiana sylvestris. Virology 173:755–758PubMedGoogle Scholar
  26. Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833PubMedGoogle Scholar
  27. Decroocq V, Salvador B, Sicard O, Glasa M, Cosson P, Svanella-Dumas L, Revers F, García JA, Candresse T (2009) The determinant of potyvirus ability to overcome the RTM resistance of Arabidopsis thaliana maps to the N-terminal region of the coat protein. Mol Plant Microbe Interact 22:1302–1311PubMedGoogle Scholar
  28. Dinesh-Kumar SP, Tham WH, Baker BJ (2000) Structure-function analysis of the tobacco mosaic virus resistance gene N. Proc Natl Acad Sci USA 97:14789–14794PubMedCentralPubMedGoogle Scholar
  29. Duprat A, Caranta C, Revers F, Menand B, Browning KS, Robaglia C (2002) The Arabidopsis eukaryotic initiation factor (iso)4E is dispensable for plant growth but required for susceptibility to potyviruses. Plant J 32:927–934PubMedGoogle Scholar
  30. Erickson FL, Holzberg S, Calderon-Urrea A, Handley V, Axtell M, Corr C, Baker B (1999) The helicase domain of the TMV replicase proteins induces the N-mediated defence response in tobacco. Plant J 18:67–75PubMedGoogle Scholar
  31. Fabre F, Bruchou C, Palloix A, Moury B (2009) Key determinants of resistance durability to plant viruses: insights from a model linking within- and between-host dynamics. Virus Res 141:140–149PubMedGoogle Scholar
  32. Farnham G, Baulcombe DC (2006) Artificial evolution extends the spectrum of viruses that are targeted by a disease-resistance gene from potato. Proc Natl Acad Sci USA 103:18828–18833PubMedCentralPubMedGoogle Scholar
  33. Felix G, Regenass M, Boller T (1993) Specific perception of subnanomolar concentrations of chitin fragments by tomato cells: induction of extracellular alkalinization, changes in protein phophorylation, and establishment of a refractory state. Plant J 4:307–316Google Scholar
  34. Fournet S, Kerlan MC, Renault L, Dantec JP, Rouaux C, Montarry J (2013) Selection of nematodes by resistant plants has implications for local adaptation and cross-virulence. Plant Pathol 62:184–193Google Scholar
  35. Furusawa I, Okuno T (1978) Infection with BMV of mesophyll protoplasts isolated from five plant species. J Gen Virol 40:489–491Google Scholar
  36. Gao Z, Johansen E, Eyers S, Thomas CL, Noel Ellis TH, Maule AJ (2004) The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell-to-cell trafficking. Plant J 40:376–385Google Scholar
  37. García-Arenal F, McDonald BA (2003) An analysis of the durability of resistance to plant viruses. Phytopathology 93:941–952PubMedGoogle Scholar
  38. García-Luque I, Ferrero ML, Rodríquez JM, Alonso E, de la Cruz A, Sanz AI, Vaquero C, Serra MT, Díaz-Ruíz JR (1993) The nucleotide sequence of the coat protein genes and 3′ non-coding regions of two resistance-breaking tobamoviruses in pepper shows that they are different viruses. Arch Virol 131:75–88PubMedGoogle Scholar
  39. Genda Y, Kanda A, Hamada H, Sato K, Ohnishi J, Tsuda S (2007) Two amino acid substitutions in the coat protein of Pepper mild mottle virus are responsible for overcoming the L 4 gene-mediated resistance in Capsicum spp. Phytopathology 97:787–793PubMedGoogle Scholar
  40. German-Retana S, Walter J, Doublet B, Roudet-Tavert G, Nicaise V, Lecampion C, Houvenaghel MC, Robaglia C, Michon T, Le Gall O (2008) Mutational analysis of plant cap-binding protein eIF4E reveals key amino acids involved in biochemical functions and potyvirus infection. J Virol 82:7601–7612PubMedCentralPubMedGoogle Scholar
  41. Gilardi P, García-Luque I, Serra MT (2004) The coat protein of tobamovirus acts as elicitor of both L 2 and L 4 gene-mediated resistance in Capsicum. J Gen Virol 85:2077–2085PubMedGoogle Scholar
  42. Göhre V, Robatzek S (2008) Breaking the barriers: microbial effector molecules subvert plant immunity. Annu Rev Phytopathol 46:189–215PubMedGoogle Scholar
  43. Gonsalves D (1998) Control of Papaya ringspot virus in papaya: a case study. Annu Rev Phytopathol 36:415–437PubMedGoogle Scholar
  44. Grzela R, Szolajska E, Ebel C, Madern D, Favier A, Wojtal I, Zagorski W, Chroboczek J (2008) Virulence factor of potato virus Y, genome-attached terminal protein VPg, is a highly disordered protein. J Biol Chem 283:213–221PubMedGoogle Scholar
  45. Hagiwara Y, Komoda K, Yamanaka T, Tamai A, Meshi T, Funada R, Tsuchiya T, Naito S, Ishikawa M (2003) Subcellular localization of host and viral proteins associated with tobamovirus RNA replication. EMBO J 22:344–353PubMedCentralPubMedGoogle Scholar
  46. Hamada H, Takeuchi S, Kiba A, Tsuda S, Hikichi Y, Okuno T (2002) Amino acid changes in Pepper mild mottle virus coat protein that affect L 3 gene-mediated resistance in pepper. J Gen Plant Pathol 68:155–162Google Scholar
  47. Hamada H, Takeuchi S, Morita Y, Sawada H, Kiba A, Hikichi Y (2003) Characterization of Paprika mild mottle virus first isolated in Japan. J Gen Plant Pathol 69:199–204Google Scholar
  48. Hamada H, Tomita R, Iwadate Y, Kobayashi K, Munemura I, Takeuchi S, Hikichi Y, Suzuki K (2007) Cooperative effect of two amino acid mutations in the coat protein of Pepper mild mottle virus overcomes L 3-mediated resistance in Capsicum plants. Virus Genes 34:205–214PubMedGoogle Scholar
  49. Hogenhout SA, Van der Hoorn RA, Terauchi R, Kamoun S (2009) Emerging concepts in effector biology of plant-associated organisms. Mol Plant Microbe Interact 22:115–122PubMedGoogle Scholar
  50. Hussain MM, Melcher U, Whittle T, Williams A, Brannan CM, Mitchell ED Jr (1987) Replication of cauliflower mosaic virus DNA in leaves and suspension culture protoplasts of cotton. Plant Physiol 83:633–639PubMedCentralPubMedGoogle Scholar
  51. Ishibashi K, Ishikawa M (2013) The resistance protein tm-1 inhibits formation of a tomato mosaic virus replication protein-host membrane protein complex. J Virol 87:7933–7939PubMedCentralPubMedGoogle Scholar
  52. Ishibashi K, Masuda K, Naito S, Meshi T, Ishikawa M (2007) An inhibitor of viral RNA replication is encoded by a plant resistance gene. Proc Natl Acad Sci USA 104:13833–13838PubMedCentralPubMedGoogle Scholar
  53. Ishibashi K, Naito S, Meshi T, Ishikawa M (2009) An inhibitory interaction between viral and cellular proteins underlies the resistance of tomato to nonadapted tobamoviruses. Proc Natl Acad Sci USA 106:8778–8783PubMedCentralPubMedGoogle Scholar
  54. Ishibashi K, Mawatari N, Miyashita S, Kishino H, Meshi T, Ishikawa M (2012) Coevolution and hierarchical interactions of Tomato mosaic virus and the resistance gene Tm-1. PLoS Pathog 8:e1002975PubMedCentralPubMedGoogle Scholar
  55. Ishikawa M, Naito S, Ohno T (1993) Effects of the tom1 mutation of Arabidopsis thaliana on the multiplication of tobacco mosaic virus RNA in protoplasts. J Virol 67:5328–5338PubMedCentralPubMedGoogle Scholar
  56. Janzac B, Fabre F, Palloix A, Moury B (2009) Constraints on evolution of virus avirulence factors predict the durability of corresponding plant resistances. Mol Plant Pathol 10:599–610PubMedGoogle Scholar
  57. Jebasingh T, Jose M, Kasin Yadunandam A, Bachiyarani S, Srividhya KV, Krishnaswamy S, Usha R (2011) Molecular modeling and conformational analysis of native and refolded viral genome-linked protein of Cardamom mosaic virus. Indian J Biochem Biophys 48:336–340PubMedGoogle Scholar
  58. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329PubMedGoogle Scholar
  59. Kang BC, Yeam I, Frantz JD, Murphy JF, Jahn MM (2005) The pvr1 locus in Capsicum encodes a translation initiation factor eIF4E that interacts with Tobacco etch virus VPg. Plant J 42:392–405PubMedGoogle Scholar
  60. Komatsu K, Hashimoto M, Ozeki J, Yamaji Y, Maejima K, Senshu H, Himeno M, Okano Y, Kagiwada S, Namba S (2010) Viral-induced systemic necrosis in plants involves both programmed cell death and the inhibition of viral multiplication, which are regulated by independent pathways. Mol Plant Microbe Interact 23:283–293PubMedGoogle Scholar
  61. Lanfermeijer FC, Dijkhuis J, Sturre MJG, de Haan P, Hille J (2003) Cloning and characterization of the durable tomato mosaic virus resistance gene Tm-2 2 from Lycopersicon esculentum. Plant Mol Biol 52:1037–1049PubMedGoogle Scholar
  62. Lellis AD, Kasschau KD, Whitham SA, Carrington JC (2002) Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during potyvirus infection. Curr Biol 12:1046–1051PubMedGoogle Scholar
  63. Léonard S, Plante D, Wittmann S, Daigneault N, Fortin MG, Laliberté JF (2000) Complex formation between potyvirus VPg and translation eukaryotic initiation factor 4E correlates with virus infectivity. J Virol 74:7730–7737PubMedCentralPubMedGoogle Scholar
  64. Léonard S, Viel C, Beauchemin C, Daigneault N, Fortin MG, Laliberté JF (2004) Interaction of VPg-Pro of Turnip mosaic virus with the translation initiation factor 4E and the poly(A)-binding protein in planta. J Gen Virol 85:1055–1063PubMedGoogle Scholar
  65. 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 14:177–186PubMedGoogle Scholar
  66. Malyshenko SI, Kondakova OA, Taliansky ME, Atabekov JG (1989) Plant virus transport function: complementation by helper viruses is non-specific. J Gen Virol 70:2751–2757Google Scholar
  67. Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK (1997) Cocrystal structure of the messenger RNA 5′ cap-binding protein (eIF4E) bound to 7-methyl-GDP. Cell 89:951–961PubMedGoogle Scholar
  68. McDonald B (2010) How can we achieve durable disease resistance in agricultural ecosystems? New Phytol 185:3–5PubMedGoogle Scholar
  69. Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980PubMedGoogle Scholar
  70. Meshi T, Watanabe Y, Saito T, Sugimoto A, Maeda T, Okada Y (1987) Function of the 30 kD protein of tobacco mosaic virus: involvement in cell-to-cell movement and dispensability for replication. EMBO J 6:2557–2563PubMedCentralPubMedGoogle Scholar
  71. Meshi T, Motoyoshi F, Maeda T, Yoshiwoka S, Watanabe H, Okada Y (1989) Mutations in the tobacco mosaic virus 30-kD protein gene overcome Tm-2 resistance in tomato. Plant Cell 1:515–522PubMedCentralPubMedGoogle Scholar
  72. Moffett P (2009) Mechanisms of recognition in dominant R gene mediated resistance. Adv Virus Res 75:1–33PubMedGoogle Scholar
  73. Nakahara KS, Shimada R, Choi SH, Yamamoto H, Shao J, Uyeda I (2010) Involvement of the P1 cistron in overcoming eIF4E-mediated recessive resistance against Clover yellow vein virus in pea. Mol Plant Microbe Interact 23:1460–1469PubMedGoogle Scholar
  74. Nicaise V, German-Retana S, Sanjuán R, Dubrana MP, Mazier M, Maisonneuve B, Candresse T, Caranta C, LeGall O (2003) The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the Potyvirus Lettuce mosaic virus. Plant Physiol 132:1272–1282PubMedCentralPubMedGoogle Scholar
  75. Nieto C, Morales M, Orjeda G, Clepet C, Monfort A, Sturbois B, Puigdomènech P, Pitrat M, Caboche M, Dogimont C, Garcia-Mas J, Aranda MA, Bendahmane A (2006) An eIF4E allele confers resistance to an uncapped and non-polyadenylated RNA virus in melon. Plant J 48:452–462PubMedGoogle Scholar
  76. Nieto C, Rodríguez-Moreno L, Rodríguez-Hernández AM, Aranda MA, Truniger V (2011) Nicotiana benthamiana resistance to non-adapted Melon necrotic spot virus results from an incompatible interaction between virus RNA and translation initiation factor 4E. Plant J 66:492–501PubMedGoogle Scholar
  77. Nishiguchi M, Kobayashi K (2011) Attenuated plant viruses: preventing virus diseases and understanding the molecular mechanism. J Gen Plant Pathol 77:221–229Google Scholar
  78. Nishiguchi M, Motoyoshi F, Oshima N (1978) Behaviour of a temperature sensitive strain of Tobacco mosaic virus in tomato leaves and protoplasts. J Gen Virol 39:53–61Google Scholar
  79. Nishiguchi M, Motoyoshi F, Oshima N (1980) Further investigation of a temperature-sensitive strain of Tobacco mosaic virus: its behaviour in tomato leaf epidermis. J Gen Virol 46:497–500Google Scholar
  80. Palloix A, Ayme V, Moury B (2009) Durability of plant major resistance genes to pathogens depends on the genetic background, experimental evidence and consequences for breeding strategies. New Phytol 183:190–199PubMedGoogle Scholar
  81. Plochocka D, Welnicki M, Zielenkiewicz P, Ostoja-Zagórski W (1996) Three-dimensional model of the potyviral genome-linked protein. Proc Natl Acad Sci USA 93:12150–12154PubMedCentralPubMedGoogle Scholar
  82. Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ (2009) Shades of gray: the world of quantitative disease resistance. Trends Plant Sci 14:21–29PubMedGoogle Scholar
  83. Quenouille J, Montarry J, Palloix A, Moury B (2013) Farther, slower, stronger: how the plant genetic background protects a major resistance gene from breakdown. Mol Plant Pathol 14:109–118PubMedGoogle Scholar
  84. Rantalainen KI, Eskelin K, Tompa P, Mäkinen K (2011) Structural flexibility allows the functional diversity of potyvirus genome-linked protein VPg. J Virol 85:2449–2457PubMedCentralPubMedGoogle Scholar
  85. Richael C, Gilchrist D (1999) The hypersensitive response: a case of hold or fold? Physiol Mol Plant Pathol 55:5–12Google Scholar
  86. Robaglia C, Caranta C (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11:40–45PubMedGoogle Scholar
  87. Roudet-Tavert G, Michon T, Walter J, Delaunay T, Redondo E, Le Gall O (2007) Central domain of a potyvirus VPg is involved in the interaction with the host translation initiation factor eIF4E and the viral protein HcPro. J Gen Virol 88:1029–1033PubMedGoogle Scholar
  88. Ruffel S, Dussault MH, Palloix A, Moury B, Bendahmane A, Robaglia C, Caranta C (2002) A natural recessive resistance gene against potato virus Y in pepper corresponds to the eukaryotic initiation factor 4E (eIF4E). Plant J 32:1067–1075PubMedGoogle Scholar
  89. Ruffel S, Gallois JL, Lesage ML, Caranta C (2005) The recessive potyvirus resistance gene pot-1 is the tomato orthologue of the pepper pvr2-eIF4E gene. Mol Genet Genomics 274:346–353PubMedGoogle Scholar
  90. Sacco MA, Mansoor S, Moffett P (2007) A RanGAP protein physically interacts with the NB-LRR protein Rx, and is required for Rx-mediated viral resistance. Plant J 52:82–93PubMedGoogle Scholar
  91. Saito T, Meshi T, Takamatsu N, Okada Y (1987) Coat protein gene sequence of tobacco mosaic virus encodes a host response determinant. Proc Natl Acad Sci USA 84:6074–6077PubMedCentralPubMedGoogle Scholar
  92. Saito T, Yamanaka K, Watanabe Y, Takamatsu N, Meshi T, Okada Y (1989) Mutational analysis of the coat protein gene of tobacco mosaic virus in relation to hypersensitive response in tobacco plants with the N’ gene. Virology 173:11–20PubMedGoogle Scholar
  93. Sakamoto M, Tomita R, Hamada H, Iwadate Y, Munemura I, Kobayashi K (2008) A primer-introduced restriction analysis-PCR-based method to analyse Pepper mild mottle virus populations in plants and field soil with respect to virus mutations that break L 3 gene-mediated resistance of Capsicum plants. Plant Pathol 57:825–833Google Scholar
  94. Sawada H, Takeuchi S, Hamada H, Kiba A, Matsumoto M, Hikichi Y (2004) A new tobamovirus-resistance gene, L 1a, of sweet pepper (Capsicum annum L.). J Jpn Soc Hortic Sci 73:552–557Google Scholar
  95. Schaad MC, Anderberg RJ, Carrington JC (2000) Strain-specific interaction of the tobacco etch virus NIa protein with the translation initiation factor eIF4E in the yeast two-hybrid system. Virology 273:300–306PubMedGoogle Scholar
  96. Sekine KT, Ishihara T, Hase S, Kusano T, Shah J, Takahashi H (2006) Single amino acid alterations in Arabidopsis thaliana RCY1 compromise resistance to Cucumber mosaic virus, but differentially suppress hypersensitive response-like cell death. Plant Mol Biol 62:669–682PubMedGoogle Scholar
  97. Sekine KT, Kawakami S, Hase S, Kubota M, Ichinose Y, Shah J, Kang HG, Klessig DF, Takahashi H (2008) High level expression of a virus resistance gene, RCY1, confers extreme resistance to Cucumber mosaic virus in Arabidopsis thaliana. Mol Plant Microbe Interact 21:1398–1407PubMedGoogle Scholar
  98. Sekine KT, Tomita R, Takeuchi S, Atsumi G, Saitoh H, Mizumoto H, Kiba A, Yamaoka N, Nishiguchi M, Hikichi Y, Kobayashi K (2012) Functional differentiation in the leucine-rich repeat domains of closely related plant virus-resistance proteins that recognize common avr proteins. Mol Plant Microbe Interact 25:1219–1229PubMedGoogle Scholar
  99. Sugawara K, Shiraishi T, Yoshida T, Fujita N, Netsu O, Yamaji Y, Namba S (2013) A replicase of Potato virus X acts as the resistance-breaking determinant for JAX1-mediated resistance. Mol Plant Microbe Interact 26:1106–1112PubMedGoogle Scholar
  100. Tameling WI, Baulcombe DC (2007) Physical association of the NB-LRR resistance protein Rx with a Ran GTPase-activating protein is required for extreme resistance to Potato virus X. Plant Cell 19:1682–1694PubMedCentralPubMedGoogle Scholar
  101. Tavert-Roudet G, Abdul-Razzak A, Doublet B, Walter J, Delaunay T, German-Retana S, Michon T, Le Gall O, Candresse T (2012) The C terminus of lettuce mosaic potyvirus cylindrical inclusion helicase interacts with the viral VPg and with lettuce translation eukaryotic initiation factor 4E. J Gen Virol 93:184–193PubMedGoogle Scholar
  102. Tomita R, Sekine KT, Mizumoto H, Sakamoto M, Murai J, Kiba A, Hikichi Y, Suzuki K, Kobayashi K (2011) Genetic basis for the hierarchical interaction between Tobamovirus spp. and L resistance gene alleles from different pepper species. Mol Plant Microbe Interact 24:108–117PubMedGoogle Scholar
  103. Truniger V, Nieto C, González-Ibeas D, Aranda M (2008) Mechanism of plant eIF4E-mediated resistance against a Carmovirus (Tombusviridae): cap-independent translation of a viral RNA controlled in cis by an (a)virulence determinant. Plant J 56:716–727PubMedGoogle Scholar
  104. Tsuda S, Kirita M, Watanabe Y (1998) Characterization of a Pepper mild mottle tobamovirus strain capable of overcoming the L 3 gene-mediated resistance, distinct from the resistance-breaking Italian isolate. Mol Plant Microbe Interact 11:327–331PubMedGoogle Scholar
  105. Tsujimoto Y, Numaga T, Ohshima K, Yano MA, Ohsawa R, Goto DB, Naito S, Ishikawa M (2003) Arabidopsis TOBAMOVIRUS MULTIPLICATION (TOM) 2 locus encodes a transmembrane protein that interacts with TOM1. EMBO J 22:335–343PubMedCentralPubMedGoogle Scholar
  106. Ueda H, Yamaguchi Y, Sano H (2006) Direct interaction between the tobacco mosaic virus helicase domain and the ATP-bound resistance protein, N factor during the hypersensitive response in tobacco plants. Plant Mol Biol 61:31–45PubMedGoogle Scholar
  107. Voinnet O (2001) RNA silencing as a plant immune system against viruses. Trends Genet 17:449–459PubMedGoogle Scholar
  108. Wang Y, Bao Z, Zhu Y, Hua J (2009) Analysis of temperature modulation of plant defense against biotrophic microbes. Mol Plant Microbe Interact 22:498–506PubMedGoogle Scholar
  109. Wang MB, Masuta C, Smith NA, Shimura H (2012) RNA silencing and plant viral diseases. Mol Plant Microbe Interact 25:1275–1285PubMedGoogle Scholar
  110. Weber H, Schultze S, Pfitzner AJ (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 Virol 67:6432–6438PubMedCentralPubMedGoogle Scholar
  111. Whitham S, McCormick S, Baker B (1996) The N gene of tobacco confers resistance to tobacco mosaic virus in transgenic tomato. Proc Natl Acad Sci USA 93:8776–8781PubMedCentralPubMedGoogle Scholar
  112. Whitham SA, Yamamoto ML, Carrington JC (1999) Selectable viruses and altered susceptibility mutants in Arabidopsis thaliana. Proc Natl Acad Sci USA 96:772–777PubMedCentralPubMedGoogle Scholar
  113. 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 12:569–582PubMedCentralPubMedGoogle Scholar
  114. Wittmann S, Chatel H, Fortin MG, Laliberté JF (1997) Interaction of the viral protein genome linked of turnip mosaic potyvirus with the translational eukaryotic initiation factor (iso) 4E of Arabidopsis thaliana using the yeast two-hybrid system. Virology 234:84–92PubMedGoogle Scholar
  115. Yamaji Y, Maejima K, Komatsu K, Shiraishi T, Okano Y, Himeno M, Sugawara K, Neriya Y, Minato N, Miura C, Hashimoto M, Namba S (2012) Lectin-mediated resistance impairs plant virus infection at the cellular level. Plant Cell 24:778–793PubMedCentralPubMedGoogle Scholar
  116. 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 97:10107–10112PubMedCentralPubMedGoogle Scholar
  117. 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 76:2491–2497PubMedCentralPubMedGoogle Scholar
  118. Yeam I, Cavatorta JR, Ripoll DR, Kang BC, Jahn MM (2007) Functional dissection of naturally occurring amino acid substitutions in eIF4E that confers recessive potyvirus resistance in plants. Plant Cell 19:2913–2928PubMedCentralPubMedGoogle Scholar
  119. Yoshii M, Nishikiori M, Tomita K, Yoshioka N, Kozuka R, Naito S, Ishikawa M (2004) The Arabidopsis cucumovirus multiplication 1 and 2 loci encode translation initiation factors 4E and 4G. J Virol 78:6102–6111PubMedCentralPubMedGoogle Scholar

Copyright information

© The Phytopathological Society of Japan and Springer Japan 2014

Authors and Affiliations

  • Kappei Kobayashi
    • 1
  • Ken-Taro Sekine
    • 2
  • Masamichi Nishiguchi
    • 1
  1. 1.Laboratory of Plant Molecular Biology and Virology, Faculty of AgricultureEhime UniversityMatsuyamaJapan
  2. 2.Iwate Biotechnology Research CenterKitakamiJapan

Personalised recommendations