1932

Abstract

Plant viruses of the genus cause significant economic losses in various crops. The emergence of new tobamoviruses such as the tomato brown rugose fruit virus (ToBRFV) poses a major threat to global agriculture. Upon infection, plants mount a complex immune response to restrict virus replication and spread, involving a multilayered defense system that includes defense hormones, RNA silencing, and immune receptors. To counter these defenses, tobamoviruses have evolved various strategies to evade or suppress the different immune pathways. Understanding the interactions between tobamoviruses and the plant immune pathways is crucial for the development of effective control measures and genetic resistance to these viruses. In this review, we discuss past and current knowledge of the intricate relationship between tobamoviruses and host immunity. We use this knowledge to understand the emergence of ToBRFV and discuss potential approaches for the development of new resistance strategies to cope with emerging tobamoviruses.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-111821-122847
2023-09-29
2024-12-12
Loading full text...

Full text loading...

/deliver/fulltext/virology/10/1/annurev-virology-111821-122847.html?itemId=/content/journals/10.1146/annurev-virology-111821-122847&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    ICTV 2021. Virus Taxonomy: 2021 Release London, UK: Int. Comm. Taxon. Viruses https://ictv.global/taxonomy
    [Google Scholar]
  2. 2.
    Broadbent L. 1976. Epidemiology and control of Tomato mosaic virus. Annu. Rev. Phytopathol. 14:75–96
    [Google Scholar]
  3. 3.
    Zhang S, Griffiths JS, Marchand G, Bernards MA, Wang A. 2022. Tomato brown rugose fruit virus: an emerging and rapidly spreading plant RNA virus that threatens tomato production worldwide. Mol. Plant Pathol. 23:91262–77
    [Google Scholar]
  4. 4.
    Dombrovsky A, Tran-Nguyen LTT, Jones RAC. 2017. Cucumber green mottle mosaic virus: rapidly increasing global distribution, etiology, epidemiology, and management. Annu. Rev. Phytopathol. 55:231–56
    [Google Scholar]
  5. 5.
    Creager ANH, Scholthof KBG, Citovsky V, Scholthof HB. 1999. Tobacco mosaic virus: pioneering research for a century. Plant Cell 11:3301–8
    [Google Scholar]
  6. 6.
    Beijerinck MW. 1898. Ueber ein Contagium vivum fluidum als Ursache der Fleckenkrankheit der Tabaksblätter. verh. K. Akad. Wet. Amsterdam 65:3–21
    [Google Scholar]
  7. 7.
    Stanley WM. 1935. Isolation of a crystalline protein possessing the properties of tobacco-mosaic virus. Science 81:2113644–45
    [Google Scholar]
  8. 8.
    Gierer A, Schramm G. 1956. Infectivity of ribonucleic acid from tobacco mosaic virus. Nature 177:4511702–3
    [Google Scholar]
  9. 9.
    Fraenkel-Conrat H. 1956. The role of the nucleic acid in the reconstitution of active tobacco mosaic virus. J. Am. Chem. Soc. 78:4882–83
    [Google Scholar]
  10. 10.
    Reagan BC, Burch-Smith TM. 2020. Viruses reveal the secrets of plasmodesmal cell biology. Mol. Plant-Microbe Interact. 33:126–39
    [Google Scholar]
  11. 11.
    Goelet P, Lomonossoff GP, Butler PJG, Akam ME, Gait MJ, Karn J. 1982. Nucleotide sequence of tobacco mosaic virus RNA. PNAS 79:195818–22
    [Google Scholar]
  12. 12.
    Ishibashi K, Ishikawa M. 2016. Replication of tobamovirus RNA. Annu. Rev. Phytopathol. 54:55–78
    [Google Scholar]
  13. 13.
    Atkins D, Hull R, Wells B, Roberts K, Moore P, Beachy RN. 1991. The tobacco mosaic virus 30K movement protein in transgenic tobacco plants is localized to plasmodesmata. J. Gen. Virol. 72:1209–11
    [Google Scholar]
  14. 14.
    Citovsky V, Knorr D, Schuster G, Zambryski P. 1990. The P30 movement protein of tobacco mosaic virus is a single-strand nucleic acid binding protein. Cell 60:4637–47
    [Google Scholar]
  15. 15.
    Wolf S, Deom CM, Beachy RN, Lucas WJ. 1989. Movement protein of tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science 246:4928377–79
    [Google Scholar]
  16. 16.
    Klug A. 1999. The tobacco mosaic virus particle: structure and assembly. Philos. Trans. R Soc. B 354: 1383.531–35
    [Google Scholar]
  17. 17.
    Hilf ME, Dawson WO. 1993. The tobamovirus capsid protein functions as a host-specific determinant of long-distance movement. Virology 193:1106–14
    [Google Scholar]
  18. 18.
    Heinlein M. 2015. Plant virus replication and movement. Virology 479:657–71
    [Google Scholar]
  19. 19.
    Baulcombe DC. 2022. The role of viruses in identifying and analyzing RNA silencing. Annu. Rev. Virol. 9:353–73
    [Google Scholar]
  20. 20.
    Lopez-Gomollon S, Baulcombe DC. 2022. Roles of RNA silencing in viral and non-viral plant immunity and in the crosstalk between disease resistance systems. Nat. Rev. Mol. Cell Biol. 23:10645–62
    [Google Scholar]
  21. 21.
    Csorba T, Kontra L, Burgyán J. 2015. Viral silencing suppressors: tools forged to fine-tune host-pathogen coexistence. Virology 479:85–103
    [Google Scholar]
  22. 22.
    Ding XS, Liu J, Cheng NH, Folimonov A, Hou YM et al. 2004. The Tobacco mosaic virus 126-kDa protein associated with virus replication and movement suppresses RNA silencing. Mol. Plant-Microbe Interact. 17:6583–92
    [Google Scholar]
  23. 23.
    Kubota K, Tsuda S, Tamai A, Meshi T. 2003. Tomato mosaic virus replication protein suppresses virus-targeted posttranscriptional gene silencing. J. Virol. 77:2011016–26
    [Google Scholar]
  24. 24.
    Vogler H, Akbergenov R, Shivaprasad PV, Dang V, Fasler M et al. 2007. Modification of small RNAs associated with suppression of RNA silencing by tobamovirus replicase protein. J. Virol. 81:1910379–88
    [Google Scholar]
  25. 25.
    Csorba T, Bovi A, Dalmay T, Burgyán J. 2007. The p122 subunit of Tobacco mosaic virus replicase is a potent silencing suppressor and compromises both small interfering RNA- and microRNA-mediated pathways. J. Virol. 81:2111768–80
    [Google Scholar]
  26. 26.
    Wang LY, Lin SS, Hung TH, Li TK, Lin NC, Shen TL. 2012. Multiple domains of the tobacco mosaic virus p126 protein can independently suppress local and systemic RNA silencing. Mol. Plant-Microbe Interact. 25:5648–57
    [Google Scholar]
  27. 27.
    Várallyay É, Havelda Z. 2013. Unrelated viral suppressors of RNA silencing mediate the control of ARGONAUTE1 level. Mol. Plant Pathol. 14:6567–75
    [Google Scholar]
  28. 28.
    Vogler H, Kwon MO, Dang V, Sambade A, Fasler M et al. 2008. Tobacco mosaic virus movement protein enhances the spread of RNA silencing. PLOS Pathog 4:4e1000038
    [Google Scholar]
  29. 29.
    Schoenberg DR, Maquat LE. 2012. Regulation of cytoplasmic mRNA decay. Nat. Rev. Genet. 13:246–59
    [Google Scholar]
  30. 30.
    Liu L, Chen X. 2016. RNA quality control as a key to suppressing RNA silencing of endogenous genes in plants. Mol. Plant 9:6826–36
    [Google Scholar]
  31. 31.
    Conti G, Zavallo D, Venturuzzi AL, Rodriguez MC, Crespi M, Asurmendi S. 2017. TMV induces RNA decay pathways to modulate gene silencing and disease symptoms. Plant J 89:173–84
    [Google Scholar]
  32. 32.
    Peng Y, Yang J, Li X, Zhang Y. 2021. Salicylic acid: biosynthesis and signaling. Annu. Rev. Plant Biol. 72:761–91
    [Google Scholar]
  33. 33.
    Fu ZQ, Dong X. 2013. Systemic acquired resistance: turning local infection into global defense. Annu. Rev. Plant Biol. 64:839–63
    [Google Scholar]
  34. 34.
    White RF. 1979. Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology 99:2410–12
    [Google Scholar]
  35. 35.
    Malamy J, Carr JP, Klessig DF, Raskin I. 1990. Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250:49831002–4
    [Google Scholar]
  36. 36.
    Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G et al. 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:5122754–56
    [Google Scholar]
  37. 37.
    Chivasa S, Murphy AM, Naylor M, Carr JP. 1997. Salicylic acid interferes with tobacco mosaic virus replication via a novel salicylhydroxamic acid-sensitive mechanism. Plant Cell 9:4547–57
    [Google Scholar]
  38. 38.
    Murphy AM, Carr JP. 2002. Salicylic acid has cell-specific effects on tobacco mosaic virus replication and cell-to-cell movement. Plant Physiol 128:2552–63
    [Google Scholar]
  39. 39.
    Xie Z, Fan B, Chen C, Chen Z. 2001. An important role of an inducible RNA-dependent RNA polymerase in plant antiviral defense. PNAS 98:116516–21
    [Google Scholar]
  40. 40.
    Lee WS, Fu SF, Li Z, Murphy AM, Dobson EA et al. 2016. Salicylic acid treatment and expression of an RNA-dependent RNA polymerase 1 transgene inhibit lethal symptoms and meristem invasion during tobacco mosaic virus infection in Nicotiana benthamiana. BMC Plant Biol 16:11–14
    [Google Scholar]
  41. 41.
    Amsbury S, Kirk P, Benitez-Alfonso Y. 2018. Emerging models on the regulation of intercellular transport by plasmodesmata-associated callose. J. Exp. Bot. 69:1105–15
    [Google Scholar]
  42. 42.
    Wang X, Sager R, Cui W, Zhang C, Lu H, Lee JY. 2013. Salicylic acid regulates plasmodesmata closure during innate immune responses in Arabidopsis. Plant Cell 25:62315–29
    [Google Scholar]
  43. 43.
    Cui W, Lee JY. 2016. Arabidopsis callose synthases CalS1/8 regulate plasmodesmal permeability during stress. Nat. Plants 2:51–9
    [Google Scholar]
  44. 44.
    Lee JY, Wang X, Cui W, Sager R, Modla S et al. 2011. A plasmodesmata-localized protein mediates crosstalk between cell-to-cell communication and innate immunity in Arabidopsis. Plant Cell 23:93353–73
    [Google Scholar]
  45. 45.
    Guenoune-Gelbart D, Elbaum M, Sagi G, Levy A, Epel BL. 2008. Tobacco mosaic virus (TMV) replicase and movement protein function synergistically in facilitating TMV spread by lateral diffusion in the plasmodesmal desmotubule of Nicotiana benthamiana. Mol. Plant-Microbe Interact. 21:3335–45
    [Google Scholar]
  46. 46.
    Huang C, Sede AR, Elvira-González L, Yan Y, Rodriguez M et al. 2022. dsRNA-induced immunity targets plasmodesmata and is suppressed by viral movement proteins. bioRxiv 2022.11.21.517408. https://doi.org/10.1101/2022.11.21.517408
  47. 47.
    Conti G, Rodriguez MC, Manacorda CA, Asurmendi S. 2012. Transgenic expression of tobacco mosaic virus capsid and movement proteins modulate plant basal defense and biotic stress responses in Nicotiana tabacum. Mol. Plant-Microbe Interact. 25:101370–84
    [Google Scholar]
  48. 48.
    Venturuzzi AL, Rodriguez MC, Conti G, Leone M, Caro MDP et al. 2021. Negative modulation of SA signaling components by the capsid protein of tobacco mosaic virus is required for viral long-distance movement. Plant J 106:4896–912
    [Google Scholar]
  49. 49.
    Padmanabhan MS, Goregaoker SP, Golem S, Shiferaw H, Culver JN. 2005. Interaction of the tobacco mosaic virus replicase protein with the Aux/IAA protein PAP1/IAA26 is associated with disease development. J. Virol. 79:42549–58
    [Google Scholar]
  50. 50.
    Padmanabhan MS, Shiferaw H, Culver JN. 2006. The Tobacco mosaic virus replicase protein disrupts the localization and function of interacting Aux/IAA proteins. Mol. Plant-Microbe Interact. 19:8864–73
    [Google Scholar]
  51. 51.
    Collum TD, Padmanabhan MS, Hsieh YC, Culver JN. 2016. Tobacco mosaic virus-directed reprogramming of auxin/indole acetic acid protein transcriptional responses enhances virus phloem loading. PNAS 113:192740–49
    [Google Scholar]
  52. 52.
    Couto D, Zipfel C. 2016. Regulation of pattern recognition receptor signalling in plants. Nat. Rev. Immunol. 16:9537–52
    [Google Scholar]
  53. 53.
    Heese A, Hann DR, Gimenez-Ibanez S, Jones AME, He K et al. 2007. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. PNAS 104:2912217–22
    [Google Scholar]
  54. 54.
    Kørner JC, Klauser D, Niehl A, Domínguez-Ferreras A, Chinchilla D et al. 2013. The immunity regulator BAK1 contributes to resistance against diverse RNA viruses. Mol. Plant-Microbe Interact. 26:111271–80
    [Google Scholar]
  55. 55.
    Niehl A, Wyrsch I, Boller T, Heinlein M. 2016. Double-stranded RNAs induce a pattern-triggered immune signaling pathway in plants. New Phytol 211:31008–19
    [Google Scholar]
  56. 56.
    Toruño TY, Stergiopoulos I, Coaker G. 2016. Plant-pathogen effectors: cellular probes interfering with plant defenses in spatial and temporal manners. Annu. Rev. Phytopathol. 54:419–41
    [Google Scholar]
  57. 57.
    Caplan J, Padmanabhan M, Dinesh-Kumar SP. 2008. Plant NB-LRR immune receptors: from recognition to transcriptional reprogramming. Cell Host Microbe 3:3126–35
    [Google Scholar]
  58. 58.
    Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:7117323–29
    [Google Scholar]
  59. 59.
    Holmes FO. 1934. Inheritance of ability to localize tobacco-mosaic virus. Phytopathology 24:984–1002
    [Google Scholar]
  60. 60.
    Holmes FO. 1938. Inheritance of resistance to tobacco-mosaic disease in tobacco. Phytopathology 28:553–61
    [Google Scholar]
  61. 61.
    Dinesh-Kumar SP, Whitham S, Choi D, Hehl R, Corr C, Baker B. 1995. Transposon tagging of tobacco mosaic virus resistance gene N: its possible role in the TMV-N-mediated signal transduction pathway. PNAS 92:104175–80
    [Google Scholar]
  62. 62.
    Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B. 1994. The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78:61101–15
    [Google Scholar]
  63. 63.
    O'Neill LAJ, Golenbock D, Bowie AG. 2013. The history of Toll-like receptors-redefining innate immunity. Nat. Rev. Immunol. 13:6453–60
    [Google Scholar]
  64. 64.
    Tóbiás I, Rast ATB, Maat DZ. 1982. Tobamoviruses of pepper, eggplant and tobacco: comparative host reactions and serological relationships. Neth. J. Plant Pathol. 88:6257–68
    [Google Scholar]
  65. 65.
    Dinesh-Kumar SP, Baker BJ. 2000. Alternatively spliced N resistance gene transcripts: their possible role in tobacco mosaic virus resistance. PNAS 97:41908–13
    [Google Scholar]
  66. 66.
    Dinesh-Kumar SP, Tham WH, Baker BJ. 2000. Structure–function analysis of the tobacco mosaic virus resistance gene N. PNAS 97:2614789–94
    [Google Scholar]
  67. 67.
    Padgett HS, Watanabe Y, Beachy RN. 1997. Identification of the TMV replicase sequence that activates the N gene-mediated hypersensitive response. Mol. Plant-Microbe Interact. 10:6709–15
    [Google Scholar]
  68. 68.
    Abbink TEM, Tjernberg PA, Bol JF, Linthorst HJM. 1998. Tobacco mosaic virus helicase domain induces necrosis in N gene-carrying tobacco in the absence of virus replication. Mol. Plant-Microbe Interact. 11:12709–15
    [Google Scholar]
  69. 69.
    Erickson FL, Holzberg S, Calderon-Urrea A, Handley V, Axtell M et al. 1999. The helicase domain of the TMV replicase proteins induces the N-mediated defence response in tobacco. Plant J 18:167–75
    [Google Scholar]
  70. 70.
    Padmanabhan MS, Ma S, Burch-Smith TM, Czymmek K, Huijser P, Dinesh-Kumar SP. 2013. Novel positive regulatory role for the SPL6 transcription factor in the N TIR-NB-LRR receptor-mediated plant innate immunity. PLOS Pathog 9:3e1003235
    [Google Scholar]
  71. 71.
    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. 61:131–45
    [Google Scholar]
  72. 72.
    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 132:3449–62
    [Google Scholar]
  73. 73.
    Padmanabhan MS, Dinesh-Kumar SP. 2010. All hands on deck—the role of chloroplasts, endoplasmic reticulum, and the nucleus in driving plant innate immunity. Mol. Plant-Microbe Interact. 23:111368–80
    [Google Scholar]
  74. 74.
    Caplan JL, Kumar AS, Park E, Padmanabhan MS, Hoban K et al. 2015. Chloroplast stromules function during innate immunity. Dev. Cell 34:145–57
    [Google Scholar]
  75. 75.
    Kumar AS, Park E, Nedo A, Alqarni A, Ren L et al. 2018. Stromule extension along microtubules coordinated with actin-mediated anchoring guides perinuclear chloroplast movement during innate immunity. eLife 7:e23625
    [Google Scholar]
  76. 76.
    Kourelis J, Adachi H. 2022. Activation and regulation of NLR immune receptor networks. Plant Cell Physiol 63:101366–77
    [Google Scholar]
  77. 77.
    Peart JR, Mestre P, Lu R, Malcuit I, Baulcombe DC. 2005. NRG1, a CC-NB-LRR protein, together with N, a TIR-NB-LRR protein, mediates resistance against tobacco mosaic virus. Curr. Biol. 15:10968–73
    [Google Scholar]
  78. 78.
    Peart JR, Cook G, Feys BJ, Parker JE, Baulcombe DC. 2002. An EDS1 orthologue is required for N-mediated resistance against tobacco mosaic virus. Plant J 29:5569–79
    [Google Scholar]
  79. 79.
    Liu Y, Schiff M, Marathe R, Dinesh-Kumar SP. 2002. Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J 30:4415–29
    [Google Scholar]
  80. 80.
    Liu Y, Burch-Smith T, Schiff M, Feng S, Dinesh-Kumar SP. 2004. Molecular chaperone Hsp90 associates with resistance protein N and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants. J. Biol. Chem. 279:32101–8
    [Google Scholar]
  81. 81.
    Mestre P, Baulcombe DC. 2006. Elicitor-mediated oligomerization of the tobacco N disease resistance protein. Plant Cell 18:2491–501
    [Google Scholar]
  82. 82.
    Zhang Y, Song G, Lal NK, Nagalakshmi U, Li Y et al. 2019. TurboID-based proximity labeling reveals that UBR7 is a regulator of N NLR immune receptor-mediated immunity. Nat. Commun. 10:3252
    [Google Scholar]
  83. 83.
    Burch-Smith TM, Schiff M, Caplan JL, Tsao J, Czymmek K, Dinesh-Kumar SP. 2007. A novel role for the TIR domain in association with pathogen-derived elicitors. PLOS Biol 5:3e68
    [Google Scholar]
  84. 84.
    Zhang D, Gao Z, Zhang H, Yang Y, Yang X et al. 2022. The MAPK-ALFIN-LIKE 7 module negatively regulates ROS scavenging genes to promote NLR-mediated immunity. PNAS 120:3e2214750120
    [Google Scholar]
  85. 85.
    Boukema IEW. 1980. Allelism of genes controlling tobamovirus resistance in Capsicum L. Euphytica 29:433–39
    [Google Scholar]
  86. 86.
    Tomita R, Sekine KT, Mizumoto H, Sakamoto M, Murai J et al. 2011. Genetic basis for the hierarchical interaction between Tobamovirus spp. and L resistance gene alleles from different pepper species. Mol. Plant-Microbe Interact. 24:1108–17
    [Google Scholar]
  87. 87.
    Mizumoto H, Nakamura I, Shimomoto Y, Sawada H, Tomita R et al. 2012. Amino acids in tobamovirus coat protein controlling pepper L1a gene-mediated resistance. Mol. Plant Pathol. 13:8915–22
    [Google Scholar]
  88. 88.
    Sekine KT, Tomita R, Takeuchi S, Atsumi G, Saitoh H et al. 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. 25:91219–29
    [Google Scholar]
  89. 89.
    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 L4 gene-mediated resistance in Capsicum spp. Phytopathology 97:7787–93
    [Google Scholar]
  90. 90.
    Antignus Y, Lachman O, Pearlsman M, Maslenin L, Rosner A. 2008. A new pathotype of Pepper mild mottle virus (PMMoV) overcomes the L4 resistance genotype of pepper cultivars. Plant Dis 92:71033–37
    [Google Scholar]
  91. 91.
    Fraile A, Pagán I, Anastasio G, Sáez E, García-Arenal F. 2011. Rapid genetic diversification and high fitness penalties associated with pathogenicity evolution in a plant virus. Mol. Biol. Evol. 28:41425–37
    [Google Scholar]
  92. 92.
    Moreno-Pérez MG, García-Luque I, Fraile A, García-Arenal F. 2016. Mutations that determine resistance breaking in a plant RNA virus have pleiotropic effects on its fitness that depend on the host environment and on the type, single or mixed, of infection. J. Virol. 90:209128–37
    [Google Scholar]
  93. 93.
    Bera S, Moreno-Pérez MG, García-Figuera S, Pagán I, Fraile A et al. 2017. Pleiotropic effects of resistance-breaking mutations on particle stability provide insight into life history evolution of a plant RNA virus. J. Virol. 91:18e00435–17
    [Google Scholar]
  94. 94.
    Moreno-Pérez MG, Bera S, McLeish M, Fraile A, García-Arenal F. 2023. Reversion of a resistance-breaking mutation shows reversion costs and high virus diversity at necrotic local lesions. Mol. Plant Pathol. 24:2142–53
    [Google Scholar]
  95. 95.
    Pelham J. 1966. Resistance in tomato to Tobacco mosaic virus. Euphytica 15:258–67
    [Google Scholar]
  96. 96.
    Meshi T, Motoyoshi F, Adachi A, Watanabe Y, Takamatsu N, Okada Y. 1988. Two concomitant base substitutions in the putative replicase genes of tobacco mosaic virus confer the ability to overcome the effects of a tomato resistance gene, Tm-1. EMBO J 7:61575–81
    [Google Scholar]
  97. 97.
    Strasser M, Pfitzner AJP. 2007. The double-resistance-breaking Tomato mosaic virus strain ToMV1–2 contains two independent single resistance-breaking domains. Arch. Virol. 152:903–14
    [Google Scholar]
  98. 98.
    Motoyoshi F, Oshima N. 1977. Expression of genetically controlled resistance to tobacco mosaic virus infection in isolated tomato leaf mesophyll protoplasts. J. Gen. Virol. 34:3499–506
    [Google Scholar]
  99. 99.
    Yamafuji R, Watanabe Y, Meshi T, Okada Y. 1991. Replication of TMV-L and Lta1 RNAs and their recombinants in TMV-resistant Tm-1 tomato protoplasts. Virology 183:199–105
    [Google Scholar]
  100. 100.
    Fraser RSS, Loughlin SAR. 1980. Resistance to tobacco mosaic virus in tomato: effects of the Tm-1 gene on virus multiplication. J. Gen. Virol. 48:187–96
    [Google Scholar]
  101. 101.
    Ishibashi K, Masuda K, Naito S, Meshi T, Ishikawa M. 2007. An inhibitor of viral RNA replication is encoded by a plant resistance gene. PNAS 104:3413833–38
    [Google Scholar]
  102. 102.
    Ishibashi K, Kezuka Y, Kobayashi C, Kato M, Inoue T et al. 2014. Structural basis for the recognition-evasion arms race between Tomato mosaic virus and the resistance gene Tm-1. PNAS 111:333486–95
    [Google Scholar]
  103. 103.
    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. 87:147933–39
    [Google Scholar]
  104. 104.
    Lanfermeijer FC, Warmink J, Hille J. 2005. The products of the broken Tm-2 and the durable Tm-22 resistance genes from tomato differ in four amino acids. J. Exp. Bot. 56:4212925–33
    [Google Scholar]
  105. 105.
    Hall TJ. 1980. Resistance at the Tm-2 locus in the tomato to Tomato mosaic virus. Euphytica 29:189–97
    [Google Scholar]
  106. 106.
    Weber H, Pfitzner AJ. 1998. Tm-2 resistance in tomato requires recognition of the carboxy terminus of the movement protein of tomato mosaic virus. Mol. Plant-Microbe Interact. 11:6498–503
    [Google Scholar]
  107. 107.
    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-22 resistance gene in the tomato. J. Virol. 67:116432–38
    [Google Scholar]
  108. 108.
    Chen T, Liu D, Niu X, Wang J, Qian L et al. 2017. Antiviral resistance protein Tm-22 functions on the plasma membrane. Plant Physiol 173:42399–410
    [Google Scholar]
  109. 109.
    Hak H, Spiegelman Z. 2021. The tomato brown rugose fruit virus movement protein overcomes Tm-22 resistance in tomato while attenuating viral transport. Mol. Plant-Microbe Interact. 34:91024–32
    [Google Scholar]
  110. 110.
    Yan ZY, Ma HY, Wang L, Tettey C, Zhao MS et al. 2021. Identification of genetic determinants of tomato brown rugose fruit virus that enable infection of plants harbouring the Tm-22 resistance gene. Mol. Plant Pathol. 22:111347–57
    [Google Scholar]
  111. 111.
    Wang J, Chen T, Han M, Qian L, Li J et al. 2020. Plant NLR immune receptor Tm-22 activation requires NB-ARC domain-mediated self-association of CC domain. PLOS Pathog 16:4e1008475
    [Google Scholar]
  112. 112.
    Zhang H, Zhao J, Liu S, Zhang D-P, Liu Y. 2013. Tm-22 confers different resistance responses against Tobacco mosaic virus dependent on its expression level. Mol. Plant 6:3971–74
    [Google Scholar]
  113. 113.
    Qian L, Zhao J, Du Y, Zhao X, Han M, Liu Y. 2018. Hsp90 interacts with Tm-22 and is essential for Tm-22-mediated resistance to Tobacco mosaic virus. Front. Plant Sci. 9:411
    [Google Scholar]
  114. 114.
    Du Y, Zhao J, Chen T, Liu Q, Zhang H et al. 2013. Type I J-domain NbMIP1 proteins are required for both Tobacco mosaic virus infection and plant innate immunity. PLOS Pathog 9:10e1003659
    [Google Scholar]
  115. 115.
    Zhao J, Liu Q, Zhang H, Jia Q, Hong Y, Liu Y. 2012. The rubisco small subunit is involved in tobamovirus movement and Tm-22-mediated extreme resistance. Plant Physiol 161:1374–83
    [Google Scholar]
  116. 116.
    Salem N, Mansour A, Ciuffo M, Falk BW, Turina M. 2016. A new tobamovirus infecting tomato crops in Jordan. Arch. Virol. 161:2503–6
    [Google Scholar]
  117. 117.
    Luria N, Smith E, Reingold V, Bekelman I, Lapidot M et al. 2017. A new Israeli Tobamovirus isolate infects tomato plants harboring Tm-22 resistance genes. PLOS ONE 12:1e0170429
    [Google Scholar]
  118. 118.
    Smith E, Dombrovsky A. 2019. Aspects in tobamovirus management in intensive agriculture. Plant Diseases—Current Threats and Management Trends, ed. Snježana Topolovec-Pintaric31–48. London: IntechOpen
    [Google Scholar]
  119. 119.
    Oladokun JO, Halabi MH, Barua P, Nath PD. 2019. Tomato brown rugose fruit disease: current distribution, knowledge and future prospects. Plant Pathol 68:91579–86
    [Google Scholar]
  120. 120.
    WUSF Public Media 2020. Virus found in Mexican tomatoes worries Florida agriculture officials WUSF 89.7, Oct. 10. https://news.wgcu.org/2019-10-10/virus-found-in-mexican-tomatoes-worries-florida-agriculture-officials
    [Google Scholar]
  121. 121.
    Maayan Y, Pandaranayaka EPJ, Srivastava DA, Lapidot M, Levin I et al. 2018. Using genomic analysis to identify tomato Tm-2 resistance-breaking mutations and their underlying evolutionary path in a new and emerging tobamovirus. Arch. Virol. 163:1863–75
    [Google Scholar]
  122. 122.
    Matzrafi M, Abu-Nassar J, Klap C, Shtarkman M, Smith E, Dombrovsky A. 2023. Solanum elaeagnifolium and S. rostratum as potential hosts of the tomato brown rugose fruit virus. PLOS ONE 18:3e0282441
    [Google Scholar]
  123. 123.
    Salem NM, Abumuslem M, Turina M, Samarah N, Sulaiman A et al. 2022. New weed hosts for tomato brown rugose fruit virus in wild Mediterranean vegetation. Plants 11:172287
    [Google Scholar]
  124. 124.
    Hak H, Raanan H, Schwarz S, Sherman Y, Dinesh-Kumar SP, Spiegelman Z. 2023. Activation of Tm-22 resistance is mediated by a conserved cysteine essential for tobacco mosaic virus movement. Mol. Plant Pathol In press. https://doi.org/10.1111/mpp.13318
    [Google Scholar]
  125. 125.
    Eldan O, Ofir A, Luria N, Klap C, Lachman O et al. 2022. Pepper plants harboring L resistance alleles showed tolerance toward manifestations of tomato brown rugose fruit virus disease. Plants 11:182378
    [Google Scholar]
  126. 126.
    Fidan H, Sarikaya P, Yildiz K, Topkaya B, Erkis G, Calis O. 2021. Robust molecular detection of the new Tomato brown rugose fruit virus in infected tomato and pepper plants from Turkey. J. Integr. Agric. 20:82170–79
    [Google Scholar]
  127. 127.
    Pelletier A, Moffett P. 2022. N and N′-mediated recognition confers resistance to tomato brown rugose fruit virus. MicroPubl. Biol. https://micropublication.org/static/pdf/micropub-biology-000660.pdf
    [Google Scholar]
  128. 128.
    Jewehan A, Kiemo FW, Salem N, Tóth Z, Salamon P, Szabó Z. 2022. Isolation and molecular characterization of a tomato brown rugose fruit virus mutant breaking the tobamovirus resistance found in wild Solanum species. Arch. Virol. 167:71559–63
    [Google Scholar]
  129. 129.
    Zinger A, Lapidot M, Harel A, Doron-Faigenboim A, Gelbart D, Levin I. 2021. Identification and mapping of tomato genome loci controlling tolerance and resistance to tomato brown rugose fruit virus. Plants 10:1179
    [Google Scholar]
  130. 130.
    Ishikawa M, Naito S, Ohnot T. 1993. Effects of the tom1 mutation of Arabidopsis thaliana on the multiplication of Tobacco mosaic virus RNA in protoplasts. J. Virol. 67:95328–38
    [Google Scholar]
  131. 131.
    Tsujimoto Y, Numaga T, Ohshima K, Yano MA, Ohsawa R et al. 2003. Arabidopsis TOBAMOVIRUS MULTIPLICATION (TOM) 2 locus encodes a transmembrane protein that interacts with TOM1. EMBO J 22:2335–43
    [Google Scholar]
  132. 132.
    Yamanaka T, Ohta T, Takahashi M, Meshi T, Schmidt R et al. 2000. TOM1, an Arabidopsis gene required for efficient multiplication of a tobamovirus, encodes a putative transmembrane protein. PNAS 97:1810107–12
    [Google Scholar]
  133. 133.
    Ali ME, Ishii Y, Taniguchi J, Waliullah S, Kobayashi K et al. 2018. Conferring virus resistance in tomato by independent RNA silencing of three tomato homologs of Arabidopsis TOM1. Arch. Virol. 163:51357–62
    [Google Scholar]
  134. 134.
    Yamanaka T, Imai T, Satoh R, Kawashima A, Takahashi M et al. 2002. Complete inhibition of Tobamovirus multiplication by simultaneous mutations in two homologous host genes. J. Virol. 76:52491–97
    [Google Scholar]
  135. 135.
    Asano M, Satoh R, Mochizuki A, Tsuda S, Yamanaka T et al. 2005. Tobamovirus-resistant tobacco generated by RNA interference directed against host genes. FEBS Lett 579:204479–84
    [Google Scholar]
  136. 136.
    Ishikawa M, Yoshida T, Matsuyama M, Kouzai Y, Kano A, Ishibashi K. 2022. Tomato brown rugose fruit virus resistance generated by quadruple knockout of homologs of TOBAMOVIRUS MULTIPLICATION1 in tomato. Plant Physiol 189:2679–86
    [Google Scholar]
  137. 137.
    Kravchik M, Shnaider Y, Abebie B, Shtarkman M, Kumari R et al. 2022. Knockout of SlTOM1 and SlTOM3 results in differential resistance to tobamovirus in tomato. Mol. Plant Pathol. 23:91278–89
    [Google Scholar]
  138. 138.
    Powell PA, Stark DM, Sanders PR, Beachy RN. 1989. Protection against tobacco mosaic virus in transgenic plants that express tobacco mosaic virus antisense RNA. PNAS 86:186949–52
    [Google Scholar]
  139. 139.
    Abel PP, Nelson RS, De B, Hoffmann N, Rogers SG et al. 1986. Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science 232:4751738–43
    [Google Scholar]
  140. 140.
    Wilson C. 2022. A purple patch for GM food. New Sci 256:340851
    [Google Scholar]
  141. 141.
    Konakalla NC, Kaldis A, Berbati M, Masarapu H, Voloudakis AE. 2016. Exogenous application of double-stranded RNA molecules from TMV p126 and CP genes confers resistance against TMV in tobacco. Planta 244:4961–69
    [Google Scholar]
  142. 142.
    Marchal C, Pai H, Kamoun S, Kourelis J. 2022. Emerging principles in the design of bioengineered made-to-order plant immune receptors. Curr. Opin. Plant Biol. 70:102311
    [Google Scholar]
/content/journals/10.1146/annurev-virology-111821-122847
Loading
/content/journals/10.1146/annurev-virology-111821-122847
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