EPPO Alert List – Tomato brown rugose fruit virus (Tobamovirus - ToBRFV)
Tomato brown rugose fruit virus (Tobamovirus, ToBRFV) was first identified on tomatoes in Jordan in 2015, outbreaks have recently occurred in Italy, Mexico, Turkey, China, United Kingdom, the Netherlands, Greece, Spain, France and Poland, where the virus causes major concerns for growers of tomato and capsicum. As ToBRFV is an emerging virus and tomato is an important crop in the EPPO region, the EPPO Secretariat decided to add it to the EPPO Alert List. Since November 2019, the EU Commission has established emergency measures to prevent the introduction into, and the spread within the EU territory.
In Germany, isolated outbreaks were detected in 2018 in glasshouse tomato crops and were subsequently eradicated. A record in Egypt has been officially denied by the Egyptian NPPO.
EPPO region: France (first found in 2020), Greece (first found in 2019), Israel (first disease symptoms in 2014), Italy (eradicated from Piemonte, Sicilia), Jordan (first identified in 2015), Netherlands (first found in 2019), Poland (first found in 2020), Spain (first found in 2019), Turkey (first found in 2019), United Kingdom (first found in 2019).
North America: Mexico (under eradication), USA (isolated findings).
Asia: China (Shandong), Israel, Jordan, Turkey.
Symptoms of ToBRFV on tomatoes
Courtesy: Diana Godínez (MX) – more pictures
On which plants
Tomato (Solanum lycopersicum) and capsicum (Capsicum sp.) are the main hosts. Inoculation experiments showed that Nicotiana benthamiana, N. glutinosa, N. sylvestris, N. tabacum (tobacco) develop symptoms and that weeds such as Chenopodiastrum murale and Solanum nigrum may act as reservoirs for ToBRFV. In one study, aubergine (Solanum melongena) and potato (S. tuberosum) did not show symptoms after inoculation of the virus and ToBRFV was not found when the plants were subsequently tested by ELISA. (Luria et al., 2017). More recently, it was reported that ToBRFV was detected in a sample of aubergine collected from the state of Sinaloa, Mexico (Senasica, 2019).
On tomatoes, symptoms vary depending on varieties. Tomato cultivars with the Tm-22 resistance gene (used against other tobamoviruses) are susceptible to ToBRFV. On tomato, foliar symptoms include chlorosis, mosaic and mottling with occasional leaf narrowing. Necrotic spots may appear on peduncles, calyces and petioles. Fruit show yellow or brown spots, with rugose symptoms rendering the fruits non-marketable. Fruits may be deformed and have irregular maturation. In the paper describing the first finding in Israel, diseased plants had 10 to 15% symptomatic fruit. In Jordan, in the first reported outbreak, disease incidence reached almost 100%. On capsicum, foliar symptoms include deformation, yellowing and mosaic. Capsicum fruits are deformed, with yellow or brown areas or green stripes.
Yellow spots on tomatoes
Courtesy: Dr Aviv Dombrovsky
Rugosis on leaves
Courtesy: Diana Godínez (MX)
Symptoms on a tomato
Courtesy: Diana Godínez (MX)
ToBRFV is transmitted by contact (contaminated tools, hands, clothing, direct plant-to-plant contact) and propagation material (grafts, cuttings). Seed transmission of ToBRFV is suspected but needs to be verified. Tobamoviruses can remain infective in seeds, plant remains and contaminated soil for months. They are found in the seed coat and the endosperm, which could explain why conventional seed disinfection treatments are not fully effective to control them. Even if transmission from seed to seedling is low, further dissemination by contact (e.g. during transplantation of seedlings or regular handling of the crop) allows a rapid spread within a glasshouse. Recent glasshouse experiments have shown that ToBRFV could be carried by bumblebees (Bombus terrestris) and transmitted to healthy tomato plants during pollination (mechanically). The disease was first observed in autumn 2014 in Israel and further spread occurred across the entire country within one year, because of human-assisted spread and trade of infected seeds or seedlings.
Plants for planting, seeds? from countries where ToBRFV occurs. The virus is also spread locally by contact.
Tomato and capsicum are important crops grown in the entire EPPO region under protected conditions. Symptoms of the disease makes the fruit unmarketable. Once the virus is introduced in an area, control measures are very limited and mainly rely on elimination of infected plants and strict hygiene measures. Testing methods (ELISA, RT-PCR) are available to detect the virus in the seed. It therefore seems desirable to avoid its further introduction and spread within the region.
Amer MA, Mahmoud SY (2020) First report of Tomato brown rugose fruit virus on tomato in Egypt. New Disease Reports 41, 24. http://dx.doi.org/10.5197/j.2044-0588.2020.041.024
Chitambar J (2018) California pest rating for Tomato brown rugose fruit virus. https://blogs.cdfa.ca.gov/Section3162/?p=5843
Dombrovsky A, Smith E (2017) Seed transmission of tobamoviruses: aspects of global disease distribution, pp 234-260. In: Jose C. Jimenez-Lopez (ed.). Seed Biology. IntechOpen. 338 p. http://doi.org/10.5772/intechopen.70244
EU (2019) Commission Implementing Decision (EU) 2019/1615 of 26 September 2019 establishing emergency measures to prevent the introduction into and the spread within the Union of Tomato brown rugose fruit virus (ToBRFV). OJ L 250, 91-94. http://data.europa.eu/eli/dec_impl/2019/1615/oj
Fidan H, Sarikaya P, Calis O (2019) First report of Tomato brown rugose fruit virus on tomato in Turkey. New Disease Reports 39, 18. http://dx.doi.org/10.5197/j.2044-0588.2019.039.018
Alim’agri (2020-02-18) Virus ToBRFV : le ministère confirme la contamination de tomates en serre dans le Finistère. https://agriculture.gouv.fr/virus-tobrfv-le-ministere-confirme-la-contamination-de-tomates-en-serre-dans-le-finistere
Boletín Oficial de la Junta de Andalucía (BOJA) https://www.juntadeandalucia.es/boja/2020/21/31
NVWA (2020-02-11) Tomato brown rugose fruit virus (ToBRFV) https://www.nvwa.nl/onderwerpen/plantenziekten-en-plagen/tomato-brown-rugose-fruit-virus-tobrfv
NVWA (2020-02-07) Tomatenvirus ToBRFV ook aangetroffen op tomatenzaad https://www.nvwa.nl/onderwerpen/plantenziekten-en-plagen/nieuws/2020/02/07/nvwa-tomatenvirus-tobrfv-ook-aangetroffen-op-tomatenzaad
SADER & SENASICA (2019) presentations made at the Seminario sobre virus del género Tobamovirus con énfasis en el Tomato brown rugose fruit virus (ToBRFV): Medidas fitosanitarias para el manejo del virus rugoso del tomate. Retrieved from http://www.cesaveson.com/files/docs/eventos/Seminario Tomato/MedidasFitosanitarias.pdf
Tomato brown rugose fruit virus (ToBRFV): caso Mexico. Retrieved from http://www.cesaveson.com/files/docs/eventos/Seminario Tomato/AntecedentesTomato.pdf
JKI (2019) Express – PRA zum Tomato brown rugose fruit virus (revised). https://pflanzengesundheit.julius-kuehn.de/dokumente/upload/ToBRFV_exp-pra-rev1_de.pdf
Levitzky N, Smith E, Lachman O, Luria N, Mizrahi Y, Bakelman H, Sela N, Laskar O, Milrot E, Dombravsky A (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.
Luria N, Smith E, Reingold V, Bekelman I, Lapidot M, Levin I, et al. (2017) A new Israeli Tobamovirus isolate infects tomato plants harboring Tm-22 resistance genes. PLoS ONE 12(1). e0170429. https://doi.org/10.1371/journal.pone.0170429
NPPO of Egypt (2020-05).
NPPO of France (2020-02).
NPPO of Germany (2019-07).
NPPO of Greece (2019-10, 2020-04).
NPPO of Italy (2019-05, 2019-07, 2019-09).
NPPO of the Netherlands (2019-10) Official suspicion of Tomato brown rugose fruit virus (ToBRFV) in Solanum lycopersicum at one professional fruit production company in municipality Westland. https://english.nvwa.nl/topics/pest-reporting/contents/pest-reports
NPPO of Spain (2019-11, 2020-02).
NPPO of Poland (2020-06).
NPPO of Turkey (2019-06).
NPPO of the United Kingdom (2019-07, 2020-04, 2020-06).
Panno S, Caruso AG, Blanco G, Davino S (2020) First report of Tomato brown rugose fruit virus infecting sweet pepper in Italy. New Disease Reports 41, 20. http://dx.doi.org/10.5197/j.2044-0588.2020.041.020
Personal communication with Dr Davino (2020-04) and Dr Salem (2019-11).
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 Disease 104(2), 601. https://doi.org/10.1094/PDIS-06-19-1189-PDN
Sagarpa-Senasica (2018) Guía de síntomas de Tomato brown rugose fruit virus (ToBRFV). 19 pp.
Sagarpa-Senasica (2018) Medidas de manejo elegibles para: Tomato brown rugose fruit virus. Version 1.1. 15 pp.
USDA-APHIS (2020-06-12) APHIS takes additional actions to safeguard US agriculture against Tomato brown rugose fruit virus. https://www.aphis.usda.gov/aphis/newsroom/stakeholder-info/sa_by_date/sa-2020/sa-06/tobrfv-safeguards
USDA-APHIS (2020-06-03) APHIS amends Federal Order for US imports of tomato (Solanum lycopersicum) and pepper (Capsicum spp.) hosts of Tomato brown rugose fruit virus (ToBRFV). https://www.aphis.usda.gov/import_export/plants/plant_imports/federal_order/downloads/2020/DA-2020-12.pdf
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), p 2973. DOI: 10.1094/PDIS-05-19-1045-PDN
EPPO RS 2016/024, 2019/012, 2019/013, 2019/014, 2019/015, 2019/027, 2019/049, 2019/123, 2019/124, 2019/143, 2019/144, 2019/145, 2019/163, 2019/191, 2019/192, 2019/200, 2019/209, 2019/210, 2019/238, 2020/037, 2020/038, 2020/039, 2020/078, 2020/079, 2020/080, 2020/102, 2020/122, 2020/123, 2020/124, 2020/125