1932

Abstract

Tomato brown rugose fruit virus (ToBRFV) is an emerging tobamovirus. It was first reported in 2015 in Jordan in greenhouse tomatoes and now threatens tomato and pepper crops around the world. ToBRFV is a stable and highly infectious virus that is easily transmitted by mechanical means and via seeds, which enables it to spread locally and over long distances. The ability of ToBRFV to infect tomato plants harboring the commonly deployed resistance genes, as well as pepper plants harboring the resistance alleles under certain conditions, limits the ability to prevent damage from the virus. The fruit production and quality of ToBRFV-infected tomato and pepper plants can be drastically affected, thus significantly impacting their market value. Herein, we review the current information and discuss the latest areas of research on this virus, which include its discovery and distribution, epidemiology, detection, and prevention and control measures, that could help mitigate the ToBRFV disease pandemic.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-021622-120703
2023-09-05
2024-06-14
Loading full text...

Full text loading...

/deliver/fulltext/phyto/61/1/annurev-phyto-021622-120703.html?itemId=/content/journals/10.1146/annurev-phyto-021622-120703&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Abou Kubaa R, Choueiri E, Heinoun K, Cillo F, Saponari M. 2022. First report of tomato brown rugose fruit virus infecting sweet pepper in Syria and Lebanon. J. Plant Pathol. 104:425
    [Google Scholar]
  2. 2.
    Abrahamian P, Cai W, Nunziata SO, Ling K-S, Jaiswal N et al. 2022. Comparative analysis of tomato brown rugose fruit virus isolates shows limited genetic diversity. Viruses 14:122816
    [Google Scholar]
  3. 3.
    Alfaro-Fernández A, Castillo P, Sanahuja E, Rodríguez-Salido MC, Font MI. 2021. First report of tomato brown rugose fruit virus in tomato in Spain. Plant Dis 105:2515
    [Google Scholar]
  4. 4.
    Alkowni R, Alabdallah O, Fadda Z. 2019. Molecular identification of tomato brown rugose fruit virus in tomato in Palestine. J. Plant Pathol. 101:3719–23
    [Google Scholar]
  5. 5.
    Alon DM, Hak H, Bornstein M, Pines G, Spiegelman Z. 2021. Differential detection of the tobamoviruses tomato mosaic virus (ToMV) and tomato brown rugose fruit virus (ToBRFV) using CRISPR-Cas12a. Plants 10:61256
    [Google Scholar]
  6. 6.
    Amer MA, Mahmoud SY 2020. First report of tomato brown rugose fruit virus on tomato in Egypt. New Dis. Rep. 41:124
    [Google Scholar]
  7. 7.
    Ashkenazi V, Rotem Y, Ecker R, Nashilevitz S, Barom N. 2018. Tolerance in plants of Solanum lycopersicum to the tobamovirus tomato brown rugose fruit virus (TBRFV) WO Patent 2018/219941
    [Google Scholar]
  8. 8.
    Ashkenazi V, Rotem Y, Ecker R, Nashilevitz S, Barom N 2020. Resistance in plants of Solanum lycopersicum to the tobamovirus tomato brown rugose fruit virus WO Patent 2020/249798
    [Google Scholar]
  9. 9.
    Avni B, Gelbart D, Sufrin-Ringwald T, Zemach H, Belausov E et al. 2022. ToBRFV infects the reproductive tissues of tomato plants but is not transmitted to the progenies by pollination. Cells 11:182864
    [Google Scholar]
  10. 10.
    Avni B, Gelbart D, Sufrin-Ringwald T, Zinger A, Chen L et al. 2021. Tomato genetic resistance to tobamoviruses is compromised. Acta Hortic 1316:89–98
    [Google Scholar]
  11. 11.
    Bačnik K, Kutnjak D, Pecman A, Mehle N, Žnidarič MT et al. 2020. Viromics and infectivity analysis reveal the release of infective plant viruses from wastewater into the environment. Water Res 177:115628
    [Google Scholar]
  12. 12.
    Batuman O, Yilmaz S, Roberts PD, McAvoy E, Hutton SF et al. 2020. Tomato brown rugose fruit virus (ToBRFV): a potential threat for tomato production in Florida. EDIS 2020:12PP360
    [Google Scholar]
  13. 13.
    Beris D, Malandraki I, Kektsidou O, Theologidis I, Vassilakos N, Varveri C. 2020. First report of tomato brown rugose fruit virus infecting tomato in Greece. Plant Dis 104:72035
    [Google Scholar]
  14. 14.
    Bernabé-Orts JM, Hernando Y, Aranda MA. 2022. Toward a CRISPR-based point-of-care test for tomato brown rugose fruit virus detection. PhytoFrontiers 2:292–100
    [Google Scholar]
  15. 15.
    Bernabé-Orts JM, Torre C, Méndez-López E, Hernando Y, Aranda MA 2021. New resources for the specific and sensitive detection of the emerging tomato brown rugose fruit virus. Viruses 13:91680
    [Google Scholar]
  16. 16.
    Betti L, Marini F, Marani F, Cuffiani M, Rabiti AL, Canova A. 1997. A TMV strain overcoming both Tm-2 and Tm-22 resistance genes in tomato. Phytopathol. Mediterr. 36:124–30
    [Google Scholar]
  17. 17.
    Botermans M, de Koning PPM, Oplaat C, Fowkes A, McGreig S et al. 2023. Tomato brown rugose fruit virus Nextstrain build version 3: rise of a novel clade. PhytoFrontiers https://doi.org/10.1094/PHYTOFR-09-22-0090-A
    [Crossref] [Google Scholar]
  18. 18.
    Broughton JP, Deng X, Yu G, Fasching CL, Servellita V et al. 2020. CRISPR-Cas12-based detection of SARS-CoV-2. Nat. Biotechnol. 38:7870–74
    [Google Scholar]
  19. 19.
    Calder VL, Palukaitis P. 1992. Nucleotide sequence analysis of the movement genes of resistance breaking strains of tomato mosaic virus. J. Gen. Virol. 73:1165–68
    [Google Scholar]
  20. 20.
    Camacho-Beltrán E, Pérez-Villarreal A, Leyva-López NE, Rodríguez-Negrete EA, Ceniceros-Ojeda EA, Méndez-Lozano J. 2019. Occurrence of tomato brown rugose fruit virus infecting tomato crops in Mexico. Plant Dis 103:61440
    [Google Scholar]
  21. 21.
    Cambrón-Crisantos JM, Rodríguez-Mendoza J, Valencia-Luna JB, Alcasio-Rangel S, de Jesús, García-Ávila C et al. 2018. First report of tomato brown rugose fruit virus (ToBRFV) in Michoacan, Mexico. Mex. J. Phytopathol. 37:1185–92
    [Google Scholar]
  22. 22.
    Caruso AG, Bertacca S, Parrella G, Rizzo R, Davino S, Panno S. 2022. Tomato brown rugose fruit virus: a pathogen that is changing the tomato production worldwide. Ann. Appl. Biol. 181:3258–74
    [Google Scholar]
  23. 23.
    Çelik A, Coşkan S, Morca AF, Santosa AI, Koolivand D. 2022. Insight into population structure and evolutionary analysis of the emerging tomato brown rugose fruit virus. Plants 11:233279
    [Google Scholar]
  24. 24.
    Chanda B, Gilliard A, Jaiswal N, Ling K-S. 2021. Comparative analysis of host range, ability to infect tomato cultivars with Tm-22 gene, and real-time reverse transcription PCR detection of tomato brown rugose fruit virus. Plant Dis 105:113643–52
    [Google Scholar]
  25. 25.
    Chanda B, Shamimuzzaman M, Gilliard A, Ling KS. 2021. Effectiveness of disinfectants against the spread of tobamoviruses: tomato brown rugose fruit virus and cucumber green mottle mosaic virus. Virol. J. 18:7
    [Google Scholar]
  26. 26.
    Davino S, Caruso AG, Bertacca S, Barone S, Panno S. 2020. Tomato brown rugose fruit virus: seed transmission rate and efficacy of different seed disinfection treatments. Plants 9:111615
    [Google Scholar]
  27. 27.
    de Ronde D, Butterbach P, Kormelink R. 2014. Dominant resistance against plant viruses. Front. Plant Sci. 5:307
    [Google Scholar]
  28. 28.
    Dey K, Vilez-Climent M, Soria P, Batuman O, Mavrodieva V et al. 2021. First report of tomato brown rugose fruit virus (ToBRFV) infecting tomato in Florida, USA. New Dis. Rep. 44:1e12028
    [Google Scholar]
  29. 29.
    Dombrovsky A, Mor N, Gantz S, Lachman O, Smith E. 2022. Disinfection efficacy of tobamovirus-contaminated soil in greenhouse-grown crops. Horticulturae 8:7563
    [Google Scholar]
  30. 30.
    Dombrovsky A, Smith E. 2017. Seed transmission of tobamoviruses: aspects of global disease distribution. Advances in Seed Biology JC Jimenez-Lopez 233–60. London: IntechOpen
    [Google Scholar]
  31. 31.
    Dubrovina AS, Kiselev KV. 2019. Exogenous RNAs for gene regulation and plant resistance. Int. J. Mol. Sci. 20:92282
    [Google Scholar]
  32. 32.
    EFSA Panel Plant Health 2011. Scientific opinion on the assessment of the risk of solanaceous pospiviroids for the EU territory and the identification and evaluation of risk management options. EFSA J 9:82330
    [Google Scholar]
  33. 33.
    Ehlers J, Nourinejhad Zarghani S, Kroschewski B, Büttner C, Bandte M 2022. Cleaning of tomato brown rugose fruit virus (ToBRFV) from contaminated clothing of greenhouse employees. Horticulturae 8:8751
    [Google Scholar]
  34. 34.
    Ehlers J, Nourinejhad Zarghani S, Kroschewski B, Büttner C, Bandte M 2022. Decontamination of tomato brown rugose fruit virus–contaminated shoe soles under practical conditions. Horticulturae 8:121210
    [Google Scholar]
  35. 35.
    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]
  36. 36.
    EPPO 2019. Update of the situation of tomato brown rugose fruit virus in Mexico EPPO Rep. Serv. 2019/192 Eur. Mediterr. Plant Prot. Organ. Paris: https://gd.eppo.int/reporting/article-6622
    [Google Scholar]
  37. 37.
    EPPO 2020. EPPO report on notifications of non-compliance EPPO Rep. Serv. 2020/068 Eur. Mediterr. Plant Prot. Organ Paris: https://gd.eppo.int/reporting/article-6746
    [Google Scholar]
  38. 38.
    EPPO 2020. EPPO report on notifications of non-compliance EPPO Rep. Serv. 2020/114 Eur. Mediterr. Plant Prot. Organ Paris: https://gd.eppo.int/reporting/article-6792
    [Google Scholar]
  39. 39.
    EPPO 2020. Eradication of tomato brown rugose fruit virus in Poland EPPO Rep. Serv. 2020/200 Eur. Mediterr. Plant Prot. Organ Paris: https://gd.eppo.int/reporting/article-6878
    [Google Scholar]
  40. 40.
    EPPO 2020. First report of tomato brown rugose fruit virus in Cyprus EPPO Rep. Serv. 2020/173 Eur. Mediterr. Plant Prot. Organ Paris: https://gd.eppo.int/reporting/article-6851
    [Google Scholar]
  41. 41.
    EPPO 2020. First report of tomato brown rugose fruit virus in Poland EPPO Rep. Serv. 2020/122 Eur. Mediterr. Plant Prot. Organ Paris: https://gd.eppo.int/reporting/article-6800
    [Google Scholar]
  42. 42.
    EPPO 2020. First report of tomato brown rugose fruit virus in the Czech Republic EPPO Rep. Serv. 2020/223 Eur. Mediterr. Plant Prot. Organ Paris: https://gd.eppo.int/reporting/article-6901
    [Google Scholar]
  43. 43.
    EPPO 2020. Tomato brown rugose fruit virus does not occur in Egypt EPPO Rep. Serv. 2020/125 Eur. Mediterr. Plant Prot. Organ. Paris: https://gd.eppo.int/reporting/article-6803
    [Google Scholar]
  44. 44.
    EPPO 2021. EPPO report on notifications of non-compliance EPPO Rep. Serv. 2021/031 Eur. Mediterr. Plant Prot. Organ Paris: https://gd.eppo.int/reporting/article-6970
    [Google Scholar]
  45. 45.
    EPPO 2021. EPPO report on notifications of non-compliance EPPO Rep. Serv. 2021/077 Eur. Mediterr. Plant Prot. Organ Paris: https://gd.eppo.int/reporting/article-7016
    [Google Scholar]
  46. 46.
    EPPO 2021. EPPO report on notifications of non-compliance EPPO Rep. Serv. 2021/170 Eur. Mediterr. Plant Prot. Organ Paris: https://gd.eppo.int/reporting/article-7109
    [Google Scholar]
  47. 47.
    EPPO 2021. First report of tomato brown rugose fruit virus in Austria EPPO Rep. Serv. 2021/159 Eur. Mediterr. Plant Prot. Organ Paris: https://gd.eppo.int/reporting/article-7098
    [Google Scholar]
  48. 48.
    EPPO 2021. First report of tomato brown rugose fruit virus in Belgium EPPO Rep. Serv. 2021/017 Eur. Mediterr. Plant Prot. Organ. Paris: https://gd.eppo.int/reporting/article-6956
    [Google Scholar]
  49. 49.
    EPPO 2021. First report of tomato brown rugose fruit virus in Bulgaria EPPO Rep. Serv. 2021/135 Eur. Mediterr. Plant Prot. Organ Paris: https://gd.eppo.int/reporting/article-7074
    [Google Scholar]
  50. 50.
    EPPO 2021. First report of tomato brown rugose fruit virus in Estonia EPPO Rep. Serv. 2021/176 Eur. Mediterr. Plant Prot. Organ. Paris: https://gd.eppo.int/reporting/article-7115
    [Google Scholar]
  51. 51.
    EPPO 2021. First report of tomato brown rugose fruit virus in Hungary EPPO Rep. Serv. 2021/134 Eur. Mediterr. Plant Prot. Organ Paris: https://gd.eppo.int/reporting/article-7073
    [Google Scholar]
  52. 52.
    EPPO 2021. First report of tomato brown rugose fruit virus in Malta EPPO Rep. Serv. 2021/106 Eur. Mediterr. Plant Prot. Organ Paris: https://gd.eppo.int/reporting/article-7045
    [Google Scholar]
  53. 53.
    EPPO 2021. First report of tomato brown rugose fruit virus in Portugal EPPO Rep. Serv. 2021/196 Eur. Mediterr. Plant Prot. Organ Paris: https://gd.eppo.int/reporting/article-7135
    [Google Scholar]
  54. 54.
    EPPO 2021. First report of tomato brown rugose fruit virus in Uzbekistan EPPO Rep. Serv. 2021/222 Eur. Mediterr. Plant Prot. Organ Paris: https://gd.eppo.int/reporting/article-7161
    [Google Scholar]
  55. 55.
    EPPO 2021. PM 7/146 (2) Tomato brown rugose fruit virus. EPPO Bull 51:2178–197
    [Google Scholar]
  56. 56.
    EPPO 2021. Update on the situation of tomato brown rugose fruit virus in Poland EPPO Rep. Serv. 2021/087 Eur. Mediterr. Plant Prot. Organ Paris: https://gd.eppo.int/reporting/article-7026
    [Google Scholar]
  57. 57.
    EPPO 2022. EPPO report on notifications of non-compliance EPPO Rep. Serv. 2022/098 Eur. Mediterr. Plant Prot. Organ Paris: https://gd.eppo.int/reporting/article-7329
    [Google Scholar]
  58. 58.
    EPPO 2022. First report of tomato brown rugose fruit virus in Finland EPPO Rep. Serv. 2022/167 Eur. Mediterr. Plant Prot. Organ Paris: https://gd.eppo.int/reporting/article-7399
    [Google Scholar]
  59. 59.
    EPPO 2022. Tomato brown rugose fruit virus (TOBRFV) datasheet. EPPO Global Database https://gd.eppo.int/taxon/TOBRFV/datasheet
    [Google Scholar]
  60. 60.
    EPPO 2022. Tomato brown rugose fruit virus (TOBRFV): hosts. EPPO Global Database https://gd.eppo.int/taxon/TOBRFV/hosts
    [Google Scholar]
  61. 61.
    Esmaeilzadeh F, Koolivand D. 2022. First report of tomato brown rugose fruit virus infecting bell pepper in Iran. J. Plant Pathol. 104:2893
    [Google Scholar]
  62. 62.
    Esmaeilzadeh F, Koolivand D. 2022. Occurrence of tomato brown rugose fruit virus in tomato in Iran. J. Plant Pathol. 104:1457
    [Google Scholar]
  63. 63.
    Fidan H, Sarikaya P, Calis O. 2019. First report of tomato brown rugose fruit virus on tomato in Turkey. New Dis. Rep. 39:118
    [Google Scholar]
  64. 64.
    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]
  65. 65.
    Folimonova SY, Achor D, Bar-Joseph M. 2020. Walking together: cross-protection, genome conservation, and the replication machinery of Citrus tristeza virus. Viruses 12:121353
    [Google Scholar]
  66. 66.
    Fulton RW. 1986. Practices and precautions in the use of cross protection for plant virus disease control. Annu. Rev. Phytopathol. 24:67–81
    [Google Scholar]
  67. 67.
    Gaafar YZA, Ziebell H. 2020. Novel targets for engineering Physostegia chlorotic mottle and tomato brown rugose fruit virus-resistant tomatoes: in silico prediction of tomato microRNA targets. PeerJ 8:e10096
    [Google Scholar]
  68. 68.
    Ghorbani A, Rostami M, Seifi S, Izadpanah K. 2021. First report of tomato brown rugose fruit virus in greenhouse tomato in Iran. New Dis. Rep. 44:2e12040
    [Google Scholar]
  69. 69.
    González-Concha LF, Ramírez-Gil JG, García-Estrada RS, Rebollar-Alviter Á, Tovar-Pedraza JM. 2021. Spatiotemporal analyses of tomato brown rugose fruit virus in commercial tomato greenhouses. Agronomy 11:71268
    [Google Scholar]
  70. 70.
    González-Concha LF, Ramírez-Gil JG, Mora-Romero GA, García-Estrada RS, Carrillo-Fasio JA, Tovar-Pedraza JM. 2023. Development of a scale for assessment of disease severity and impact of tomato brown rugose fruit virus on tomato yield. Eur. J. Plant Pathol. 165:579–92
    [Google Scholar]
  71. 71.
    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]
  72. 72.
    Hamborg Z, Blystad D-R. 2022. First report of tomato brown rugose fruit virus in tomato in Norway. Plant Dis 106:72004
    [Google Scholar]
  73. 73.
    Hamelink R, Kalisvaart J, Rashidi H. 2019. TBRFV resistant tomato plant WO Patent 2019/110130
    [Google Scholar]
  74. 74.
    Hasan ZM, Salem NM, Ismail ID, Akel EH, Ahmad AY. 2022. First report of tomato brown rugose fruit virus on greenhouse tomato in Syria. Plant Dis 106:2772
    [Google Scholar]
  75. 75.
    He S, Krainer KMC. 2020. Pandemics of people and plants: Which is the greater threat to food security?. Mol. Plant 13:7933–34
    [Google Scholar]
  76. 76.
    Heinlein M. 2015. Plant virus replication and movement. Virology479–480:657–71
    [Google Scholar]
  77. 77.
    Hiddink G, Willmann R, Woudenberg JHC, Souza-Richards R. 2023. Seed health testing: doing things right. PhytoFrontiers https://doi.org/10.1094/PHYTOFR-03-22-0029-FI
    [Google Scholar]
  78. 78.
    Iobbi V, Lanteri AP, Minuto A, Santoro V, Ferrea G et al. 2022. Autoxidation products of the methanolic extract of the leaves of Combretum micranthum exert antiviral activity against tomato brown rugose fruit virus (ToBRFV). Molecules 27:3760
    [Google Scholar]
  79. 79.
    Iobbi V, Santoro V, Maggi N, Giacomini M, Lanteri AP et al. 2023. Characterization of sulfur compounds and antiviral activity against tomato brown rugose fruit virus (ToBRFV) of Italian “Vessalico” garlic compared to other cultivars and landrace. LWT 174:114411
    [Google Scholar]
  80. 80.
    ISF-ISHI-Veg 2020. Detection of infectious tomato brown rugose fruit virus (ToBRFV) in tomato and pepper seeds Rep., Int. Seed Fed., Nyon Switz: https://worldseed.org/wp-content/uploads/2020/11/Tomato-ToBRFV_2020v1.5.pdf
    [Google Scholar]
  81. 81.
    Ishibashi K, Ishikawa M. 2016. Replication of tobamovirus RNA. Annu. Rev. Phytopathol. 54:55–78
    [Google Scholar]
  82. 82.
    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]
  83. 83.
    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]
  84. 84.
    Jewehan A, Salem N, Tóth Z, Salamon P, Szabó Z. 2022. Evaluation of responses to tomato brown rugose fruit virus (ToBRFV) and selection of resistant lines in Solanum habrochaites and Solanum peruvianum germplasm. J. Gen. Plant Pathol. 88:3187–96
    [Google Scholar]
  85. 85.
    Jewehan A, Salem N, Tóth Z, Salamon P, Szabó Z. 2022. Screening of Solanum (sections Lycopersicon and Juglandifolia) germplasm for reactions to the tomato brown rugose fruit virus (ToBRFV). J. Plant Dis. Prot. 129:1117–23
    [Google Scholar]
  86. 86.
    Jones RAC. 2021. Global plant virus disease pandemics and epidemics. Plants 10:2233
    [Google Scholar]
  87. 87.
    Kabas A, Fidan H, Kucukaydin H, Atan HN. 2022. Screening of wild tomato species and interspecific hybrids for resistance/tolerance to tomato brown rugose fruit virus (ToBRFV). Chil. J. Agric. Res. 82:1189–96
    [Google Scholar]
  88. 88.
    Kalinina NO, Khromov A, Love AJ, Taliansky ME 2020. CRISPR applications in plant virology: virus resistance and beyond. Phytopathology 110:118–28
    [Google Scholar]
  89. 89.
    Kalisvaart J, Ludeking DJW, Roovers AJM. 2022. Gene leading to ToBRFV resistance in S lycopersicum. WO Patent 2022/013452
    [Google Scholar]
  90. 90.
    Klap C, Luria N, Smith E, Bakelman E, Belausov E et al. 2020. The potential risk of plant-virus disease initiation by infected tomatoes. Plants 9:5623
    [Google Scholar]
  91. 91.
    Klap C, Luria N, Smith E, Hadad L, Bakelman E et al. 2020. Tomato brown rugose fruit virus contributes to enhanced pepino mosaic virus titers in tomato plants. Viruses 12:8879
    [Google Scholar]
  92. 92.
    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]
  93. 93.
    Kopeliovitch E, Gilan I. 2022. A tomato plant comprising dominant resistance genes to tomato brown rugose fruit virus WO Patent 2022/018734
    [Google Scholar]
  94. 94.
    Kubo S, Ikeda T, Imaizumi S, Takanami Y, Mikami Y. 1990. A potent plant virus inhibitor found in Mirabilis jalapa L. Jpn. J. Phytopathol 56:4481–87
    [Google Scholar]
  95. 95.
    Kutsher Y, Evenor D, Belausov E, Lapidot M, Reuveni M. 2021. Leaf plasmodesmata respond differently to TMV, ToBRFV and TYLCV infection. Plants 10:71442
    [Google Scholar]
  96. 96.
    Levitzky N, Smith E, Lachman O, Luria N, Mizrahi Y et al. 2019. The bumblebee Bombus terrestris carries a primary inoculum of tomato brown rugose fruit virus contributing to disease spread in tomatoes. PLOS ONE 14:1e0210871
    [Google Scholar]
  97. 97.
    Lindbo J. 2022. Tomato plants resistant to ToBRFV, TMV, ToMV and ToMMV and corresponding resistance genes WO Patent 2022/117884
    [Google Scholar]
  98. 98.
    Ling K-S, Gilliard AC, Zia B. 2022. Disinfectants useful to manage the emerging tomato brown rugose fruit virus in greenhouse tomato production. Horticulturae 8:121193
    [Google Scholar]
  99. 99.
    Ling K-S, Tian T, Gurung S, Salati R, Gilliard A. 2019. First report of tomato brown rugose fruit virus infecting greenhouse tomato in the United States. Plant Dis 103:61439
    [Google Scholar]
  100. 100.
    Loh YL, Skelton A, Fox A 2022. On site detection of tomato brown rugose fruit virus: validation of ToBRFV diagnostics (LAMP) for use by UK growers Rep. PE035, Agric. Hortic. Dev. Board Stoneleigh, UK:
    [Google Scholar]
  101. 101.
    Luigi M, Manglli A, Tiberini A, Bertin S, Ferretti L et al. 2022. Inter-laboratory comparison of RT-PCR-based methods for the detection of tomato brown rugose fruit virus on tomato. Pathogens 11:2207
    [Google Scholar]
  102. 102.
    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]
  103. 103.
    Luria N, Smith E, Sela N, Lachman O, Bekelman I et al. 2018. A local strain of paprika mild mottle virus breaks L3 resistance in peppers and is accelerated in tomato brown rugose fruit virus-infected Tm-22-resistant tomatoes. Virus Genes 54:2280–89
    [Google Scholar]
  104. 104.
    Ma Z, Zhang H, Ding M, Zhang Z, Yang X, Zhou X. 2021. Molecular characterization and pathogenicity of an infectious cDNA clone of tomato brown rugose fruit virus. Phytopathol. Res. 3:14
    [Google Scholar]
  105. 105.
    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. 163:71863–75
    [Google Scholar]
  106. 106.
    Magaña-Álvarez AA, Pérez-Brito D, Vargas-Hernández BY, Ramírez-Pool JA, Núñez-Muñoz LA et al. 2021. Detection of tomato brown rugose fruit virus (ToBRFV) in solanaceous plants in Mexico. J. Plant Dis. Prot. 128:61627–35
    [Google Scholar]
  107. 107.
    Mahillon M, Kellenberger I, Dubuis N, Brodard J, Bunter M et al. 2022. First report of tomato brown rugose fruit virus in tomato in Switzerland. New Dis. Rep. 45:1e12065
    [Google Scholar]
  108. 108.
    McKinney H. 1929. Mosaic diseases in the Canary Islands, West Africa and Gibraltar. J. Agric. Res. 39:577–78
    [Google Scholar]
  109. 109.
    Menzel W, Knierim D, Winter S, Hamacher J, Heupel M. 2019. First report of tomato brown rugose fruit virus infecting tomato in Germany. New Dis. Rep. 39:1
    [Google Scholar]
  110. 110.
    Menzel W, Winter S. 2019. Identification of novel and known tobamoviruses in tomato and other solanaceous crops using a new pair of generic primers and development of a specific RT-qPCR for ToBRFV. Acta Hortic 1316:143–48
    [Google Scholar]
  111. 111.
    Meshi T, Motoyoshi F, Maeda T, Yoshiwoka S, Watanabe H, Okada Y. 1989. Mutations in the tobacco mosaic virus 30-kD protein gene overcome Tm-2 resistance in tomato. Plant Cell 1:5515–22
    [Google Scholar]
  112. 112.
    Millenaar F, Vredenbregt-Pillon P, Altena J, Mammella MA, Verbakel H. 2021. Solanum lycopersicum plants having improved Tobamovirus resistance. WO Patent 2021/213892
  113. 113.
    Nicaise V. 2014. Crop immunity against viruses: outcomes and future challenges. Front. Plant Sci. 5:660
    [Google Scholar]
  114. 114.
    Nourinejhad Zarghani S, Monavari M, Ehlers J, Hamacher J, Büttner C, Bandte M 2022. Comparison of models for quantification of tomato brown rugose fruit virus based on a bioassay using a local lesion host. Plants 11:243443
    [Google Scholar]
  115. 115.
    Orfanidou CG, Cara M, Merkuri J, Papadimitriou K, Katis NI, Maliogka VI. 2022. First report of tomato brown rugose fruit virus in tomato in Albania. J. Plant Pathol. 104:855
    [Google Scholar]
  116. 116.
    Ortiz-Martínez LE, Ochoa-Martínez DL. 2023. Elicitors and biostimulants in the production of tomato infected with Tomato brown rugose fruit virus. J. Plant Dis. Prot. 130:351–60
    [Google Scholar]
  117. 117.
    Pallas V, García JA. 2011. How do plant viruses induce disease? Interactions and interference with host components. J. Gen. Virol. 92:122691–705
    [Google Scholar]
  118. 118.
    Pandey AK, Sain SK, Singh P. 2016. A perspective on integrated disease management in agriculture. Bio Bull 2:213–29
    [Google Scholar]
  119. 119.
    Panno S, Caruso AG, Barone S, Lo Bosco G, Rangel EA, Davino S 2020. Spread of tomato brown rugose fruit virus in Sicily and evaluation of the spatiotemporal dispersion in experimental conditions. Agronomy 10:6834
    [Google Scholar]
  120. 120.
    Panno S, Caruso AG, Blanco G, Davino S. 2020. First report of tomato brown rugose fruit virus infecting sweet pepper in Italy. New Dis. Rep. 41:120
    [Google Scholar]
  121. 121.
    Panno S, Caruso AG, Davino S. 2019. First report of tomato brown rugose fruit virus on tomato crops in Italy. Plant Dis 103:61443
    [Google Scholar]
  122. 122.
    Panno S, Ruiz-Ruiz S, Caruso AG, Alfaro-Fernandez A, San Ambrosio MIF, Davino S 2019. Real-time reverse transcription polymerase chain reaction development for rapid detection of tomato brown rugose fruit virus and comparison with other techniques. PeerJ 7:e7928
    [Google Scholar]
  123. 123.
    Pechar GS, Donaire L, Gosalvez B, García-Almodovar C, Sánchez-Pina MA et al. 2022. Editing melon eIF4E associates with virus resistance and male sterility. Plant Biotechnol. J. 20:102006–22
    [Google Scholar]
  124. 124.
    Pechinger K, Chooi KM, MacDiarmid RM, Harper SJ, Ziebell H. 2019. A new era for mild strain cross-protection. Viruses 11:7670
    [Google Scholar]
  125. 125.
    Pfitzner AJP 2006. Resistance to tobacco mosaic virus and tomato mosaic virus in tomato BT: natural resistance mechanisms of plants to viruses. Natural Resistance Mechanisms of Plants to Viruses G Loebenstein, JP Carr 399–413. Dordrecht, Neth: Springer
    [Google Scholar]
  126. 126.
    Pyott DE, Sheehan E, Molnar A. 2016. Engineering of CRISPR/Cas9-mediated potyvirus resistance in transgene-free Arabidopsis plants. Mol. Plant Pathol. 17:81276–88
    [Google Scholar]
  127. 127.
    Ragasová L, Hakalová E, Ferby V, Čechová J, Klapcová G, Pokluda R. 2022. Effect of plant growth promoting microorganisms on pepper plants infected with tomato brown rugose fruit virus. Diversity 14:8635
    [Google Scholar]
  128. 128.
    Reason J. 2000. Human error: models and management. BMJ 320:7237768–70
    [Google Scholar]
  129. 129.
    Rivera-Márquez K, Núñez-Muñoz LA, Calderón-Pérez B, De La Torre-Almaraz R, Vargas-Hernández BY et al. 2022. Bioinformatic-based approach for mutagenesis of plant immune Tm-22 receptor to confer resistance against tomato brown rugose fruit virus (ToBRFV). Front. Plant Sci. 13:984846
    [Google Scholar]
  130. 130.
    Rizzo D, Da Lio D, Panattoni A, Salemi C, Cappellini G et al. 2021. Rapid and sensitive detection of tomato brown rugose fruit virus in tomato and pepper seeds by reverse transcription loop-mediated isothermal amplification assays (real time and visual) and comparison with RT-PCR end-point and RT-QPCR methods. Front. Microbiol. 12:640932
    [Google Scholar]
  131. 131.
    Robertson G, Burger J, Campa M. 2022. CRISPR/Cas-based tools for the targeted control of plant viruses. Mol. Plant Pathol. 23:111701–18
    [Google Scholar]
  132. 132.
    Sabra A, Al Saleh MA, Alshahwan IM, Amer MA 2021. First report of tomato brown rugose fruit virus infecting tomato crop in Saudi Arabia. Plant Dis 106:41310
    [Google Scholar]
  133. 133.
    Salem N, 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]
  134. 134.
    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]
  135. 135.
    Salem NM, Cao MJ, Odeh S, Turina M, Tahzima R. 2020. First report of tobacco mild green mosaic virus and tomato brown rugose fruit virus infecting Capsicum annuum in Jordan. Plant Dis 104:2601
    [Google Scholar]
  136. 136.
    Salem NM, Sulaiman A, Samarah N, Turina M, Vallino M. 2022. Localization and mechanical transmission of tomato brown rugose fruit virus in tomato seeds. Plant Dis 106:1275–81
    [Google Scholar]
  137. 137.
    Samarah N, Sulaiman A, Salem NM, Turina M. 2021. Disinfection treatments eliminated tomato brown rugose fruit virus in tomato seeds. Eur. J. Plant Pathol. 159:1153–62
    [Google Scholar]
  138. 138.
    Sarkes A, Fu H, Feindel D, Harding M, Feng J. 2020. Development and evaluation of a loop-mediated isothermal amplification (LAMP) assay for the detection of tomato brown rugose fruit virus (ToBRFV). PLOS ONE 15:6e0230403
    [Google Scholar]
  139. 139.
    Skelton A, Buxton-Kirk A, Ward R, Harju V, Frew L et al. 2019. First report of tomato brown rugose fruit virus in tomato in the United Kingdom. New Dis. Rep. 40:12
    [Google Scholar]
  140. 140.
    Skelton A, Frew L, Buxton-Kirk A, Ward R, Forde S et al. 2021. Tomato brown rugose fruit virus: survival of the virus and efficacy of disinfection approaches Rep. PE033a, Agric. Hortic. Dev. Board Stoneleigh, UK:
    [Google Scholar]
  141. 141.
    Skelton A, Gentit P, Porcher L, Visage M, Fowkes A et al. 2022. First report of tomato brown rugose fruit virus in tomato in France. New Dis. Rep. 45:1e12061
    [Google Scholar]
  142. 142.
    Spiegelman Z, Hak H, Loeb Ezra J, Sherman Y 2022. Tobamovirus-resistant tomato plants WO Patent 2022/091104
    [Google Scholar]
  143. 143.
    Tiberini A, Manglli A, Taglienti A, Vučurović A, Brodarič J et al. 2022. Development and validation of a one-step reverse transcription real-time PCR assay for simultaneous detection and identification of tomato mottle mosaic virus and tomato brown rugose fruit virus. Plants 11:4489
    [Google Scholar]
  144. 144.
    Vaisman M, Hak H, Arazi T, Spiegelman Z. 2023. The impact of tobamovirus infection on root development involves induction of auxin response factor 10a in tomato. Plant Cell Physiol 63:1980–93
    [Google Scholar]
  145. 145.
    van de Vossenberg BTLH, Visser M, Bruinsma M, Koenraadt HMS, Westenberg M, Botermans M. 2020. Real-time tracking of tomato brown rugose fruit virus (ToBRFV) outbreaks in the Netherlands using Nextstrain. PLOS ONE 15:10e0234671
    [Google Scholar]
  146. 146.
    Vargas-Hernández BY, Ramírez-Pool JA, Núñez-Muñoz LA, Calderón-Pérez B, De La Torre-Almaráz R et al. 2022. Development of a droplet digital polymerase chain reaction (ddPCR) assay for the detection of tomato brown rugose fruit virus (ToBRFV) in tomato and pepper seeds. J. Virol. Methods 302:114466
    [Google Scholar]
  147. 147.
    Verma HN, Abid Ali Khan MM 1984. Management of plant virus diseases by Pseuderanthemum bicolor leaf extract. J. Plant Dis. Prot. 91:3266–72
    [Google Scholar]
  148. 148.
    Vučurović A, Brodarič J, Jakomin T, Pecman A, Beloglavec AB, Mehle N. 2022. First report of tomato brown rugose fruit virus in tomato in Slovenia. New Dis. Rep. 45:2e12079
    [Google Scholar]
  149. 149.
    WUSF Public Media 2019. Virus found in Mexican tomatoes worries Florida agriculture officials. WGCU https://news.wgcu.org/2019-10-10/virus-found-in-mexican-tomatoes-worries-florida-agriculture-officials
    [Google Scholar]
  150. 150.
    Yan Z, Ma H, Han S, Geng C, Tian Y, Li X. 2019. First report of tomato brown rugose fruit virus infecting tomato in China. Plant Dis 103:112973
    [Google Scholar]
  151. 151.
    Yan Z, Ma H, Wang L, Tettey C, Zhao M 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]
  152. 152.
    Yan Z, Zhao M, Ma H, Liu L, Yang G et al. 2021. Biological and molecular characterization of tomato brown rugose fruit virus and development of quadruplex RT-PCR detection. J. Integr. Agric. 20:71871–79
    [Google Scholar]
  153. 153.
    Ykema M, Verweij CW, de la Fuente van Bentem S. 2020. Tomato plant resistant to tomato brown rugose fruit virus WO Patent 2020/147921
    [Google Scholar]
  154. 154.
    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]
  155. 155.
    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]
/content/journals/10.1146/annurev-phyto-021622-120703
Loading
/content/journals/10.1146/annurev-phyto-021622-120703
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