1932

Abstract

During the past three decades, the economic impact of tospoviruses has increased, causing high yield losses in a variety of crops and ornamentals. Owing to the difficulty in combating thrips vectors with insecticides, the best way to limit/prevent tospovirus-induced diseases involves a management strategy that includes virus resistance. This review briefly presents current tospovirus taxonomy, diversity, molecular biology, and cytopathology as an introduction to a more extensive description of the two main resistance genes employed against tospoviruses: the gene in tomato and the in pepper. Natural and experimental resistance-breaking (RB) isolates allowed the identification of the viral avirulence protein triggering each of the two resistance gene products; epidemiology of RB isolates is discussed to reinforce the need for allelic variants and the need to search for new/alternative resistance genes. Ongoing efforts for alternative resistance strategies are described not only for (TSWV) in pepper and tomato but also for other vegetable crops heavily impacted by tospoviruses.

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2016-08-04
2024-04-17
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Literature Cited

  1. Abe H, Tomitaka Y, Shimoda T, Seo S, Sakurai T. 1.  et al. 2012. Antagonistic plant defense system regulated by phytohormones assists interactions among vector insect, thrips and a tospovirus. Plant Cell Physiol. 53:204–12 [Google Scholar]
  2. Andolfo G, Sanseverino W, Aversano R, Frusciante L, Ercolano M. 2.  2014. Genome-wide identification and analysis of candidate genes for disease resistance in tomato. Mol. Breed. 33:227–33 [Google Scholar]
  3. Aramburu J, Galipienso L, Soler S, López C. 3.  2010. Characterization of Tomato spotted wilt virus isolates that overcome the Sw-5 resistance gene in tomato and fitness assays. Phytopathol. Mediterr. 49:342–51 [Google Scholar]
  4. Aramburu J, Marti M. 4.  2003. The occurrence in north-east Spain of a variant of Tomato spotted wilt virus (TSWV) that breaks resistance in tomato (Lycopersicon esculentum) containing the Sw-5 gene. Plant Pathol. 52:407 [Google Scholar]
  5. Bag S, Schwartz HF, Cramer CS, Havey MJ, Pappu HR. 5.  2015. Iris yellow spot virus (Tospovirus: Bunyaviridae): from obscurity to research priority. Mol. Plant Pathol. 16:224–37 [Google Scholar]
  6. Ballinger MJ, Bruenn JA, Hay J, Czechowski D, Taylor DJ. 6.  2014. Discovery and evolution of bunyavirids in arctic phantom midges and ancient bunyavirid-like sequences in insect genomes. J. Virol. 88:8783–94 [Google Scholar]
  7. Belfanti E, Malatrasi M, Orsi I, Boni AG. 7.  2015. Isolated nucleotide sequence from Solanum lycopersicum for improved resistance to tomato spotted wilt virus, TSWV. US Patent No. WO2015090468-A1 [Google Scholar]
  8. Bernoux M, Ve T, Williams S, Warren C, Hatters D. 8.  et al. 2011. Structural and functional analysis of a plant resistance protein TIR domain reveals interfaces for self-association, signaling, and autoregulation. Cell Host Microbe 9:200–11 [Google Scholar]
  9. Birithia R, Subramanian S, Villinger J, Muthomi JW, Narla RD, Pappu HR. 9.  2012. First report of Tomato yellow ring virus (Tospovirus, Bunyaviridae) infecting tomato in Kenya. Plant Dis. 96:1384–85 [Google Scholar]
  10. Black LL, Hobbs HA, Gatti JM. 10.  1991. Tomato spotted wilt virus-resistance in Capsicum chinense PI 152225 and 159236. Plant Dis. 75:863 [Google Scholar]
  11. Boateng CO, Schwartz HF, Havey MJ, Otto K. 11.  2014. Evaluation of onion germplasm for resistance to Iris yellow spot (Iris yellow spot virus) and onion thrips, Thrips tabaci. Southwest. Entomol. 39:237–60 [Google Scholar]
  12. Boiteux LS. 12.  1995. Allelic relationships between genes for resistance to tomato spotted wilt tospovirus in Capsicum chinense. Theor. Appl. Genet. 90:146–49 [Google Scholar]
  13. Boiteux LS, de Ávila AC. 13.  1994. Inheritance of a resistance specific to tomato spotted wilt tospovirus in Capsicum chinense PI-159236. Euphytica 75:139–42 [Google Scholar]
  14. Boiteux L, Giordano L, de B. 14.  1992. Screening Lycopersicon germplasm for resistance to a Brazilian isolate of tomato spotted wilt virus (TSWV). TGC Rep. 42:13–14 [Google Scholar]
  15. Boiteux LS, Giordano L, de B. 15.  1993. Genetic basis of resistance against 2 tospovirus species in tomato (Lycopersicon esculentum). Euphytica 71:151–54 [Google Scholar]
  16. Brooks C, Nekrasov V, Lippman ZB, Van Eck J. 16.  2014. Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol. 166:1292–97 [Google Scholar]
  17. Brown JKM. 17.  2015. Durable resistance of crops to disease: a Darwinian perspective. Annu. Rev. Phytopathol. 53:513–39 [Google Scholar]
  18. Cañizares MC, Navas-Castillo J, Moriones E. 18.  2008. Multiple suppressors of RNA silencing encoded by both genomic RNAs of the crinivirus, Tomato chlorosis virus. Virology 379:168–74 [Google Scholar]
  19. Chen K, Gao C. 19.  2014. Targeted genome modification technologies and their applications in crop improvements. Plant Cell Rep. 33:575–83 [Google Scholar]
  20. Chen L, Hao L, Parry MAJ, Phillips AL, Hu Y-G. 20.  2014. Progress in TILLING as a tool for functional genomics and improvement of crops. J. Integr. Plant Biol. 56:425–43 [Google Scholar]
  21. Cheng C, Gao X, Feng B, Sheen J, Shan L, He P. 21.  2013. Plant immune response to pathogens differs with changing temperatures. Nat. Commun. 4:2530 [Google Scholar]
  22. Cho J, Custer D, Brommonschenkel S, Tanksley S. 22.  1996. Conventional breeding: host-plant resistance and the use of molecular markers to develop resistance to tomato spotted wilt virus in vegetables. Acta Hortic 431:367–78 [Google Scholar]
  23. Ciuffo M, Finetti-Sialer MM, Gallitelli D, Turina M. 23.  2005. First report in Italy of a resistance-breaking strain of Tomato spotted wilt virus infecting tomato cultivars carrying the Sw5 resistance gene. Plant Pathol. 54:564 [Google Scholar]
  24. Ciuffo M, Kurowski C, Vivoda E, Copes B, Masenga V. 24.  et al. 2009. A new Tospovirus sp. in cucurbit crops in Mexico. Plant Dis. 93:467–74 [Google Scholar]
  25. Cramer CS, Singh N, Kamal N, Pappu HR. 25.  2014. Screening onion plant introduction accessions for tolerance to onion thrips and Iris yellow spot. HortScience 49:1253–61 [Google Scholar]
  26. Debreczeni DE, López C, Aramburu J, Darós JA, Soler S. 26.  et al. 2015. Complete sequence of three different biotypes of tomato spotted wilt virus (wild type, tomato Sw-5 resistance-breaking and pepper Tsw resistance-breaking) from Spain. Arch. Virol. 160:2117–23 [Google Scholar]
  27. Debreczeni DE, Rubio L, Aramburu J, López C, Galipienso L. 27.  et al. 2014. Transmission of Tomato spotted wilt virus isolates able and unable to overcome tomato or pepper resistance by its vector Frankliniella occidentalis. Ann. Appl. Biol. 164:182–89 [Google Scholar]
  28. de Medeiros RB, Figueiredo J, Resende RD, de Ávila AC. 28.  2005. Expression of a viral polymerase-bound host factor turns human cell lines permissive to a plant- and insect-infecting virus. PNAS 102:1175–80 [Google Scholar]
  29. de Oliveira AS, Melo FL, Inoue-Nagata AK, Nagata T, Kitajima EW, Resende RO. 29.  2012. Characterization of Bean necrotic mosaic virus: a member of a novel evolutionary lineage within the genus Tospovirus. PLOS ONE 7:e38634 [Google Scholar]
  30. de Oliveira AS, Koolhaas I, Boiteux LS, Caldararu OF, Petrescu A-J. 29a.  et al. 2016. Cell death triggering and effector recognition by Sw-5 SD-CNL proteins from resistant and susceptible tomato isolines to Tomato spotted wilt virus. Mol. Plant Pathol. [Google Scholar]
  31. De Ronde D, Butterbach P, Kormelink R. 29b.  2014. Dominant resistance against plant viruses. Front. Plant Sci. 5:307 [Google Scholar]
  32. De Ronde D, Butterbach P, Lohuis D, Hedil M, Van Lent JWM, Kormelink R. 30.  2013. Tsw gene-based resistance is triggered by a functional RNA silencing suppressor protein of the Tomato spotted wilt virus. Mol. Plant Pathol. 14:405–15 [Google Scholar]
  33. de Ronde D, Pasquier A, Ying S, Butterbach P, Lohuis D, Kormelink R. 31.  2014. Analysis of Tomato spotted wilt virus NSS protein indicates the importance of the N-terminal domain for avirulence and RNA silencing suppression. Mol. Plant Pathol. 15:185–95 [Google Scholar]
  34. Dianese EC, de Fonseca MEN, Goldbach R, Kormelink R, Inoue-Nagata AK. 32.  et al. 2010. Development of a locus-specific, co-dominant SCAR marker for assisted-selection of the Sw-5 (Tospovirus resistance) gene cluster in a wide range of tomato accessions. Mol. Breed. 25:133–42 [Google Scholar]
  35. Dianese EC, Fonseca MEN, Inoue-Nagata AK, Resende RO, Boiteux LS. 33.  2011. Search in Solanum (section Lycopersicon) germplasm for sources of broad-spectrum resistance to four Tospovirus species. Euphytica 180:307–19 [Google Scholar]
  36. Dietzgen RG, Martin KM, Anderson G, Goodin MM. 34.  2012. In planta localization and interactions of Impatiens necrotic spot Tospovirus proteins. J. Gen. Virol. 93:2490–95 [Google Scholar]
  37. Díez M, Roselló S, Jordá C, Lacasa A, Costa J, Nuez F. 35.  1995. Agronomic behaviour of resistant tomato cvs. and lines to TSWV and influence of inoculation methods. Acta Hortic. 402:527–32 [Google Scholar]
  38. Dong JH, Yin YY, Fang Q, McBeath JH, Zhang ZK. 36.  2013. A new tospovirus causing chlorotic ringspot on Hippeastrum sp. in China. Virus Genes 46:567–70 [Google Scholar]
  39. Duijsings D, Kormelink R, Goldbach R. 37.  2001. In vivo analysis of the TSWV cap-snatching mechanism: single base complementarity and primer length requirements. EMBO J. 20:2545–52 [Google Scholar]
  40. Farnham G, Baulcombe DC. 38.  2006. Artificial evolution extends the spectrum of viruses that are targeted by a disease-resistance gene from potato. PNAS 103:18828–33 [Google Scholar]
  41. Feng Z, Chen X, Bao Y, Dong J, Zhang Z, Tao X. 39.  2013. Nucleocapsid of Tomato spotted wilt tospovirus forms mobile particles that traffic on an actin/endoplasmic reticulum network driven by myosin XI-K. New Phytol. 200:1212–24 [Google Scholar]
  42. Finlay KW. 40.  1953. Inheritance of spotted wilt resistance in tomato. II. Five genes controlling spotted wilt resistance in four tomato types. Aust. J. Biol. Sci. 6:153–63 [Google Scholar]
  43. Garcia-Cano E, Resende RO, Fernandez-Munoz R, Moriones E. 41.  2006. Synergistic interaction between Tomato chlorosis virus and Tomato spotted wilt virus results in breakdown of resistance in tomato. Phytopathology 96:1263–69 [Google Scholar]
  44. Garcia-Marcos A, Pacheco R, Manzano A, Aguilar E, Tenllado F. 42.  2013. Oxylipin biosynthesis genes positively regulate programmed cell death during compatible infections with the synergistic pair Potato virus XPotato virus Y and Tomato spotted wilt virus. J. Virol. 87:5769–83 [Google Scholar]
  45. Geerts-Dimitriadou C, Lu Y-Y, Geertsema C, Goldbach R, Kormelink R. 43.  2012. Analysis of the Tomato spotted wilt virus ambisense S RNA-encoded hairpin structure in translation. PLOS ONE 7:e31013 [Google Scholar]
  46. Giner A, Lakatos L, García-Chapa M, López-Moya JJ, Burgyán J. 44.  2010. Viral protein inhibits RISC activity by Argonaute binding through conserved WG/GW motifs. PLOS Pathog. 6:e1000996 [Google Scholar]
  47. Goldbach R, Peters D. 45.  1996. Molecular and biological aspects of tospoviruses. The Bunyaviridae RM Elliot 129–57 New York: Plenum Press [Google Scholar]
  48. Gordillo LF, Stevens MR, Millard MA, Geary B. 46.  2008. Screening two Lycopersicon peruvianum collections for resistance to Tomato spotted wilt virus. Plant Dis. 92:694–704 [Google Scholar]
  49. Hallwass M, De Oliveira AS, Dianese EDC, Lohuis D, Boiteux LS. 47.  et al. 2014. The Tomato spotted wilt virus cell-to-cell movement protein (NSM) triggers a hypersensitive response in Sw-5-containing resistant tomato lines and in Nicotiana benthamiana transformed with the functional Sw-5b resistance gene copy. Mol. Plant Pathol. 15:871–80 [Google Scholar]
  50. Harris CJ, Slootweg EJ, Goverse A, Baulcombe DC. 48.  2013. Stepwise artificial evolution of a plant disease resistance gene. PNAS 110:21189–94 [Google Scholar]
  51. Hassani-Mehraban A, Botermans M, Verhoeven JTJ, Meekes E, Saaijer J. 49.  et al. 2010. A distinct tospovirus causing necrotic streak on Alstroemeria sp in Colombia. Arch. Virol. 155:423–28 [Google Scholar]
  52. Hassani-Mehraban A, Cheewachaiwit S, Relevante C, Kormelink R, Peters D. 50.  2011. Tomato necrotic ring virus (TNRV), a recently described tospovirus species infecting tomato and pepper in Thailand. Eur. J. Plant Pathol. 130:449–56 [Google Scholar]
  53. Hedil M, Hassani-Mehraban A, Lohuis D, Kormelink R. 51.  2014. Analysis of the A-U rich hairpin from the intergenic region of tospovirus S RNA as target and inducer of RNA silencing. PLOS ONE 9:e106027 [Google Scholar]
  54. Hedil M, Sterken MG, de Ronde D, Lohuis D, Kormelink R. 52.  2015. Analysis of tospovirus NSS proteins in suppression of systemic silencing. PLOS ONE 10:e0134517 [Google Scholar]
  55. Hogenhout SA, Ammar ED, Whitfield AE, Redinbaugh MG. 53.  2008. Insect vector interactions with persistently transmitted viruses. Annu. Rev. Phytopathol. 46:327–59 [Google Scholar]
  56. Jahn M, Paran I, Hoffmann K, Radwanski ER, Livingstone KD. 54.  et al. 2000. Genetic mapping of the Tsw locus for resistance to the Tospovirus Tomato spotted wilt virus in Capsicum spp. and its relationship to the Sw-5 gene for resistance to the same pathogen in tomato. Mol. Plant-Microbe Interact. 13:673–82 [Google Scholar]
  57. Jones JDG, Dangl JL. 55.  2006. The plant immune system. Nature 444:323–29 [Google Scholar]
  58. Kikkert M, Van Lent J, Storms M, Bodegom P, Kormelink R, Goldbach R. 56.  1999. Tomato spotted wilt virus particle morphogenesis in plant cells. J. Virol. 73:2288–97 [Google Scholar]
  59. Kim S, Park M, Yeom S-I, Kim Y-M, Lee JM. 57.  et al. 2014. Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat. Genet. 46:270–78 [Google Scholar]
  60. Komoda K, Ishibashi K, Kawamura-Nagaya K, Ishikawa M. 58.  2014. Possible involvement of eEF1A in Tomato spotted wilt virus RNA synthesis. Virology 468:81–87 [Google Scholar]
  61. Kormelink R. 59.  2011. The molecular biology of tospoviruses and resistance strategies. Bunyaviridae: Molecular and Cellular Biology RM Elliott, A Plyusin 163–91 New York: Plenum Press [Google Scholar]
  62. Kormelink R, Dehaan P, Meurs C, Peters D, Goldbach R. 60.  1992. The nucleotide-sequence of the messenger-RNA segment of Tomato spotted wilt virus, a bunyavirus with 2 ambisense RNA segments. J. Gen. Virol. 73:2795–804 [Google Scholar]
  63. Kormelink R, Vanpoelwijk F, Peters D, Goldbach R. 61.  1992. Nonviral heterogeneous sequences at the 5′ ends of tomato spotted wilt virus messenger-RNAs. J. Gen. Virol. 73:2125–28 [Google Scholar]
  64. Latham LJ, Jones RAC. 62.  1998. Selection of resistance breaking strains of Tomato spotted wilt tospovirus. Ann. Appl. Biol. 133:385–402 [Google Scholar]
  65. Leastro MO, Pallas V, Resende RO, Sanchez-Navarro JA. 63.  2015. The movement proteins (NSM) of distinct tospoviruses peripherally associate with cellular membranes and interact with homologous and heterologous NSM and nucleocapsid proteins. Virology 478:39–49 [Google Scholar]
  66. Leipe DD, Koonin EV, Aravind L. 64.  2004. STAND, a class of P-loop NTPases including animal and plant regulators of programmed cell death: multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer. J. Mol. Biol. 343:1–28 [Google Scholar]
  67. Li C-X, Shi M, Tian J-H, Lin X-D, Kang Y-J. 65.  et al. 2015. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. eLife 4:e05378 [Google Scholar]
  68. Londono A, Capobianco H, Zhang S, Polston JE. 66.  2012. First record of Tomato chlorotic spot virus in the USA. Trop. Plant Pathol. 37:333–38 [Google Scholar]
  69. López C, Aramburu J, Galipienso L, Soler S, Nuez F, Rubio L. 67.  2011. Evolutionary analysis of tomato Sw-5 resistance-breaking isolates of Tomato spotted wilt virus. J. Gen. Virol. 92:210–15 [Google Scholar]
  70. Lukasik-Shreepaathy E, Vossen JH, Tameling WIL, de Vroomen MJ, Cornelissen BJC, Takken FLW. 68.  2012. Protein-protein interactions as a proxy to monitor conformational changes and activation states of the tomato resistance protein I-2. J. Exp. Bot. 63:3047–60 [Google Scholar]
  71. Maekawa T, Kufer TA, Schulze-Lefert P. 69.  2011. NLR functions in plant and animal immune systems: so far and yet so close. Nat. Immun. 12:818–26 [Google Scholar]
  72. Mandal B, Jain RK, Krishnareddy M, Kumar NKK, Ravi KS, Pappu HR. 70.  2012. Emerging problems of tospoviruses (Bunyaviridae) and their management in the Indian subcontinent. Plant Dis. 96:468–79 [Google Scholar]
  73. Margaria P, Bosco L, Vallino M, Ciuffo M, Mautino GC. 71.  et al. 2014. The NSS protein of Tomato spotted wilt virus is required for persistent infection and transmission by Frankliniella occidentalis. J. Virol. 88:5788–802 [Google Scholar]
  74. Margaria P, Ciuffo M, Pacifico D, Turina M. 72.  2007. Evidence that the nonstructural protein of Tomato spotted wilt virus is the avirulence determinant in the interaction with resistant pepper carrying the Tsw gene. Mol. Plant-Microbe Interact. 20:547–58 [Google Scholar]
  75. Margaria P, Ciuffo M, Rosa C, Turina M. 73.  2015. Evidence of a tomato spotted wilt virus resistance-breaking strain originated through natural reassortment between two evolutionary-distinct isolates. Virus Res. 196:157–61 [Google Scholar]
  76. Margaria P, Ciuffo M, Turina M. 74.  2004. Resistance breaking strain of Tomato spotted wilt virus (Tospovirus; Bunyaviridae) on resistant pepper cultivars in Almeria, Spain. Plant Pathol. 53:795 [Google Scholar]
  77. Maris PC, Joosten NN, Goldbach RW, Peters D. 75.  2004. Tomato spotted wilt virus infection improves host suitability for its vector Frankliniella occidentalis. Phytopathology 94:706–11 [Google Scholar]
  78. Meng J, Liu P, Zhu L, Zou C, Li J, Chen B. 76.  2015. Complete genome sequence of mulberry vein banding associated virus, a new tospovirus infecting mulberry. PLOS ONE 10:e0136196 [Google Scholar]
  79. Meyers BC, Kozik A, Griego A, Kuang HH, Michelmore RW. 77.  2003. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809–34 [Google Scholar]
  80. Minoia S, Petrozza A, D’Onofrio O, Piron F, Mosca G. 78.  et al. 2010. A new mutant genetic resource for tomato crop improvement by TILLING technology. BMC Res. Notes 3:69 [Google Scholar]
  81. Mokili JL, Rohwer F, Dutilh BE. 79.  2012. Metagenomics and future perspectives in virus discovery. Curr. Opin. Virol. 2:63–77 [Google Scholar]
  82. Morozov SY, Makarova SS, Erokhina TN, Kopertekh L, Schiemann J. 80.  et al. 2014. Plant 4/1 protein: potential player in intracellular, cell-to-cell and long-distance signaling. Front. Plant Sci. 5:26 [Google Scholar]
  83. Moury B, Palloix A, Selassie KG, Marchoux G. 81.  1997. Hypersensitive resistance to tomato spotted wilt virus in three Capsicum chinense accessions is controlled by a single gene and is overcome by virulent strains. Euphytica 94:45–52 [Google Scholar]
  84. Moury B, Selassie KG, Marchoux G, Daubeze AM, Palloix A. 82.  1998. High temperature effects on hypersensitive resistance to Tomato spotted wilt Tospovirus (TSWV) in pepper (Capsicum chinense Jacq.). Eur. J. Plant Pathol. 104:489–98 [Google Scholar]
  85. Multani PS, Cramer CS, Steiner RL, Creamer R. 83.  2009. Screening winter-sown onion entries for Iris yellow spot virus tolerance. HortScience 44:627–32 [Google Scholar]
  86. Mundt CC. 84.  2014. Durable resistance: a key to sustainable management of pathogens and pests. Infect. Genet. Evol. 27:446–55 [Google Scholar]
  87. Ngoc Huy H, Yang H-B, Kang B-C. 85.  2013. Identification and inheritance of a new source of resistance against Tomato spotted wilt virus (TSWV) in Capsicum. Sci. Hortic. 161:8–14 [Google Scholar]
  88. Paape M, Solovyev AG, Erokhina TN, Minina EA, Schepetilnikov MV. 86.  et al. 2006. At-4/1, an interactor of the Tomato spotted wilt virus movement protein, belongs to a new family of plant proteins capable of directed intra- and intercellular trafficking. Mol. Plant-Microbe Interact. 19:874–83 [Google Scholar]
  89. Pappu HR, Jones RA, Jain RK. 87.  2009. Global status of tospovirus epidemics in diverse cropping systems: successes achieved and challenges ahead. Virus Res. 141:219–36 [Google Scholar]
  90. Pavan S, Jacobsen E, Visser RGF, Bai Y. 88.  2010. Loss of susceptibility as a novel breeding strategy for durable and broad-spectrum resistance. Mol. Breed. 25:1–12 [Google Scholar]
  91. Peiró A, Cañizares MC, Rubio L, López C, Moriones E. 89.  et al. 2014. The movement protein (NSM) of Tomato spotted wilt virus is the avirulence determinant in the tomato Sw-5 gene-based resistance. Mol. Plant Pathol. 15:802–13 [Google Scholar]
  92. Persley DM, Thomas JE, Sharman M. 90.  2006. Tospoviruses: an Australian perspective. Australas. Plant Pathol. 35:161–80 [Google Scholar]
  93. Piron F, Nicolai M, Minoia S, Piednoir E, Moretti A. 91.  et al. 2010. An induced mutation in tomato eIF4E leads to immunity to two potyviruses. PLOS ONE 5:e11313 [Google Scholar]
  94. Plyusnin A, Beaty BJ, Elliott RM, Goldbach R, Kormelink R. 92.  et al. 2012. Bunyaviridae. Virus Taxonomy AMQ King, MJ Adams, EB Carstens, EJ Lefkowitz 725–41 Amsterdam: Elsevier [Google Scholar]
  95. Price DL, Memmott FD, Scott JW, Olson SM, Stevens MR. 93.  2007. Identification of molecular markers linked to a new Tomato spotted wilt virus resistance source in tomato. Rep. Tomato Genet. Coop. 57:35 [Google Scholar]
  96. Quito-Avila DF, Peralta EL, Martin RR, Ibarra MA, Alvarez RA. 94.  et al. 2014. Detection and occurrence of Melon yellow spot virus in Ecuador: an emerging threat to cucurbit production in the region. Eur. J. Plant Pathol. 140:193–97 [Google Scholar]
  97. Rairdan GJ, Collier SM, Sacco MA, Baldwin TT, Boettrich T, Moffett P. 95.  2008. The coiled-coil and nucleotide binding domains of the potato Rx disease resistance protein function in pathogen recognition and signaling. Plant Cell 20:739–51 [Google Scholar]
  98. Ramana CV, Rao PV, Rao RDVJP, Kumar SS, Reddy IP, Reddy YN. 96.  2011. Genetic analysis for Peanut bud necrosis virus (PBNV) resistance in tomato (Lycopersicon esculentum Mill.). Acta Hortic. 914:459–63 [Google Scholar]
  99. Renukadevi P, Nagendran K, Nakkeeran S, Karthikeyan G, Jawaharlal M. 97.  et al. 2015. First report of Tomato spotted wilt virus infection of Chrysanthemum in India. Plant Dis. 99:1190 [Google Scholar]
  100. Ribeiro D, Borst JW, Goldbach R, Kormelink R. 98.  2009. Tomato spotted wilt virus nucleocapsid protein interacts with both viral glycoproteins Gn and Gc in planta. Virology 383:121–30 [Google Scholar]
  101. Ribeiro D, Goldbach R, Kormelink R. 99.  2009. Requirements for ER-arrest and sequential exit to the Golgi of Tomato spotted wilt virus glycoproteins. Traffic 10:664–72 [Google Scholar]
  102. Ribeiro D, Jung M, Moling S, Borst JW, Goldbach R, Kormelink R. 100.  2013. The cytosolic nucleoprotein of the plant-infecting bunyavirus Tomato spotted wilt recruits endoplasmic reticulum–resident proteins to endoplasmic reticulum export sites. Plant Cell 25:3602–14 [Google Scholar]
  103. Rigola D, van Oeveren J, Janssen A, Bonne A, Schneiders H. 101.  et al. 2009. High-throughput detection of induced mutations and natural variation using KeyPoint (TM) technology. PLOS ONE 4:e4761 [Google Scholar]
  104. Riley DG, Joseph SV, Kelley WT, Olson S, Scott J. 102.  2011. Host plant resistance to Tomato spotted wilt virus (Bunyaviridae: Tospovirus) in tomato. HortScience 46:1626–33 [Google Scholar]
  105. Roggero P, Lisa V, Nervo G, Pennazio S. 103.  1996. Continuous high temperature can break the hypersensitivity of Capsicum chinense “PI 152225” to tomato spotted wilt tospovirus (TSWV). Phytopathol. Mediterr. 35:117–20 [Google Scholar]
  106. Roggero P, Masenga V, Tavella L. 104.  2002. Field isolates of Tomato spotted wilt virus overcoming resistance in pepper and their spread to other hosts in Italy. Plant Dis. 86:950–54 [Google Scholar]
  107. Rosello S, Diez MJ, Lacasa A, Jorda C, Nuez F. 105.  1997. Testing resistance to TSWV introgressed from Lycopersicon peruvianum by artificial transmission techniques. Euphytica 98:93–98 [Google Scholar]
  108. Rosello S, Diez MJ, Nuez F. 106.  1998. Genetics of tomato spotted wilt virus resistance coming from Lycoper-sicon peruvianum. Eur. J. Plant Pathol. 104:499–509 [Google Scholar]
  109. Rosello S, Ricarte B, Diez MJ, Nuez F. 107.  2001. Resistance to Tomato spotted wilt virus introgressed from Lycopersicon peruvianum in line UPV 1 may be allelic to Sw-5 and can be used to enhance the resistance of hybrids cultivars. Euphytica 119:357–67 [Google Scholar]
  110. Saidi M, Warade SD. 108.  2008. Tomato breeding for resistance to Tomato spotted wilt virus (TSWV): an overview of conventional and molecular approaches. Czech J. Genet. Plant Breed. 44:83–92 [Google Scholar]
  111. Schnettler E, Hemmes H, Huismann R, Goldbach R, Prins M, Kormelink R. 109.  2010. Diverging affinity of Tospovirus RNA silencing suppressor proteins, NSS, for various RNA duplex molecules. J. Virol. 84:11542–54 [Google Scholar]
  112. Seepiban C, Gajanandana O, Attathom T, Attathom S. 110.  2011. Tomato necrotic ringspot virus, a new tospovirus isolated in Thailand. Arch. Virol. 156:263–74 [Google Scholar]
  113. Sharman M, Persley DM. 111.  2006. Field isolates of Tomato spotted wilt virus overcoming resistance in capsicum in Australia. Australas. Plant Pathol. 35:123–28 [Google Scholar]
  114. Shi A, Vierling R, Grazzini R, Chen P, Caton H, Panthee D. 112.  2011. Identification of molecular markers for Sw-5 gene of tomato spotted wilt virus resistance. Am. J. Biotechnol. Mol. Sci. 1:8–16 [Google Scholar]
  115. Shimomoto Y, Kobayashi K, Okuda M. 113.  2014. Identification and characterization of Lisianthus necrotic ringspot virus, a novel distinct tospovirus species causing necrotic disease of lisianthus (Eustoma grandiflorum). J. Gen. Plant Pathol. 80:169–75 [Google Scholar]
  116. Singh P, Indi SS, Savithri HS. 114.  2014. Groundnut bud necrosis virus encoded NSM associates with membranes via its C-terminal domain. PLOS ONE 9:e99370 [Google Scholar]
  117. Snippe M, Borst JW, Goldbach R, Kormelink R. 115.  2007. Tomato spotted wilt virus Gc and N proteins interact in vivo. Virology 357:115–23 [Google Scholar]
  118. Snippe M, Goldbach R, Kormelink R. 116.  2005. Tomato spotted wilt virus particle assembly and the prospects of fluorescence microscopy to study protein-protein interactions involved. Adv. Virus Res. 65:63–120 [Google Scholar]
  119. Snippe M, Smeenk L, Goldbach R, Kormelink R. 117.  2007. The cytoplasmic domain of tomato spotted wilt virus Gn glycoprotein is required for Golgi localisation and interaction with Gc. Virology 363:272–79 [Google Scholar]
  120. Soellick TR, Uhrig JF, Bucher GL, Kellmann JW, Schreier PH. 118.  2000. The movement protein NSM of tomato spotted wilt tospovirus (TSWV): RNA binding, interaction with the TSWV N protein, and identification of interacting plant proteins. PNAS 97:2373–78 [Google Scholar]
  121. Sohrab SS, Bhattacharya P, Rana D, Kamal MA, Pande M. 119.  2014. Development of interspecific Solanum lycopersicum and screening for Tospovirus resistance. Saudi J. Biol. Sci. 22:730–38 [Google Scholar]
  122. Soler S, Cebolla-Cornejo J, Nuez F. 120.  2003. Control of diseases induced by tospoviruses in tomato: an update of the genetic approach. Phytopathol. Mediterr. 42:207–19 [Google Scholar]
  123. Soler S, Debreczeni D, Vidal E, Aramburu J, López C. 121.  et al. 2015. A new Capsicum baccatum accession shows tolerance to wild-type and resistance-breaking isolates of Tomato spotted wilt virus. Ann. Appl. Biol. 167:343–53 [Google Scholar]
  124. Soler S, Prohens J, López C, Aramburu J, Galipienso L, Nuez F. 122.  2010. Viruses infecting tomato in Valencia, Spain: occurrence, distribution and effect of seed origin. J. Phytopathol. 158:797–805 [Google Scholar]
  125. Somani A, Gopal J. 123.  2004. Screening of exotic potato germplasm for resistance to stem necrosis. Indian Phytopathol. 57:61–64 [Google Scholar]
  126. Spano R, Mascia T, Kormelink R, Gallitelli D. 124.  2015. Grafting on a non-transgenic tolerant tomato variety confers resistance to the infection of a Sw5-breaking strain of Tomato spotted wilt virus via RNA silencing. PLOS ONE 10:e0141319 [Google Scholar]
  127. Spassova MI, Prins TW, Folkertsma RT, Klein-Lankhorst RM, Hille J. 125.  et al. 2001. 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. 7:151–61 [Google Scholar]
  128. Sreekanth M, Sreeramulu M, Rao RD, Babu BS, Babu TR. 126.  2002. Evaluation of greengram genotypes (Vigna radiata L. Wilczek) for resistance to Thrips palmi Karny and Peanut bud necrosis virus*. Indian J. Plant Prot. 30:109–14 [Google Scholar]
  129. Stevens MR, Heiny D, Rhoads D, Griffiths P, Scott J. 127.  1995. A linkage map of the tomato spotted wilt virus resistance gene Sw-5 using near isogenic lines and an interspecific cross. Acta Hortic. 431:385–92 [Google Scholar]
  130. Stevens MR, Price DL, Memmott FD, Scott JW, Olson SM. 128.  2007. Identification of markers linked to Sw-7 a new Tomato spotted wilt virus resistance gene, derived from S. chilense. Abstracts from the 2007 Tomato Breeders Roundtable State College, PA: Pa. State Univ http://tgc.ifas.ufl.edu/2007/2007IndividualAbsPDf/Identification%20of%20Markers%20Linked%20to%20Sw.pdf [Google Scholar]
  131. Stevens MR, Scott S, Gergerich R. 129.  1994. Evaluation of seven Lycopersicon species for resistance to tomato spotted wilt virus (TSWV). Euphytica 80:79–84 [Google Scholar]
  132. Stevens MR, Scott SJ, Gergerich RC. 130.  1992. Inheritance of a gene for resistance to tomato spotted wilt virus (TSWV) from Lycopersicon peruvianum Mill. Euphytica 59:9–17 [Google Scholar]
  133. Sugiyama M, Kawazu Y, Fukino N, Yoshioka Y, Shimomura K. 131.  et al. 2015. Mapping of quantitative trait loci for Melon yellow spot virus resistance in cucumber (Cucumis sativus L.). Euphytica 205:615–25 [Google Scholar]
  134. Sugiyama M, Okuda M, Sakata Y. 132.  2009. Evaluation of resistance to melon yellow spot virus in a cucumber germplasm collection. Plant Breed. 128:696–700 [Google Scholar]
  135. Sugiyama M, Yoshioka Y, Sakata Y. 133.  2009. Effect of temperature on symptom expression and viral spread of Melon yellow spot virus in resistant cucumber accessions. J. Gen. Plant Pathol. 75:381–87 [Google Scholar]
  136. Takahashi H, Suzuki M, Natsuaki K, Shigyo T, Hino K. 134.  et al. 2001. Mapping the virus and host genes involved in the resistance response in cucumber mosaic virus-infected Arabidopsis thaliana. Plant Cell Physiol. 42:340–47 [Google Scholar]
  137. Takken FLW, Goverse A. 135.  2012. How to build a pathogen detector: structural basis of NB-LRR function. Curr. Opin. Plant Biol. 15:375–84 [Google Scholar]
  138. Tentchev D, Verdin E, Marchal C, Jacquet M, Aguilar JM, Moury B. 136.  2011. Evolution and structure of Tomato spotted wilt virus populations: evidence of extensive reassortment and insights into emergence processes. J. Gen. Virol. 92:961–73 [Google Scholar]
  139. Torres R, Larenas J, Fribourg C, Romero J. 137.  2012. Pepper necrotic spot virus, a new tospovirus infecting solanaceous crops in Peru. Arch. Virol. 157:609–15 [Google Scholar]
  140. Tripathi D, Raikhy G, Goodin MM, Dietzgen RG, Pappu HR. 138.  2015. In vivo localization of Iris yellow spot Tospovirus (Bunyaviridae)-encoded proteins and identification of interacting regions of nucleocapsid and movement proteins. PLOS ONE 10:e0118973 [Google Scholar]
  141. Tripathi D, Raikhy G, Pappu HR. 139.  2015. Movement and nucleocapsid proteins coded by two tospovirus species interact through multiple binding regions in mixed infections. Virology 478:137–47 [Google Scholar]
  142. Turina M, Tavella L, Ciuffo M. 140.  2012. Tospoviruses in the Mediterranean area. Adv. Virus Res. 84:403–37 [Google Scholar]
  143. van Knippenberg I, Lamine M, Goldbach R, Kormelink R. 141.  2005. Tomato spotted wilt virus transcriptase in vitro displays a preference for cap donors with multiple base complementarity to the viral template. Virology 335:122–30 [Google Scholar]
  144. van Schie CCN, Takken FLW. 142.  2014. Susceptibility genes 101: how to be a good host. Annu. Rev. Phytopathol. 52:551–81 [Google Scholar]
  145. von Bargen S, Salchert K, Paape M, Piechulla B, Kellmann JW. 143.  2001. Interactions between the tomato spotted wilt virus movement protein and plant proteins showing homologies to myosin, kinesin and DNAJ-like chaperones. Plant Physiol. Biochem. 39:1083–93 [Google Scholar]
  146. Webster CG, Frantz G, Reitz SR, Funderburk JE, Mellinger HC. 144.  et al. 2015. Emergence of Groundnut ringspot virus and Tomato chlorotic spot virus in vegetables in Florida and the southeastern United States. Phytopathology 105:388–98 [Google Scholar]
  147. Webster CG, Reitz SR, Perry KL, Adkins S. 145.  2011. A natural M RNA reassortant arising from two species of plant- and insect-infecting bunyaviruses and comparison of its sequence and biological properties to parental species. Virology 413:216–25 [Google Scholar]
  148. Wen RH, Khatabi B, Ashfield T, Maroof MAS, Hajimorad MR. 146.  2013. The HC-Pro and P3 cistrons of an avirulent Soybean mosaic virus are recognized by different resistance genes at the complex Rsv1 locus. Mol. Plant-Microbe Interact. 26:203–15 [Google Scholar]
  149. Whitfield AE, Falk BW, Rotenberg D. 147.  2015. Insect vector-mediated transmission of plant viruses. Virology 479:278–89 [Google Scholar]
  150. Whitfield AE, Ullman DE, German TL. 148.  2005. Tospovirus-thrips interactions. Annu. Rev. Phytopathol. 43:459–89 [Google Scholar]
  151. Whitham S, McCormick S, Baker B. 149.  1996. The N gene of tobacco confers resistance to tobacco mosaic virus in transgenic tomato. PNAS 93:8776–81 [Google Scholar]
  152. Yin Y, Zheng K, Dong J, Fang Q, Wu S. 150.  et al. 2014. Identification of a new tospovirus causing necrotic ringspot on tomato in China. Virol. J. 11:213 [Google Scholar]
  153. Zarzynska-Nowak A, Rymelska N, Borodynko N, Hasiow-Jaroszewska B. 151.  2016. The occurrence of Tomato yellow ring virus on tomato in Poland. Plant Dis. 100:234 [Google Scholar]
  154. Zhou J, Kantartzi SK, Wen RH, Newman M, Hajimorad MR. 152.  et al. 2011. Molecular characterization of a new tospovirus infecting soybean. Virus Genes 43:289–95 [Google Scholar]
  155. Zhu Y, Qian W, Hua J. 153.  2010. Temperature modulates plant defense responses through NB-LRR proteins. PLOS Pathog. 6:e1000844 [Google Scholar]
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