1932

Abstract

Tospoviruses are among the most important plant pathogens and cause serious crop losses worldwide. Tospoviruses have evolved to smartly utilize the host cellular machinery to accomplish their life cycle. Plants mount two layers of defense to combat their invasion. The first one involves the activation of an antiviral RNA interference (RNAi) defense response. However, tospoviruses encode an RNA silencing suppressor that enables them to counteract antiviral RNAi. To further combat viral invasion, plants also employ intracellular innate immune receptors (e.g., Sw-5b and Tsw) to recognize different viral effectors (e.g., NSm and NSs). This leads to the triggering of a much more robust defense against tospoviruses called effector-triggered immunity (ETI). Tospoviruses have further evolved their effectors and can break Sw-5b-/Tsw-mediated resistance. The arms race between tospoviruses and both layers of innate immunity drives the coevolution of host defense and viral genes involved in counter defense. In this review, a state-of-the-art overview is presented on the tospoviral life cycle and the multilined interplays between tospoviruses and the distinct layers of defense.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-082718-100309
2019-08-25
2024-12-05
Loading full text...

Full text loading...

/deliver/fulltext/phyto/57/1/annurev-phyto-082718-100309.html?itemId=/content/journals/10.1146/annurev-phyto-082718-100309&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Adkins S, Quadt R, Choi TJ, Ahlquist P, German T 1995. An RNA-dependent RNA polymerase activity associated with virions of tomato spotted wilt virus, a plant- and insect-infecting bunyavirus. Virology 207:308–11
    [Google Scholar]
  2. 2. 
    Almasi A, Csillery G, Csomor Z, Nemes K, Palkovics L et al. 2015. Phylogenetic analysis of Tomato spotted wilt virus (TSWV) NSs protein demonstrates the isolated emergence of resistance-breaking strains in pepper. Virus Genes 50:71–78
    [Google Scholar]
  3. 3. 
    Almási A, Nemes K, Csomor Z, Tobias I, Palkovics L, Salanki K 2017. A single point mutation in Tomato spotted wilt virus NSs protein is sufficient to overcome Tsw-gene-mediated resistance in pepper. J. Gen. Virol. 98:1521–25
    [Google Scholar]
  4. 4. 
    Aramburu J, Marti M. 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. 5. 
    Bezerra IC, de O, Resende R, Pozzer L, Nagata T, Kormelink R, De Avila AC 1999. Increase of tospoviral diversity in Brazil with the identification of two new tospovirus species, one from chrysanthemum and one from zucchini. Phytopathology 89:823–30
    [Google Scholar]
  6. 6. 
    Black LL, Hobbs HA, Gatti JM 1991. Tomato spotted wilt virus resistance in Capsicum chinense Pi 152225 and 159236. Plant Dis 75:863
    [Google Scholar]
  7. 7. 
    Blakqori G, Delhaye S, Habjan M, Blair CD, Sanchez-Vargas I et al. 2007. La Crosse bunyavirus nonstructural protein NSs serves to suppress the type I interferon system of mammalian hosts. J. Virol. 81:4991–99
    [Google Scholar]
  8. 8. 
    Boevink P, Oparka K, Santa Cruz S, Martin B, Betteridge A, Hawes C 1998. Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J 15:441–47
    [Google Scholar]
  9. 9. 
    Boiteux LS. 1995. Allelic relationships between genes for resistance to Tomato spotted wilt tospovirus in Capsicum chinense. Theor. Appl. Genet 90:146–9
    [Google Scholar]
  10. 10. 
    Boiteux LS, De Avila AC 1994. Inheritance of a resistance specific to Tomato spotted wilt tospovirus in Capsicum Chinense Pi 159236. Euphytica 75:139–42
    [Google Scholar]
  11. 11. 
    Bouloy M, Plotch SJ, Krug RM 1978. Globin mRNAs are primers for the transcription of influenza viral RNA in vitro. PNAS 75:4886–90
    [Google Scholar]
  12. 12. 
    Brandizzi F, Snapp EL, Roberts AG, Lippincott-Schwartz J, Hawes C 2002. Membrane protein transport between the endoplasmic reticulum and the golgi in tobacco leaves is energy dependent but cytoskeleton independent: evidence from selective photobleaching. Plant Cell 14:1293–309
    [Google Scholar]
  13. 13. 
    Brommonschenkel SH, Frary A, Frary A, Tanksley SD 2000. The broad-spectrum tospovirus resistance gene Sw-5 of tomato is a homolog of the root-knot nematode resistance gene Mi. Mol. Plant-Microbe Interact 13:1130–38
    [Google Scholar]
  14. 14. 
    Bucher E, Sijen T, de Haan P, Goldbach R, Prins M 2003. Negative-strand tospoviruses and tenuiviruses carry a gene for a suppressor of gene silencing at analogous genomic positions. J. Virol. 77:1329–36
    [Google Scholar]
  15. 15. 
    Caplan J, Padmanabhan M, Dinesh-Kumar SP 2008. Plant NB-LRR immune receptors: from recognition to transcriptional reprogramming. Cell Host Microbe 3:126–35
    [Google Scholar]
  16. 16. 
    Casteel CL, Walling LL, Paine TD 2006. Behavior and biology of the tomato psyllid, Bactericerca cockerelli, in response to the Mi-1.2 gene. Entomol. Exp. Appl. 121:67–72
    [Google Scholar]
  17. 17. 
    Chan AY, Vreede FT, Smith M, Engelhardt OG, Fodor E 2006. Influenza virus inhibits RNA polymerase II elongation. Virology 351:210–17
    [Google Scholar]
  18. 18. 
    Chen XJ, Zhu M, Jiang L, Zhao WY, Li J et al. 2016. A multilayered regulatory mechanism for the autoinhibition and activation of a plant CC-NB-LRR resistance protein with an extra N-terminal domain. New Phytol 212:161–75
    [Google Scholar]
  19. 19. 
    Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G 2006. The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18:465–76
    [Google Scholar]
  20. 20. 
    Chung BN, Choi HS, Yang EY, Cho JD, Cho IS et al. 2012. Tomato spotted wilt virus isolates giving different infection in commercial Capsicum annuum cultivars. Plant Pathol. J. 28:87–92
    [Google Scholar]
  21. 21. 
    Ciuffo M, Finetti-Sialer MM, Gallitelli D, Turina M 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]
  22. 22. 
    Collier SM, Moffett P. 2009. NB-LRRs work a “bait and switch” on pathogens. Trends Plant Sci 14:521–29
    [Google Scholar]
  23. 23. 
    Dahan-Meir T, Filler-Hayut S, Melamed-Bessudo C, Bocobza S, Czosnek H et al. 2018. Efficient in planta gene targeting in tomato using geminiviral replicons and the CRISPR/Cas9 system. Plant J 95:5–16
    [Google Scholar]
  24. 24. 
    da Silva LL, Snapp EL, Denecke J, Lippincott-Schwartz J, Hawes C, Brandizzi F 2004. Endoplasmic reticulum export sites and Golgi bodies behave as single mobile secretory units in plant cells. Plant Cell 16:1753–71
    [Google Scholar]
  25. 25. 
    de Avila AC, Huguenot C, de O, Resende R, Kitajima EW, Goldbach RW, Peters D 1990. Serological differentiation of 20 isolates of tomato spotted wilt virus. J. Gen. Virol. 71:2801–7
    [Google Scholar]
  26. 26. 
    de Haan P, Gielen JJ, Prins M, Wijkamp IG, van Schepen A et al. 1992. Characterization of RNA-mediated resistance to tomato spotted wilt virus in transgenic tobacco plants. Nat. Biotechnol. 10:1133–37
    [Google Scholar]
  27. 27. 
    de Haan P, Kormelink R, Resende RD, Vanpoelwijk F, Peters D, Goldbach R 1991. Tomato spotted wilt virus L RNA encodes a putative RNA-polymerase. J. Gen. Virol. 72:2207–16
    [Google Scholar]
  28. 28. 
    de Medeiros RB, Figueiredo J, Resende RD, De Avila AC 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. 29. 
    De Oliveira AS, Koolhaas I, Boiteux LS, Caldararu OF, Petrescu AJ 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 17:1442–54
    [Google Scholar]
  30. 30. 
    de Oliveira VC, da Silva Morgado F, Ardisson-Araujo DM, Resende RO, Ribeiro BM 2015. The silencing suppressor (NSs) protein of the plant virus Tomato spotted wilt virus enhances heterologous protein expression and baculovirus pathogenicity in cells and lepidopteran insects. Arch. Virol. 160:2873–79
    [Google Scholar]
  31. 31. 
    de Ronde D, Butterbach P, Lohuis D, Hedil M, Van Lent JWM, Kormelink R 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]
  32. 32. 
    de Ronde D, Lohuis D, Kormelink R 2018. Identification and characterization of a new class of Tomato spotted wilt virus isolates that break Tsw-based resistance in a temperature-dependent manner. Plant Pathol 68:60–71
    [Google Scholar]
  33. 33. 
    de Ronde D, Pasquier A, Ying S, Butterbach P, Lohuis D, Kormelink R 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. 34. 
    Dodds PN, Lawrence GJ, Ellis JG 2001. Six amino acid changes confined to the leucine-rich repeat β-strand/β-turn motif determine the difference between the P and P2 rust resistance specificities in flax. Plant Cell 13:163–78
    [Google Scholar]
  35. 35. 
    Duijsings D, Kormelink R, Goldbach R 1999. Alfalfa mosaic virus RNAs serve as cap donors for tomato spotted wilt virus transcription during coinfection of Nicotiana benthamiana. J. Virol 73:5172–75
    [Google Scholar]
  36. 36. 
    Farnham G, Baulcombe DC. 2006. Artificial evolution extends the spectrum of viruses that are targeted by a disease-resistance gene from potato. PNAS 103:18828–33
    [Google Scholar]
  37. 37. 
    Feng ZK, Chen XJ, Bao YQ, Dong JH, Zhang ZK, Tao XR 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]
  38. 38. 
    Feng ZK, Xue F, Xu M, Chen XJ, Zhao WY et al. 2016. The ER-membrane transport system is critical for intercellular trafficking of the NSm movement protein and tomato spotted wilt tospovirus. PLOS Pathog 12:e1005443
    [Google Scholar]
  39. 39. 
    Ferrand L, Garcia ML, Resende RO, Balatti PA, Dal Bo E 2015. First report of a resistance-breaking isolate of Tomato spotted wilt virus infecting sweet pepper harboring the Tsw gene in Argentina. Plant Dis 99:1869–70
    [Google Scholar]
  40. 40. 
    Foster SJ, Park TH, Pel M, Brigneti G, Sliwka J et al. 2009. Rpi-vnt1.1, a Tm-22 homolog from Solanum venturii, confers resistance to potato late blight. Mol. Plant-Microbe Interact. 22:589–600
    [Google Scholar]
  41. 41. 
    García-Cano E, Resende RO, Fernández-Muñoz R, Moriones E 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]
  42. 42. 
    Garcia-Ruiz H, Peralta SMG, Harte-Maxwell PA 2018. Tomato spotted wilt virus NSs protein supports infection and systemic movement of a potyvirus and is a symptom determinant. Viruses 10:E129
    [Google Scholar]
  43. 43. 
    Geerts-Dimitriadou C, Goldbach R, Kormelink R 2011. Preferential use of RNA leader sequences during influenza A transcription initiation in vivo. Virology 409:27–32
    [Google Scholar]
  44. 44. 
    Geerts-Dimitriadou C, Zwart MP, Goldbach R, Kormelink R 2011. Base-pairing promotes leader selection to prime in vitro influenza genome transcription. Virology 409:17–26
    [Google Scholar]
  45. 45. 
    Gielen JJL, de Haan P, Kool AJ, Peters D, van Grinsven MQJM, Goldbach RW 1991. Engineered resistance to Tomato spotted wilt virus, a negative-strand RNA virus. Nat. Biotechnol. 9:1363–67
    [Google Scholar]
  46. 46. 
    Gilbertson RL, Batuman O, Webster CG, Adkins S 2015. Role of the insect supervectors Bemisia tabaci and Frankliniella occidentalis in the emergence and global spread of plant viruses. Annu. Rev. Virol. 2:67–93
    [Google Scholar]
  47. 47. 
    Giner A, Lakatos L, Garcia-Chapa M, Lopez-Moya JJ, Burgyan J 2010. Viral protein inhibits RISC activity by argonaute binding through conserved WG/GW motifs. PLOS Pathog 6:e1000996
    [Google Scholar]
  48. 48. 
    Goulden MG, Kohm BA, Cruz SS, Kavanagh TA, Baulcombe DC 1993. A feature of the coat protein of Potato virus X affects both induced virus-resistance in potato and viral fitness. Virology 197:293–302
    [Google Scholar]
  49. 49. 
    Guo Y, Liu BC, Ding ZZ, Li GB, Liu MZ et al. 2017. Distinct mechanism for the formation of the ribonucleoprotein complex of Tomato spotted wilt virus. J. Virol 91:e00892–17
    [Google Scholar]
  50. 50. 
    Guo Z, Li Y, Ding SW 2018. Small RNA-based antimicrobial immunity. Nat. Rev. Immunol. 19:31–44
    [Google Scholar]
  51. 51. 
    Hallwass M, de Oliveira AS, de Campos Dianese E, Lohuis D, Boiteux LS 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]
  52. 52. 
    Harris CJ, Slootweg EJ, Goverse A, Baulcombe DC 2013. Stepwise artificial evolution of a plant disease resistance gene. PNAS 110:21189–94
    [Google Scholar]
  53. 53. 
    Hashimoto M, Neriya Y, Yamaji Y, Namba S 2016. Recessive resistance to plant viruses: potential resistance genes beyond translation initiation factors. Front. Microbiol. 7:1695
    [Google Scholar]
  54. 54. 
    Hassani-Mehraban A, Brenkman AB, van den Broek NJF, Goldbach R, Kormelink R 2009. RNAi-mediated transgenic tospovirus resistance broken by intraspecies silencing suppressor protein complementation. Mol. Plant-Microbe Interact. 22:1250–57
    [Google Scholar]
  55. 55. 
    Hedil M, de Ronde D, Kormelink R 2017. Biochemical analysis of NSs from different tospoviruses. Virus Res 242:149–55
    [Google Scholar]
  56. 56. 
    Hedil M, Kormelink R. 2016. Viral RNA silencing suppression: the enigma of bunyavirus NSs proteins. Viruses 8:E208
    [Google Scholar]
  57. 57. 
    Hedil M, Sterken MG, de Ronde D, Lohuis D, Kormelink R 2015. Analysis of tospovirus NSs proteins in suppression of systemic silencing. PLOS ONE 10:e0134517
    [Google Scholar]
  58. 58. 
    Jahn M, Paran I, Hoffmann K, Radwanski ER, Livingstone KD 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]
  59. 59. 
    Jan FJ, Fagoaga C, Pang SZ, Gonsalves D 2000. A minimum length of N gene sequence in transgenic plants is required for RNA-mediated tospovirus resistance. J. Gen. Virol. 81:235–42
    [Google Scholar]
  60. 60. 
    Jiang L, Huang Y, Sun L, Wang B, Zhu M et al. 2017. Occurrence and diversity of Tomato spotted wilt virus isolates breaking the Tsw resistance gene of Capsicum chinense in Yunnan, southwest China. Plant Pathol 66:980–89
    [Google Scholar]
  61. 61. 
    Jones JD, Vance RE, Dangl JL 2016. Intracellular innate immune surveillance devices in plants and animals. Science 354:aaf6395
    [Google Scholar]
  62. 62. 
    Kavanagh T, Goulden M, Santa Cruz S, Chapman S, Barker I, Baulcombe D 1992. Molecular analysis of a resistance-breaking strain of potato virus X. Virology 189:609–17
    [Google Scholar]
  63. 63. 
    Kikkert M, Van Lent J, Storms M, Bodegom P, Kormelink R, Goldbach R 1999. Tomato spotted wilt virus particle morphogenesis in plant cells. J. Virol. 73:2288–97
    [Google Scholar]
  64. 64. 
    Kim SB, Kang WH, Huy HN, Yeom SI, An JT et al. 2017. Divergent evolution of multiple virus-resistance genes from a progenitor in Capsicum spp. New Phytol 213:886–99
    [Google Scholar]
  65. 65. 
    Kim SH, Qi D, Ashfield T, Helm M, Innes RW 2016. Using decoys to expand the recognition specificity of a plant disease resistance protein. Science 351:684–87
    [Google Scholar]
  66. 66. 
    Kohm BA, Goulden MG, Gilbert JE, Kavanagh TA, Baulcombe DC 1993. A Potato virus X resistance gene mediates an induced, nonspecific resistance in protoplasts. Plant Cell 5:913–20
    [Google Scholar]
  67. 67. 
    Komoda K, Ishibashi K, Kawamura-Nagaya K, Ishikawa M 2014. Possible involvement of eEF1A in Tomato spotted wilt virus RNA synthesis. Virology 468:81–87
    [Google Scholar]
  68. 68. 
    Komoda K, Narita M, Yamashita K, Tanaka I, Yao M 2017. Asymmetric trimeric ring structure of the nucleocapsid protein of tospovirus. J. Virol. 91:e01002–17
    [Google Scholar]
  69. 69. 
    Kormelink R. 2011. The molecular biology of tospoviruses and resistance strategies. Bunyaviridae: Molecular and Cellular Biology A Plyusnin, RM Elliott 163–91 New York: Plenum Press
    [Google Scholar]
  70. 70. 
    Kormelink R, Garcia ML, Goodin M, Sasaya T, Haenni AL 2011. Negative-strand RNA viruses: the plant-infecting counterparts. Virus Res 162:184–202
    [Google Scholar]
  71. 71. 
    Kormelink R, Kitajima EW, de Haan P, Zuidema D, Peters D, Goldbach R 1991. The nonstructural protein (Nss) encoded by the ambisense-S RNA segment of Tomato spotted wilt virus is associated with fibrous structures in infected-plant cells. Virology 181:459–68
    [Google Scholar]
  72. 72. 
    Kormelink R, Storms M, Van Lent J, Peters D, Goldbach R 1994. Expression and subcellular location of the NSm protein of Tomato spotted wilt virus (TSWV), a putative viral movement protein. Virology 200:56–65
    [Google Scholar]
  73. 73. 
    Kormelink R, van Poelwijk F, Peters D, Goldbach R 1992. Nonviral heterogeneous sequences at the 5′ ends of Tomato spotted wilt virus messenger-RNAs. J. Gen. Virol. 73:2125–8
    [Google Scholar]
  74. 74. 
    Lan H, Chen H, Liu Y, Jiang C, Mao Q et al. 2016. Small interfering RNA pathway modulates initial viral infection in midgut epithelium of insect after ingestion of virus. J. Virol. 90:917–29
    [Google Scholar]
  75. 75. 
    Latham LJ, Jones RAC. 1998. Selection of resistance breaking strains of tomato spotted wilt tospovirus. Ann. Appl. Biol. 133:385–402
    [Google Scholar]
  76. 76. 
    Leastro MO, De Oliveira AS, Pallas V, Sanchez-Navarro JA, Kormelink R, Resende RO 2017. The NSm proteins of phylogenetically related tospoviruses trigger Sw-5b-mediated resistance dissociated of their cell-to-cell movement function. Virus Res 240:25–34
    [Google Scholar]
  77. 77. 
    Lewandowski DJ, Adkins S. 2005. The tubule-forming NSm protein from Tomato spotted wilt virus complements cell-to-cell and long-distance movement of Tobacco mosaic virus hybrids. Virology 342:26–37
    [Google Scholar]
  78. 78. 
    Li J, Feng ZK, Wu JY, Huang Y, Lu G et al. 2015. Structure and function analysis of nucleocapsid protein of Tomato spotted wilt virus interacting with RNA using homology modeling. J. Biol. Chem. 290:3950–61
    [Google Scholar]
  79. 79. 
    Li J, Huang H, Zhu M, Huang S, Zhang W et al. 2019. A plant immune receptor adopts a two-step recognition mechanism to enhance viral effector perception. Mol. Plant 12:2248–62
    [Google Scholar]
  80. 80. 
    Li W, Lewandowski DJ, Hilf ME, Adkins S 2009. Identification of domains of the Tomato spotted wilt virus NSm protein involved in tubule formation, movement and symptomatology. Virology 390:110–21
    [Google Scholar]
  81. 81. 
    Lin T, Zhu G, Zhang J, Xu X, Yu Q et al. 2014. Genomic analyses provide insights into the history of tomato breeding. Nat. Genet. 46:1220–26
    [Google Scholar]
  82. 82. 
    Lopez C, Aramburu J, Galipienso L, Soler S, Nuez F, Rubio L 2011. Evolutionary analysis of tomato Sw-5 resistance-breaking isolates of Tomato spotted wilt virus. J. Gen. Virol 92:210–15
    [Google Scholar]
  83. 83. 
    Lovato FA, Inoue-Nagata AK, Nagata T, de Avila AC, Pereira LAR, Resende RO 2008. The N protein of Tomato spotted wilt virus (TSWV) is associated with the induction of programmed cell death (PCD) in Capsicum chinense plants, a hypersensitive host to TSWV infection. Virus Res 137:245–52
    [Google Scholar]
  84. 84. 
    Mackenzie DJ, Ellis PJ. 1992. Resistance to Tomato spotted wilt virus-infection in transgenic tobacco expressing the viral nucleocapsid gene. Mol. Plant-Microbe Interact. 5:34–40
    [Google Scholar]
  85. 85. 
    Maekawa T, Cheng W, Spiridon LN, Toller A, Lukasik E et al. 2011. Coiled-coil domain-dependent homodimerization of intracellular barley immune receptors defines a minimal functional module for triggering cell death. Cell Host Microbe 9:187–99
    [Google Scholar]
  86. 86. 
    Maes P, Alkhovsky SV, Bao YM, Beer M, Birkhead M et al. 2018. Taxonomy of the family Arenaviridae and the order Bunyavirales: update 2018. Arch. Virol. 163:2295–310
    [Google Scholar]
  87. 87. 
    Margaria P, Bosco L, Vallino M, Ciuffo M, Mautino GC 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]
  88. 88. 
    Margaria P, Ciuffo M, Pacifico D, Turina M 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]
  89. 89. 
    Margaria P, Ciuffo M, Rosa C, Turina M 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]
  90. 90. 
    Margaria P, Miozzi L, Ciuffo M, Rosa C, Axtell MJ et al. 2016. Comparison of small RNA profiles in Nicotiana benthamiana and Solanum lycopersicum infected by polygonum ringspot tospovirus reveals host-specific responses to viral infection. Virus Res 211:38–45
    [Google Scholar]
  91. 91. 
    Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM 1998. The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307–19
    [Google Scholar]
  92. 92. 
    Mir MA, Duran WA, Hjelle BL, Ye C, Panganiban AT 2008. Storage of cellular 5′ mRNA caps in P bodies for viral cap-snatching. PNAS 105:19294–99
    [Google Scholar]
  93. 93. 
    Mitter N, Koundal V, Williams S, Pappu H 2013. Differential expression of tomato spotted wilt virus-derived viral small RNAs in infected commercial and experimental host plants. PLOS ONE 8:e76276
    [Google Scholar]
  94. 94. 
    Mucyn TS, Clemente A, Andriotis VM, Balmuth AL, Oldroyd GE et al. 2006. The tomato NBARC-LRR protein Prf interacts with Pto kinase in vivo to regulate specific plant immunity. Plant Cell 18:2792–806
    [Google Scholar]
  95. 95. 
    Nebenfuhr A, Gallagher LA, Dunahay TG, Frohlick JA, Mazurkiewicz AM et al. 1999. Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol 121:1127–42
    [Google Scholar]
  96. 96. 
    Nombela G, Williamson VM, Muniz M 2003. The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Mol. Plant-Microbe Interact 16:645–49
    [Google Scholar]
  97. 97. 
    Oliveira VC, Bartasson L, de Castro ME, Correa JR, Ribeiro BM, Resende RO 2011. A silencing suppressor protein (NSs) of a tospovirus enhances baculovirus replication in permissive and semipermissive insect cell lines. Virus Res 155:259–67
    [Google Scholar]
  98. 98. 
    Oliver JE, Whitfield AE. 2016. The genus Tospovirus: emerging bunyaviruses that threaten food security. Annu. Rev. Virol. 29:101–24
    [Google Scholar]
  99. 99. 
    Pang SZ, Slightom JL, Gonsalves D 1993. Different mechanisms protect transgenic tobacco against tomato spotted wilt and impatiens necrotic spot tospoviruses. Nat. Biotechnol. 11:819–24
    [Google Scholar]
  100. 100. 
    Peiro A, Canizares MC, Rubio L, Lopez C, Moriones E 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]
  101. 101. 
    Peng JC, Chen TC, Raja JAJ, Yang CF, Chien WC et al. 2014. Broad-spectrum transgenic resistance against distinct tospovirus species at the genus level. PLOS ONE 9:e96073
    [Google Scholar]
  102. 102. 
    Pozzer L, Bezerra IC, Kormelink R, Prins M, Peters D et al. 1999. Characterization of a tospovirus isolate of Iris yellow spot virus associated with a disease in onion fields in Brazil. Plant Dis 83:345–50
    [Google Scholar]
  103. 103. 
    Prins M, de Haan P, Luyten R, van Veller M, van Grinsven MQJM, Goldbach R 1995. Broad resistance to tospoviruses in transgenic tobacco plants expressing 3 tospoviral nucleoprotein gene-sequences. Mol. Plant-Microbe Interact. 8:85–91
    [Google Scholar]
  104. 104. 
    Prins M, Kikkert M, Ismayadi C, de Graauw W, de Haan P, Goldbach R 1997. Characterization of RNA-mediated resistance to tomato spotted wilt virus in transgenic tobacco plants expressing NSm gene sequences. Plant Mol. Biol. 33:235–43
    [Google Scholar]
  105. 105. 
    Ramesh SV, Williams S, Kappagantu M, Mitter N, Pappu HR 2017. Transcriptome-wide identification of host genes targeted by tomato spotted wilt virus-derived small interfering RNAs. Virus Res 238:13–23
    [Google Scholar]
  106. 106. 
    Reguera J, Weber F, Cusack S 2010. Bunyaviridae RNA polymerases (L-protein) have an N-terminal, influenza-like endonuclease domain, essential for viral cap-dependent transcription. PLOS Pathog 6:e1001101
    [Google Scholar]
  107. 107. 
    Ribeiro D, Borst JW, Goldbach R, Kormelink R 2009. Tomato spotted wilt virus nucleocapsid protein interacts with both viral glycoproteins Gn and Gc in planta. Virology 383:121–30
    [Google Scholar]
  108. 108. 
    Ribeiro D, Foresti O, Denecke J, Wellink J, Goldbach R, Kormelink RJM 2008. Tomato spotted wilt virus glycoproteins induce the formation of endoplasmic reticulum- and Golgi-derived pleomorphic membrane structures in plant cells. J. Gen. Virol. 89:1811–18
    [Google Scholar]
  109. 109. 
    Ribeiro D, Goldbach R, Kormelink R 2009. Requirements for ER-arrest and sequential exit to the Golgi of Tomato spotted wilt virus glycoproteins. Traffic 10:664–72
    [Google Scholar]
  110. 110. 
    Ribeiro D, Jung M, Moling S, Borst JW, Goldbach R, Kormelink R 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]
  111. 111. 
    Rotenberg D, Jacobson AL, Schneweis DJ, Whiffleld AE 2015. Thrips transmission of tospoviruses. Curr. Opin. Virol. 15:80–89
    [Google Scholar]
  112. 112. 
    Sanfaçon H. 2015. Plant translation factors and virus resistance. Viruses 7:3392–419
    [Google Scholar]
  113. 113. 
    Schnettler E, Hemmes H, Huismann R, Goldbach R, Prins M, Kormelink R 2010. Diverging affinity of tospovirus RNA silencing suppressor proteins, NSs, for various RNA duplex molecules. J. Virol. 84:11542–54
    [Google Scholar]
  114. 114. 
    Scholthof KBG, Adkins S, Czosnek H, Palukaitis P, Jacquot E et al. 2011. Top 10 plant viruses in molecular plant pathology. Mol. Plant Pathol. 12:938–54
    [Google Scholar]
  115. 115. 
    Shen Y, Zhao XH, Yao M, Li C, Miriam K et al. 2014. A versatile complementation assay for cell-to-cell and long distance movements by cucumber mosaic virus based agro-infiltration. Virus Res 190:25–33
    [Google Scholar]
  116. 116. 
    Shimatani Z, Kashojiya S, Takayama M, Terada R, Arazoe T et al. 2017. Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat. Biotechnol. 35:441–43
    [Google Scholar]
  117. 117. 
    Soellick TR, Uhrig JF, Bucher GL, Kellmann JW, Schreier PH 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]
  118. 118. 
    Sonoda S, Tsumuki H. 2004. Analysis of RNA-mediated virus resistance by NSs and NSm gene sequences from Tomato spotted wilt virus. Plant Sci 166:771–78
    [Google Scholar]
  119. 119. 
    Spassova MI, Prins TW, Folkertsma RT, Klein-Lankhorst RM, Hille J 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]
  120. 120. 
    Stefano G, Hawes C, Brandizzi F 2014. ER: the key to the highway. Curr. Opin. Plant Biol. 22:30–38
    [Google Scholar]
  121. 121. 
    Stefano G, Renna L, Chatre L, Hanton SL, Moreau P et al. 2006. In tobacco leaf epidermal cells, the integrity of protein export from the endoplasmic reticulum and of ER export sites depends on active COPI machinery. Plant J 46:95–110
    [Google Scholar]
  122. 122. 
    Storms MMH, Kormelink R, Peters D, van Lent JWM, Goldbach RW 1995. The nonstructural NSm protein of tomato spotted wilt virus induces tubular structures in plant and insect cells. Virology 214:485–93
    [Google Scholar]
  123. 123. 
    Storms MMH, van der Schoot C, Prins M, Kormelink R, van Lent JWM, Goldbach RW 1998. A comparison of two methods of microinjection for assessing altered plasmodesmal gating in tissues expressing viral movement proteins. Plant J 13:131–40
    [Google Scholar]
  124. 124. 
    Takeda A, Sugiyama K, Nagano H, Mori M, Kaido M et al. 2002. Identification of a novel RNA silencing suppressor. NSs protein of Tomato spotted wilt virus. FEBS Lett. 532:75–79
    [Google Scholar]
  125. 125. 
    Takken FLW, Tameling WIL. 2009. To nibble at plant resistance proteins. Science 324:744–46
    [Google Scholar]
  126. 126. 
    Tomato Gene Consort 2012. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–41
    [Google Scholar]
  127. 127. 
    Truniger V, Aranda MA. 2009. Recessive resistance to plant viruses. Adv. Virus Res. 75:119–59
    [Google Scholar]
  128. 128. 
    Turina M, Kormelink R, Resende RO 2016. Resistance to tospoviruses in vegetable crops: epidemiological and molecular aspects. Annu. Rev. Phytopathol. 54:347–71
    [Google Scholar]
  129. 129. 
    van der Vossen EAG, Gros J, Sikkema A, Muskens M, Wouters D et al. 2005. The Rpi-blb2 gene from Solanum bulbocastanum is an Mi-1 gene homolog conferring broad-spectrum late blight resistance in potato. Plant J 44:208–22
    [Google Scholar]
  130. 130. 
    van der Vossen EAG, van der Voort JNAMR, Kanyuka K, Bendahmane A, Sandbrink H et al. 2000. Homologues of a single resistance-gene cluster in potato confer resistance to distinct pathogens: a virus and a nematode. Plant J 23:567–76
    [Google Scholar]
  131. 131. 
    van Knippenberg I, Goldbach R, Kormelink R 2002. Purified Tomato spotted wilt virus particles support both genome replication and transcription in vitro. Virology 303:278–86
    [Google Scholar]
  132. 132. 
    van Knippenberg I, Goldbach R, Kormelink R 2004. In vitro transcription of Tomato spotted wilt virus is independent of translation. J. Gen. Virol. 85:1335–38
    [Google Scholar]
  133. 133. 
    van Knippenberg I, Lamine M, Goldbach R, Kormelink R 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]
  134. 134. 
    van Ooijen G, Mayr G, Kasiem MMA, Albrecht M, Cornelissen BJC, Takken FLW 2008. Structure-function analysis of the NB-ARC domain of plant disease resistance proteins. J. Exp. Bot. 59:1383–97
    [Google Scholar]
  135. 135. 
    van Poelwijk F, Kolkman J, Goldbach R 1996. Sequence analysis of the 5′ ends of tomato spotted wilt virus N mRNAs. Arch. Virol. 141:177–84
    [Google Scholar]
  136. 136. 
    Voeltz GK, Prinz WA, Shibata Y, Rist JM, Rapoport TA 2006. A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124:573–86
    [Google Scholar]
  137. 137. 
    Vos P, Simons G, Jesse T, Wijbrandi J, Heinen L et al. 1998. The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nat. Biotechnol. 16:1365–69
    [Google Scholar]
  138. 138. 
    Vossen JH, van Arkel G, Bergervoet M, Jo KR, Jacobsen E, Visser RG 2016. The Solanum demissum R8 late blight resistance gene is an Sw-5 homologue that has been deployed worldwide in late blight resistant varieties. Theor. Appl. Genet. 129:1785–96
    [Google Scholar]
  139. 139. 
    Whitfield AE, Ullman DE, German TL 2005. Tospovirus–thrips interactions. Annu. Rev. Phytopathol. 43:459–89
    [Google Scholar]
  140. 140. 
    Williams LV, López Lambertini PM, Shohara K, Biderbost EB 2001. Occurrence and geographical distribution of Tospovirus species infecting tomato crops in Argentina. Plant Dis 85:1227–29
    [Google Scholar]
  141. 141. 
    Williams SJ, Sornaraj P, deCourcy-Ireland E, Menz RI, Kobe B et al. 2011. An autoactive mutant of the M flax rust resistance protein has a preference for binding ATP, whereas wild-type M protein binds ADP. Mol. Plant-Microbe Interact. 24:897–906
    [Google Scholar]
  142. 142. 
    Yang CF, Chen KC, Cheng YH, Raja JAJ, Huang YL et al. 2014. Generation of marker-free transgenic plants concurrently resistant to a DNA geminivirus and a RNA tospovirus. Sci. Rep. 4:5717
    [Google Scholar]
  143. 143. 
    Yao M, Zhang T, Zhou T, Zhou Y, Zhou X, Tao X 2012. Repetitive prime-and-realign mechanism converts short capped RNA leaders into longer ones that may be more suitable for elongation during rice stripe virus transcription initiation. J. Gen. Virol. 93:194–202
    [Google Scholar]
  144. 144. 
    Yazhisai U, Rajagopalan PA, Raja JAJ, Chen TC, Yeh SD 2015. Untranslatable tospoviral NSs fragment coupled with L conserved region enhances transgenic resistance against the homologous virus and a serologically unrelated tospovirus. Transgenic Res 24:635–49
    [Google Scholar]
  145. 145. 
    Yin K, Gao C, Qiu JL 2017. Progress and prospects in plant genome editing. Nat. Plants 3:17107
    [Google Scholar]
  146. 146. 
    Yuan P, Bartlam M, Lou Z, Chen S, Zhou J et al. 2009. Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site. Nature 458:909–13
    [Google Scholar]
  147. 147. 
    Zhang H, Zhang JS, Lang ZB, Botella JR, Zhu JK 2017. Genome editing: principles and applications for functional genomics research and crop improvement. Crit. Rev. Plant. Sci. 36:291–309
    [Google Scholar]
  148. 148. 
    Zhao WY, Jiang L, Feng ZK, Chen XJ, Huang Y et al. 2016. Plasmodesmata targeting and intercellular trafficking of Tomato spotted wilt tospovirus movement protein NSm is independent of its function in HR induction. J. Gen. Virol. 97:1990–97
    [Google Scholar]
  149. 149. 
    Zhu M, Jiang L, Bai B, Zhao W, Chen X et al. 2017. The intracellular immune receptor Sw-5b confers broad-spectrum resistance to tospoviruses through recognition of a conserved 21-amino acid viral effector epitope. Plant Cell 29:2214–32
    [Google Scholar]
  150. 150. 
    Zipfel C. 2014. Plant pattern-recognition receptors. Trends Immunol 35:345–51
    [Google Scholar]
/content/journals/10.1146/annurev-phyto-082718-100309
Loading
/content/journals/10.1146/annurev-phyto-082718-100309
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error