Tomato brown rugose fruit virus

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Tomato brown rugose fruit virus
DOI.10.5772.F2.png
Tomato brown rugose fruit virus (ToBRFV)-infected tomato plants
Virus classification OOjs UI icon edit-ltr.svg
(unranked): Virus
Realm: Riboviria
Kingdom: Orthornavirae
Phylum: Kitrinoviricota
Class: Alsuviricetes
Order: Martellivirales
Family: Virgaviridae
Genus: Tobamovirus
Species:
Tomato brown rugose fruit virus

Tomato brown rugose fruit virus (ToBRFV) 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.

Contents

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 the Autumn of 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 mosaic virus . [7] (This is not the first report of PMV in tomato, as this has been known to occur since the discovery of TMV.) [8] Measures to eradicate the virus were taken. [9] In Autumn of 2018 symptoms were noted on tomato crops in Sicily, Italy. and confirmed as being caused by ToBRFV. [10] In May 2019 ToBRFV emerged on tomato crops in mainland Italy, in the Piemonte region. [11] This outbreak was eradicated. [12]

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. [13] An outbreak was also detected in California in Autumn 2018 and eradicated by the California Department of Food and Agriculture. [14] The pathway of introduction into North America was unknown. [14] By February 2019, ToBRFV had been detected in 20 States across Mexico, and the first positive in aubergine was reported. [15]

In January 2019 the first case of ToBRFV in Turkey was reported in tomato crops grown in greenhouses in Antalya province [16] which since then spread to Ankara, Eskişehir, Bartın, and Zonguldak provinces as of 2022. [17] 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. [18] 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. [19] The Netherlands also reported their first outbreak on tomato crops, [20] as well as Greece, [21] Spain [22] and ToBRFV was reported from France in January 2020. [23] By February 2020 17 outbreaks had been detected in the Netherlands [24] and an additional 9 sites were infected in Spain [25] and the first outbreak on Capsicum annuum was detected in Italy. [26] In August 2021 the first positive case of ToBRFV was confirmed in Slovenia. [27] Department of Primary Industries and Regions South Australia (PIRSA) reported an outbreak in two farms [28] August 2024, prompting an Australian Tomato import ban by New Zealand [29]

ToBRFV is abundant in treated municipal wastewater effluent, and is being investigated as a surrogate that can be monitored, to verify removal of viruses by membrane filters (e.g. microfiltration, ultrafiltration, and membrane bioreactors) that are an important treatment in some water reuse facilities. ToBRFV can be monitored in wastewater effluent using the same qPCR technologies that are also used to monitor SARS-CoV-2 in wastewater effluent.

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, [15] but the virus could not be experimentally transmitted to this host in other studies. [30] It has also been detected on weed species. [6]

Symptoms in tomato vary based on the tomato variety and may be mild to severe. [31] 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 misshapen or turn yellow and are often unmarketable due to symptoms. [31]

On sweet peppers, symptoms include mosaic, discolouration and vein clearing on young leaves, browning of the stem and mosaic and distortion of fruits. [26]

Transmission

Different transmission means of tomato brown rugose fruit virus Plants-09-00623-g005.png
Different transmission means of tomato brown rugose fruit virus

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. [31] Seed transmission is suspected but has not yet been verified, [32] though it has been detected on tomato seed moving in trade. [24] The virus can also spread via plant propagation. [31] 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. [33]

Management

Several cultivars have been developed with resistance against ToBRV and are sold commercially. [34] As the virus is transmitted easily through mechanical means, hygiene best practise is essential to reduce impacts when outbreaks are detected. [31] 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. [35] The disinfectants Virkon S and Huwa-San are effective on most surfaces, but only after an hour of exposure. [35] Plastic trays can be soaked in hot water (90 °C (194 °F) for 5 minutes) to eliminate the virus, or at 70 °C (158 °F) for 5 minutes and then treated with Virkon. [35]

Related Research Articles

<i>Tobamovirus</i> Genus of viruses

Tobamovirus is a genus of positive-strand RNA viruses in the family Virgaviridae. Many plants, including tobacco, potato, tomato, and squash, serve as natural hosts. Diseases associated with this genus include: necrotic lesions on leaves. The name Tobamovirus comes from the host and symptoms of the first virus discovered.

Phytophthora citrophthora, also known as brown rot of citrus, is a soil borne oomycete that infects several economically important citrus crops. A diagnostic symptom of P. citrophthora is gummosis, wherein lesions around the base of the tree exude sap. Other common symptoms include dark longitudinal lesions forming at the soil line, a sour smell, and eventual cracking of the bark. Advanced symptoms include yellowing and necrosis of the tree canopy. Girdling action caused by the pathogen around the trunk can often cause the collapse of the tree. Resistant lemon varieties have been developed and their implementation has been effective at controlling the spread of the disease. Fruits that have been infected with P. citrophthora exhibit symptoms of brown rot characterized by a distinct odor. This disease is most active in the moderate temperatures of spring, fall, and winter months, opposite of most other Phytophthora species.

Alternaria japonica is a fungal plant pathogen. It is a cause of black spot disease in cruciferous plants. It is not a major source of crop loss, but is considered dangerous for plants during the seedling stage.

Pseudocercospora fuligena is a fungal plant pathogen infecting tomatoes. It is the cause of the fungal disease black leaf mold. The fungus was first described in the Philippines in 1938 and has since been reported in numerous countries throughout the tropics and subtropics. It was reported in the United States in 1974, initially in Florida, and has since been reported in non-tropical regions including Ohio and North Carolina.

<i>Phoma destructiva</i> Species of fungus

Phoma destructiva is a fungal plant pathogen infecting tomatoes and potatoes.

<i>Beet curly top virus</i> Species of virus

Beet curly top virus (BCTV) is a pathogenic plant virus of the family Geminiviridae, containing a single-stranded DNA. The family Geminiviridae consists of nine genera based on their host range, virus genome structure, and type of insect vector. BCTV is a Curtovirus affecting hundreds of plants. The only known vector is the beet leafhopper, which is native to the Western United States.

<i>Cucumber mosaic virus</i> Species of virus

Cucumber mosaic virus (CMV) is a plant pathogenic virus in the family Bromoviridae. This virus has a worldwide distribution and a very wide host range, having the reputation of the widest host range of any known plant virus. It can be transmitted from plant to plant both mechanically by sap and by aphids in a stylet-borne fashion. It can also be transmitted in seeds and by the parasitic weeds, Cuscuta sp. (dodder).

<i>Pepper mild mottle virus</i> Species of virus

Pepper mild mottle virus (PMMoV) is a plant pathogenic virus that occurs worldwide on species of field grown bell, hot and ornamental pepper species. It is caused by members of the plant virus genus Tobamovirus—otherwise known as the tobacco mosaic virus family. Tobamovirus are viruses that contain positive sense RNA genomes that infect plants. Symptoms of the disease vary depending on the cultivar. Typical symptoms include the chlorosis of leaves, stunting, and distorted and lumpy fruiting structures. The virus is spread by mechanical transmission and infected seeds. Avoidance is the best means of controlling the disease because once a plant is infected it cannot be treated. Only seeds that have been tested and treated for the pathogen should be planted.

<i>Soybean mosaic virus</i> Plant disease

Soybean mosaic virus (SMV) is a member of the plant virus genus Potyvirus. It infects mainly plants belonging to the family Fabaceae but has also been found infecting other economically important crops. SMV is the cause of soybean mosaic disease that occurs in all the soybean production areas of the world. Soybean is one of the most important sources of edible oil and proteins and pathogenic infections are responsible for annual yield losses of about $4 billion in the United States. Among these pathogens, SMV is the most important and prevalent viral pathogen in soybean production worldwide. It causes yield reductions of about 8% to 35%, but losses as high as 94% have been reported.

<i>Puccinia thaliae</i> Species of fungus

Puccinia thaliae is the causal agent of canna rust, a fungal disease of Canna. Symptoms include yellow to tan spots on the plant's leaves and stems. Initial disease symptoms will result in scattered sori, eventually covering the entirety of the leaf with coalescing postulates. Both leaf surfaces, although more predominant on the underside (abaxial) of the leaf, will show yellow to brownish spore-producing these pustulate structures, and these are the signs of the disease. Spots on the upper leaf-surface coalesce and turn to brown-to-black as the disease progresses. Infection spots will become necrotic with time, with small holes developing in older leaves. These infected leaves eventually become dry and prematurely fall.

<i>Orthotospovirus</i> Genus of viruses

Orthotospovirus is a genus of negative-strand RNA viruses, in the family Tospoviridae of the order Bunyavirales, which infects plants. Tospoviruses take their name from the species Tomato spotted wilt orthotospovirus (TSWV) which was discovered in Australia in 1919. TSWV remained the only known member of the family until the early 1990s when genetic characterisation of plant viruses became more common. There are now at least twenty species in the genus with more being discovered on a regular basis. Member viruses infect over eight hundred plant species from 82 different families.

High plains disease is a viral disease afflicting wheat and maize. It is caused by the negative-sense ssRNA virus High Plains wheat mosaic emaravirus. Symptoms are similar to Wheat streak mosaic virus, with leaf veins showing yellow flecks and streaks, followed by leaf margin purpling in maize. Depending on the timing of infection, stunting and death occur. Plants can be doubly infected with high plains virus and wheat streak mosaic virus.

<i>High Plains wheat mosaic emaravirus</i> Species of virus

High Plains wheat mosaic emaravirus (WMoV), or High Plains virus (HPV) or Maize red stripe virus (MRSV/MRStV) is the causative agent of High plains disease of maize and wheat. It is spread by wheat curl mite, Aceria tosichella, which also transmits Wheat streak mosaic virus. The mite's ability to transmit a number of different viruses to cereal crops make it an economically important agricultural pest. In late June 2017 this virus was first detected in Canada, in Alberta. The Alberta samples were 99% similar to those in the USA. As Wheat streak mosaic virus is already present in Alberta, and coinfection with these two causes even more severe damage, this could cause much higher yield losses.

Little cherry disease or LChD, sometimes referred to as little cherry, K & S little cherry or sour cherry decline, is a viral infectious disease that affects cherry trees, most notably sweet cherries and sour cherries . Little cherry disease should not be confused with cherry buckskin disease, which is caused by Phytoplasma. Note that both diseases are among the diseases referred to as cherry decline.

<i>Verticillium nonalfalfae</i> Species of fungus

Verticillium nonalfalfae is a soilborne fungus in the order Hypocreales. It causes verticillium wilt in some plant species, particularly Ailanthus altissima. The fungus produces a resting mycelium characterized by brown-pigmented hyphae. It is most closely related to V. dahliae and V. alfalfae.

Phytophthora hydropathica is an oomycete plant pathogen that is found in aquatic environments such as irrigation and river water. The pathogen was previously classified as P. drechsleri Dre II before being categorized as its own distinct species. P. hydropathica has been primarily found in association with ornamental plant nurseries. The pathogen has been isolated throughout the Southern United States, as well as internationally in Mexico, Italy, and Spain.

Papaya leaf curl virus(PaLCuV) is a DNA virus from the genus Begomovirus and the family Geminiviridae. PaLCuV causes severe disease in papaya (Carica papaya), but can sometimes infect other crops such as tobacco or tomato. It can be found in tropical and subtropical regions primarily in India, but closely related species have also been detected in countries such as China, Malaysia, Nigeria and South Korea. This virus is transmitted by an insect vector from the family Aleyrodidae and order Hemiptera, the whitefly Bemisia tabaci. PaLCuV has been responsible for several epidemics and causes severe economic losses. Because of the broad diversity of these viruses, their characterization and control remains difficult.

Cranberry fruit rot (CFR) is a disease complex of multiple fungal agents affecting the American cranberry. Cranberry fruit rot can be categorized into field rot and storage rot. The importance of field rot and fruit rot depends on how the cranberries will be processed after harvest. If cranberries are immediately processed after harvest, growers focus on preventing field rot while with fresh market cranberries, growers seek to prevent storage rot. There are 10-15 fungal pathogens known to cause cranberry fruit rot diseases, some active in only field rot, storage rot, or both. The majority of these fungal pathogens are ascomycetes, with the rest being deuteromycetes. There is no known bacterial pathogen that plays a role in CFR or any major disease on cranberry, potentially due to the low pH conditions on the cranberry fruit.

Tomato mottle mosaic virus is a Tobamovirus which infects Solanum lycopersicum. First detected in Mexico in 2013 from S. lycopersicum samples taken in 2009, ToMMV has since been found worldwide. In 2014, some S. lycopersicum samples from Florida in 2010 and 2012 and a Nicotiana tabacum 'Xanthi nc' sample were retested using an assay that distinguishes ToMMV from other Tobamoviruses, especially the closely related Tomato mosaic virus and Tobacco mosaic virus. These samples tested positive for ToMMV, indicating that the virus was widespread and had been for several years prior to when it was recognized.

Epicoccum sorghinum is an ascomycete fungus with known plant pathogenicity to sugarcane and rice, causing ring spot disease and leaf spot disease. This fungus is primarily known for its production of tenuazonic acid, which leads to complications with growth and causes the symptoms of leaf spot disease. Tenuazonic acid not only affects plant growth, but has recently been proven to impact human health due to its prevalence in food and beverages. It is widely dispersed, affecting multiple hosts in different countries. Although not a serious threat, Epicoccum sorghinum has been known to influence the sorghum grain-mold complex in ways which reduce crop yields, seed viability, and kernel weight. As a result of continuous phylogenetic and morphological discoveries relevant to Epicoccum sorghinum, this fungus has undergone a number of name changes.

References

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  13. ↑ 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.
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  17. ↑ Çelik, Ali; Coşkan, Sevgi; Morca, Ali Ferhan; Santosa, Adyatma Irawan; Koolivand, Davoud (28 November 2022). "Insight into Population Structure and Evolutionary Analysis of the Emerging Tomato Brown Rugose Fruit Virus". Plants. 11 (23): 3279. doi: 10.3390/plants11233279 . PMC   9738901 . PMID   36501319.
  18. ↑ 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. doi: 10.1094/PDIS-05-19-1045-PDN . ISSN   0191-2917.
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  23. ↑ EPPO (February 2020). "First report of tomato brown rugose fruit virus in France". EPPO. Retrieved 13 April 2020.
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  25. ↑ EPPO (February 2020). "Update on the situation of tomato brown rugose fruit virus in Spain". EPPO. Retrieved 13 April 2020.
  26. 1 2 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.
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  33. ↑ 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. Bibcode:2019PLoSO..1410871L. doi: 10.1371/journal.pone.0210871 . ISSN   1932-6203. PMC   6336271 . PMID   30653593.
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