Tomato Brown Rugose Fruit Virus

» A new viral disease of tomatoes first observed in Israel in 2014 has since been detected in Europe, the Middle-East, and North America.

» No tomato varieties are known to be resistant to the Tomato brown rugose fruit virus.

» Preventing the spread of the virus is currently the best means of managing the disease. 

History of the Disease

Virus-like symptoms were observed on tomato plants in Israel in 2014.1 The symptoms were similar to those caused by tobamoviruses, including Tobacco mosaic virus (TMV) and Tomato mosaic virus (ToMV), but the varieties showing symptoms contained the Tm22 gene, which provides resistance to both of these viruses. Similar symptoms occurred on Tm22 tomato varieties in Jordon in 2015.2 Testing of these plants revealed the presence of a new virus, closely related to TMV and ToMV, in the tobamovirus group. The new virus was given the name Tomato brown rugose fruit virus (TBRFV) [also abbreviated ToBRFV in some articles].

TBRFV was detected on tomatoes growing in Germany and southern Italy in 2018.3 The disease appears to have been eradicated in Germany, but the virus was detected in Italy again in early 2019. The virus was also detected in tomato plants in California and Mexico in 2018. All of the infected plants in California were destroyed, and the disease is now considered to be eradicated there. Efforts to eradicate the virus in Mexico are currently underway. 

Symptoms

Mild to severe mosaic symptoms develop on the leaves of TBRFV-infected plants (Figure 1). Yellowing of the leaf veins and narrowing of leaf blades occur occasionally. Symptoms develop most commonly on the upper leaves.1 Yellow spots form on infected fruit, and brown rugose (wrinkled) patches 

Figure 1. Foliar symptoms of TBRFV infection of tomato: (A) mosaic discoloration of leaves, (B) narrowing and distortion of leaf blades.

develop on fruit surfaces (Figure 2).2 Necrotic (brown, dead) lesions sometimes form on peduncles, pedicels, and the calyx of tomato fruit. The disease tends to be more severe during times of stress, such as periods of high temperatures.

The occurrence and severity of symptoms vary with the age of the plant at the time of infection; the most severe symptoms are seen on plants infected at a young age. Tomato variety and growing conditions (temperature and light) also affect the expression of symptoms, as do fruit load and nutritional status. Symptoms typically develop within 12 to 18 days of infection, and the disease can result in yield losses of 30 to 70%.1,2 

Figure 2. Fruit symptoms: (A) brown necrotic lesions, (B) rugose fruit surface, brown streaking, and calyx necrosis.

Tobamoviruses and TBRFV

Tomato brown rugose fruit virus has been identified as a member of the Tobamovirus genus, which also contains Tobacco mosaic virus and Tomato mosaic virus.2 These viruses are very stable outside of their plant hosts, which is unusual for plant viruses. Tobamovirus particles can survive in crop debris, on tools, stakes, trellis wires, containers, greenhouse benches, and seedling trays for months to years. These viruses are mechanically transmitted in infected plant sap, meaning that anything that transfers infected plant sap from one plant to another can spread the disease. Therefore, TBRFV can be easily spread during commercial production operations including seedling production, transplanting, pruning, trellising, tying, spraying, and harvesting.4,5

TMV and ToMV are seedborne viruses, and it is possible that TBRFV is transmitted on tomato seed.1 It has also been reported that TBRFV can be spread by bumblebees.4

TBRFV can infect tomato and pepper under natural conditions. Inoculation experiments have shown that TBRFV also can infect tobacco, European black nightshade, several species of Chenopodium and Chenopodiastrum, and petunia. Thus far, eggplant and potato have not been shown to be hosts of TBRFV.1

Management

No commercial tomato varieties have been found to be resistant to TBRFV. Varieties do vary in the severity of symptom expression. However, even varieties that show only mild symptoms can contain high levels of TBRFV in their tissues and can serve as sources of inoculum for other tomato and pepper plants. The major resistance genes (Tm1, Tm2, Tm22) in tomato that provide resistance to ToMV and TMV do not provide resistance to TBRFV.1,2,5

Figure 3. Wearing disposable gloves, coveralls, and shoe covers can help prevent the spread of TBRFV on clothing.

Efforts to manage TBRFV currently focus on using clean seed and transplants and strict sanitation practices. Because the virus is easily spread on hands and clothing, workers should be encouraged to wash their hands regularly, to wear clean clothing every day, and to disinfect shoes before and after entering greenhouses, or to wear clean, disposable coveralls and shoe covers when entering greenhouses (Figure 3).5 Workers should wash their hands before and after putting on gloves. When moving to new greenhouses, workers should wash their hands, and put on new gloves coveralls, and shoe covers. 

The tools used in seedling and fruit production operations should be regularly disinfected using solutions of household bleach (diluted to 0.5% NaOCl), Virkon® S, or non-fat (skimmed) milk. These disinfectants have been shown to help prevent the mechanical transmission of several tomato viruses, including TMV and ToMV, so they also may help reduce the spread of TBRFV.6 It is important to monitor the concentration of disinfectant solutions throughout the day to ensure the proper concentration is maintained.

Workers should be grouped to work in specific greenhouse areas, and the movement of workers between areas should be minimized.

Stakes, seedling trays, and greenhouse surfaces should be thoroughly cleaned and disinfected between plantings. 

Bringing boxes, plants, and other material from external sources into greenhouses should be restricted. Some growers ask workers to avoid bringing food items containing tomatoes and peppers to work, as these items can be sources of the virus.

Only healthy seed and seedlings should be used.5 Seed companies often test tomato seed-lots for the presence of tobamoviruses (including TBRFV). Specific methods for detection are recommended by the International Seed Federation (ISF.)7 Seed companies can apply sanitizing agents to seed to reduce the presence of infective virus particles. Wet and dry heat treatments of seeds have also been shown to be effective at reducing the presence of some seedborne tomato viruses. Given that TBRFV is a virus, these procedures may also be effective for reducing the presence of this pathogen.5,8,9

Isolate production practices in greenhouses containing infected plants, and assume that all plants in the house may be infected. Work in greenhouses containing only healthy plants before working in houses containing plants suspected of being infected by TBRFV. Remove and destroy any plants that develop symptoms as soon as possible to reduce the risk of spreading the disease.

To minimize symptom expression, growers can decrease plant stress and provide optimum growing conditions. Promoting a good balance of generative and vegetative growth by reducing fruit loads can help reduce plant stress, as can ensuring adequate levels of fertilization at critical growing stages. 

Sources

1 Luria, N., Smith, E., Reingold, V., Bekelman, I., Lapidot, M., Levin, I., Elad, N., Tam, Y., Sela, N., Abu-Ras, A., Ezra, N., Haberman, A., Yitzhak, L., Lachman, O., and Dombrovsky, A. 2017. A New Israeli tobamovirus Isolate infects tomato plants harboring Tm-2(2) resistance genes. Plos One 12.
2 Salem, N., Mansour, A., Ciuffo, M., Falk, B., and Turina, M. 2016. A new tobamovirus infecting tomato crops in Jordan. Archives of Virology 161:503-506.
3 EPPO Global Database. https://gd.eppo.int/taxon/TOBRFV
4 Levitzky, N., Smith, E., Lachman, O., Luria, N., Mizrahi, Y., Bakelman, H., Sela, N., Laskar, O., Milrot, E., and Dombrovsky, 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.
5 Jones, J., Zitter, T., Momol, T., and Miller, S. 2014. Compendium of tomato diseases and pests, second edition. American Phytopathological Society, St. Paul, MN.
6 Li, R., Miller, S. A., Baysal-Gurel, F., Ling, K. S., and Kurowski, C. J. 2015. Evaluation of disinfectants to control mechanical transmission of tomato viruses and viroids in greenhouse tomatoes. In International Symposium on Tomato Diseases 1069:221-227.
7 Method for the detection of infectious tobamoviruses on tomato seed. International Seed Federation. https://www.worldseed.org/our-work/phytosanitary-matters/seed-health/ishi-veg-protocols/
8 Paylan, I. C., Erkan, S., Cetinkaya, N., Ergun, M., and Pazarlar, S. 2014. Effects of different treatments on the inactivation of various seedborne viruses in some vegetables. Ozone-Science & Engineering 36:422-426.
9 Ling, K.-S. 2010. Effectiveness of chemo- and thermotherapeutic treatments on Pepino mosaic virus in tomato seed. Plant Dis. 94:325-328.
Websites verified 2/18/2019

Additional Information

For additional agronomic information, please contact your local seed representative.
 
Performance may vary, from location to location and from year to year, as local growing, soil and weather conditions may vary. Growers should evaluate data from multiple locations and years whenever possible and should consider the impacts of these conditions on the grower’s fields. The recommendations in this article are based upon information obtained from the cited sources and should be used as a quick reference for information about greenhouse tomato production. The content of this article should not be substituted for the professional opinion of a producer, grower, agronomist, pathologist and similar professional dealing with this specific crop. SEMINIS VEGETABLE SEEDS, INC. AND MONSANTO CANADA ULC DO NOT WARRANT THE ACCURACY OF ANY INFORMATION OR TECHNICAL ADVICE PROVIDED HEREIN AND DISCLAIMS ALL LIABILITY FOR ANY CLAIM INVOLVING SUCH INFORMATION OR ADVICE. 
9018_S2 Published 04-01-2019
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