Tomato brown rugose fruit virus

Tomato brown rugose fruit virus (ToBRV) is a plant virus in the genus Tobamovirus that was first described in 2015. It has spread rapidly since it was first noted in Jordan and Israel. The main hosts are tomato and peppers. The virus causes symptoms including mosaic and distortion of leaves and brown, wrinkly spots (rugose) on fruits. Outbreaks can be severe and leave fruit unmarketable.

Tomato brown rugose fruit virus
Virus classification
(unranked): Virus
Realm: Riboviria
Kingdom: Orthornavirae
Phylum: Kitrinoviricota
Class: Alsuviricetes
Order: Martellivirales
Family: Virgaviridae
Genus: Tobamovirus
Species:
Tomato brown rugose fruit virus

History and distribution

In 2015 greenhouse tomato crops in Jordan showed mild foliar symptoms during the season, with fruit then developing strong brown rugose symptoms. Total RNA was extracted from the plants and Reverse transcription polymerase chain reaction (RT-PCR) were negative for many common tomato viruses but indicated the presence of a new tobamovirus[1]. After sequencing and characterisation, the name tomato brown fruit rugose virus (ToBRFV) was proposed.[1] The name was approved by the International Committee on Taxonomy of Viruses later the same year.[2] In 2019 it was confirmed that symptoms observed on Capsicum annuum crops in Jordan in 2015 and 2016 were caused by infection of ToBRFV and Tobacco mild green mosaic virus.[3]

A disease with similar symptoms had emerged earlier in Ohad, Israel in Autumn 2014 and began to spread in the country within a year. Transmission electron microscopy showed the presence of rod-like viral structures consistent with Tobamovirus and the complete sequence showed high sequence identity to the Jordanian isolate of tomato brown rugose fruit virus.[4] The infected plants in Israel were cultivars that carried the Tm-22 resistance gene which confers diseases resistance against some other tobamoviruses.[4] ToBRFV has also been confirmed from Palestine[5] with symptoms first noted in Autumn 2018.[6]

Tomato brown rugose fruit virus spread rapidly to other tomato growing regions. After emerging in Israel and Jordan, the virus spread to Europe. Symptoms were noted in July 2018 on 25 hectares of greenhouse tomatoes in Germany. Plants were found to be infected with both ToBRFV and pepino mosic virus.[7] Measures to eradicate the virus were taken.[8] In Autumn of 2018 symptoms were noted on tomato crops in Sicily, Italy. and confirmed as being caused by ToBRFV.[9] In May 2019 ToBRFV emerged on tomato crops in mainland Italy, in the Piemonte region.[10] This outbreak was eradicated.[11]

Disease caused by tomato brown rugose fruit virus also emerged in North America in Autumn 2018, initially being reported from Mexico. This also included the first case of Capsicum being infected.[12] An outbreak was also detected in California in Autumn 2018 and eradicated by the California Department of Food and Agriculture.[13] The pathway of introduction into North America was unknown.[13] By February 2019, ToBRFV had been detected in 20 States across Mexico, and the first positive in aubergine was reported.[14]

In January 2019 the first case of ToBRFV in Turkey was reported in greenhouse crops.[15] In April 2019 disease on tomato crops in Shandong, China was confirmed to be caused by ToBRFV, the pathway of introduction to China was unknown.[16] New outbreaks also emerged in Europe over the course of 2019. In Summer 2019 the first outbreak of ToBRFV occurred in the United Kingdom, with action taken to eradicate the virus.[17] The Netherlands also reported their first outbreak on tomato crops[18], as well as Greece[19], Spain[20] and ToBRFV was reported from France in January 2020.[21] By February 2020 17 outbreaks had been detected in the Netherlands[22] and an additional 9 sites were infected in Spain[23] and the first outbreak on Capsicum annuum was detected in Italy.[24]

Hosts and symptoms

Most outbreaks of ToBRFV have been reported on tomato, but Capsicum species have also been reported to be infected.[6] An instance of infection of aubergine has been reported in Mexico[14], but the virus could not be experimentally transmitted to this host in other studies.[25] It has also been detected on weed species.[6].

Symptoms in tomato vary based on the tomato variety and may be mild to severe.[26] Foliar symptoms include mild to severe mosaic, narrowing and discolouration. Classic symptoms are the brown and wrinkled (rugose) patches that form on infected fruits, though fruits may also be mishapen or turn yellow and are often unmarketable due to symptoms.[26]

On sweet peppers, symptoms include mosaic, discolouration and vein clearing on young leaves, browning of the stem and mosaic and distortion of fruits.[24]

Transmission

Tomato brown rugose fruit virus can be transmitted mechanically - the virus is stable outside of the plant and so can spread between plants on contaminated tools, clothes or hands.[26] Seed transmission is suspected but has not yet been verified,[27] though it has been detected on tomato seed moving in trade.[22] The plant can also spread via propagation.[26] It has been inferred that mechanical transmission from the seed coat to the growing plant may occur.[6].

Buff-tailed bumblebees are often used in tomato production to pollinate plants. It has been found that bumblebees can also spread ToBRFV between tomato as they pick up the virus during pollination.[28]

Management

To date no cultivars resistant to ToBRFV have been identified.[6][16] As the virus is transmitted easily through mechanical means, hygiene best practise is essential to reduce impacts when outbreaks are detected.[26] The virus can survive a long time on various surfaces - at least 2 hours on skin and gloves, at least 3 on hard plastics and at least 1 month on glass, aluminium and stainless steel.[29] The disinfectants Virkon S and Huwa San are effective on most surfaces, but only after an hour of exposure.[29]. Plastic trays can be soaked in hot water (90°C for 5 minutes) to eliminate the virus, or at 70°C for 5 minutes and then treated with Virkon.[29]

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References
  1. Salem, N.; Mansour, A.; Ciuffo, M.; Falk, B. W.; Turina, M. (2015). "A new tobamovirus infecting tomato crops in Jordan". Archives of Virology. 161 (2): 503–506. doi:10.1007/s00705-015-2677-7. ISSN 0304-8608.
  2. Adams, M (July 2016). "Create two new species in the genus Tobamovirus, family Virgaviridae" (PDF). International Committee on Taxonomy of Viruses. Retrieved 13 April 2020.
  3. Salem, N. M.; Cao, M. J.; 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 Disease. 104 (2): 601. doi:10.1094/PDIS-06-19-1189-PDN. ISSN 0191-2917.
  4. Melcher, Ulrich; Luria, Neta; Smith, Elisheva; Reingold, Victoria; Bekelman, Ilana; Lapidot, Moshe; Levin, Ilan; Elad, Nadav; Tam, Yehudit; Sela, Noa; Abu-Ras, Ahmad; Ezra, Nadav; Haberman, Ami; Yitzhak, Liron; Lachman, Oded; Dombrovsky, Aviv (2017). "A New Israeli Tobamovirus Isolate Infects Tomato Plants Harboring Tm-22 Resistance Genes". PLOS ONE. 12 (1): e0170429. doi:10.1371/journal.pone.0170429. ISSN 1932-6203.
  5. Alkowni, Raed; Alabdallah, Osama; Fadda, Ziad (2019). "Molecular identification of tomato brown rugose fruit virus in tomato in Palestine". Journal of Plant Pathology. 101 (3): 719–723. doi:10.1007/s42161-019-00240-7. ISSN 1125-4653.
  6. Oladokun, J. O.; Halabi, M. H.; Barua, P.; Nath, P. D. (2019). "Tomato brown rugose fruit disease: current distribution, knowledge and future prospects". Plant Pathology. 68 (9): 1579–1586. doi:10.1111/ppa.13096. ISSN 0032-0862.
  7. Menzel, W.; Knierim, D.; Winter, S.; Hamacher, J.; Heupel, M. (2019). "First report of Tomato brown rugose fruit virus infecting tomato in Germany". New Disease Reports. 39: 1. doi:10.5197/j.2044-0588.2019.039.001. ISSN 2044-0588.
  8. EPPO (January 2019). "First report of Tomato brown rugose fruit virus in Germany". EPPO. Retrieved 13 April 2020.
  9. Panno, S.; Caruso, A. G.; Davino, S. (2019). "First Report of Tomato Brown Rugose Fruit Virus on Tomato Crops in Italy". Plant Disease. 103 (6): 1443–1443. doi:10.1094/PDIS-12-18-2254-PDN. ISSN 0191-2917.
  10. EPPO. "New outbreak of Tomato brown rugose fruit virus in Italy (Piemonte)". EPPO. Retrieved 13 April 2020.
  11. EPPO (September 2019). "Tomato brown rugose fruit virus eradicated from Piemonte (Italy)". EPPO. Retrieved 13 April 2020.
  12. Cambrón-Crisantos, José Manuel; Rodríguez-Mendoza, Johan; Valencia-Luna, Jessica Berenice; Alcasio-Rangel, Salomé; García-Ávila, Clemente De Jesús; López-Buenfil, José Abel; Ochoa-Martínez, Daniel Leobardo (2018). "Primer reporte de Tomato brown rugose fruit virus (ToBRFV) en Michoacán, México". Revista Mexicana de Fitopatología, Mexican Journal of Phytopathology. 37 (1). doi:10.18781/R.MEX.FIT.1810-5. ISSN 2007-8080.
  13. 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 Disease. 103 (6): 1439. doi:10.1094/PDIS-11-18-1959-PDN. ISSN 0191-2917.
  14. EPPO (September 2019). "Update of the situation of Tomato brown rugose fruit virus in Mexico". EPPO. Retrieved 13 April 2020.
  15. Fidan, H.; Sarikaya, P.; Calis, O. (2019). "First report of Tomato brown rugose fruit virus on tomato in Turkey". New Disease Reports. 39: 18. doi:10.5197/j.2044-0588.2019.039.018. ISSN 2044-0588.
  16. Yan, Z.-Y.; Ma, H.-Y.; Han, S.-L.; Geng, C.; Tian, Y.-P.; Li, X.-D. (2019). "First Report of Tomato brown rugose fruit virus Infecting Tomato in China". Plant Disease. 103 (11): 2973–2973. doi:10.1094/PDIS-05-19-1045-PDN. ISSN 0191-2917.
  17. Skelton, A.; Buxton-Kirk, A.; Ward, R.; Harju, V.; Frew, L.; Fowkes, A.; Long, M.; Negus, A.; Forde, S.; Adams, I.P.; Pufal, H.; McGreig, S.; Weekes, R.; Fox, A. (2019). "First report of Tomato brown rugose fruit virus in tomato in the United Kingdom". New Disease Reports. 40: 12. doi:10.5197/j.2044-0588.2019.040.012. ISSN 2044-0588.
  18. EPPO (October 2019). "First report of Tomato brown rugose fruit virus in the Netherlands". EPPO. Retrieved 13 April 2020.
  19. Beris, Despoina; Malandraki, Ioanna; Kektsidou, Oxana; Theologidis, Ioannis; Vassilakos, Nikon; Varveri, Christina (2020). "First report of Tomato brown rugose fruit virus infecting tomato in Greece". Plant Disease. doi:10.1094/PDIS-01-20-0212-PDN. ISSN 0191-2917.
  20. EPPO (November 2019). "First report of Tomato brown rugose fruit virus in Spain". EPPO. Retrieved 13 April 2020.
  21. EPPO (February 2020). "First report of tomato brown rugose fruit virus in France". EPPO. Retrieved 13 April 2020.
  22. EPPO (February 2020). "Update on the situation of tomato brown rugose fruit virus in the Netherlands". EPPO. Retrieved 13 April 2020.
  23. EPPO (February 2020). "Update on the situation of tomato brown rugose fruit virus in Spain". EPPO. Retrieved 13 April 2020.
  24. Panno, S.; Caruso, A.G.; Blanco, G.; Davino, S. (2020). "First report of Tomato brown rugose fruit virus infecting sweet pepper in Italy". New Disease Reports. 41: 20. doi:10.5197/j.2044-0588.2020.041.020. ISSN 2044-0588.
  25. Panno, Stefano; Ruiz-Ruiz, Susana; Caruso, Andrea Giovanni; Alfaro-Fernandez, Ana; Font San Ambrosio, Maria Isabel; Davino, Salvatore (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. doi:10.7717/peerj.7928. ISSN 2167-8359.
  26. Fox, Adrian. "Tomato Brown Rugose Fruit Virus". AHDB. Retrieved 13 April 2020.
  27. EPPO. "EPPO Alert List – Tomato brown rugose fruit virus (Tobamovirus - ToBRFV)". Retrieved 13 April 2020.
  28. Berta, Graziella; Levitzky, Naama; Smith, Elisheva; Lachman, Oded; Luria, Neta; Mizrahi, Yaniv; Bakelman, Helen; Sela, Noa; Laskar, Orly; Milrot, Elad; Dombrovsky, Aviv (2019). "The bumblebee Bombus terrestris carries a primary inoculum of Tomato brown rugose fruit virus contributing to disease spread in tomatoes". PLOS ONE. 14 (1): e0210871. doi:10.1371/journal.pone.0210871. ISSN 1932-6203.
  29. AHDB. "Survival and disinfection of Tomato Brown Rugose Fruit virus". AHDB. Retrieved 13 April 2020.
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