EPPO Global Database

Tomato chlorosis virus(TOCV00)

EPPO Datasheet: Tomato chlorosis virus

Last updated: 2021-07-09

IDENTITY

Preferred name: Tomato chlorosis virus
Taxonomic position: Viruses and viroids: Riboviria: Closteroviridae: Crinivirus
Other scientific names: ToCV, Tomato chlorosis closterovirus, Tomato chlorosis crinivirus
view more common names online...
EPPO Categorization: A2 list
view more categorizations online...
EPPO Code: TOCV00

HOSTS 2021-07-09

ToCV has been found to infect 84 dicotyledonous plant species belonging to 25 botanical families, including economically important crops (Fiallo-Olivé et al., 2019). ToCV naturally infects tomato (Solanum lycopersicum) (Wisler et al., 1998a) pepper (Capsicum annuum) (Lozano et al., 2004) and potato (Solanum tuberosum) (Fortes & Navas-Castillo, 2012). Transmission experiments have shown the presence of ToCV in potato tubers from infected plants, which subsequently produced infected plants themselves, and that this species served as virus source for tomato infection via B. tabaci transmission (Fortes, Navas-Castillo, 2012). The studies showed that tomato is a better source of inoculum than potato (Mituti et al., 2018). In Taiwan, Zinnia was also reported as a host (Tsai et al., 2004). The weeds Datura stramonium and Solanum nigrum have been identified as hosts in Portugal. The experimental host range includes species in the families Aizoaceae, Amaranthaceae, Apocynaceae, Asteraceae, Chenopodiaceae, Plumbaginaceae, Solanaceae. ToCV infects a wide range of weeds, but information of the importance of these weeds to the occurrence of epidemics of ToCV is still lacking, but these plants likely serve as reservoirs of ToCV in the absence of susceptible cultivated hosts (Souza et al., 2020).

Host list: Abelmoschus esculentus, Abutilon theophrasti, Alcea rosea, Alternanthera philoxeroides, Amaranthus graecizans subsp. sylvestris, Amaranthus retroflexus, Amaranthus viridis, Ammi majus, Anadendrum affine, Anagallis foemina, Aralia nudicaulis, Bauhinia variegata, Bidens bipinnata, Brassica oleracea var. capitata, Brassica, Calotropis procera, Capsicum annuum, Cardamine flexuosa, Cerastium glomeratum, Cestrum elegans, Cestrum nocturnum, Chenopodiastrum murale, Chenopodium album, Chenopodium opulifolium, Cirsium arvense, Codiaeum variegatum, Convolvulus arvensis, Conyza sp., Corchorus olitorius, Coriandrum sativum, Cucumis melo, Cucumis sativus, Cucurbita moschata, Datura stramonium, Eranthemum pulchellum, Erigeron annuus, Erigeron canadensis, Eruca vesicaria, Euphorbia heterophylla, Ficus benjamina, Ficus carica, Fumaria officinalis, Galium aparine, Glebionis coronaria, Glycine max, Gomphrena globosa, Gossypium barbadense, Gossypium hirsutum, Heliotropium lasiocarpum, Hibiscus cannabinus, Hibiscus rosa-sinensis, Ipomoea batatas, Ipomoea cholulensis, Ipomoea coccinea, Ipomoea hederacea, Jatropha integerrima, Lactuca saligna, Lactuca sativa, Lactuca serriola, Leucaena leucocephala, Luffa aegyptiaca, Malva parviflora, Malva sylvestris, Mazus pumilus, Metaplexis japonica, Momordica charantia, Morus alba, Nicandra physalodes, Nicotiana benthamiana, Nicotiana tabacum, Oxalis pes-caprae, Pelargonium auritum, Pentas lanceolata, Phaseolus vulgaris, Physalis angulata, Physalis peruviana, Physalis philadelphica, Physalis pubescens, Phytolacca americana, Phytolacca icosandra, Plantago major, Portulaca oleracea, Raphanus raphanistrum, Ricinus communis, Ruta chalepensis, Schefflera arboricola, Sisymbrium irio, Solanum aethiopicum, Solanum americanum, Solanum arcanum, Solanum chilense, Solanum chmielewskii, Solanum corneliomulleri, Solanum elaeagnifolium, Solanum galapagense, Solanum habrochaites, Solanum huaylasense, Solanum jamaicense, Solanum lycopersicum, Solanum mammosum, Solanum melongena, Solanum neorickii, Solanum nigrescens, Solanum nigrum, Solanum paniculatum, Solanum pennellii, Solanum peruvianum, Solanum pimpinellifolium, Solanum scuticum, Solanum sessiliflorum, Solanum sisymbriifolium, Solanum stramoniifolium, Solanum subinerme, Solanum tuberosum, Solanum velleum, Sonchus asper, Sonchus oleraceus, Stellaria media, Tectona grandis, Tribulus terrestris, Trigonotis peduncularis, Veronica hederifolia, Vicia faba, Vicia sativa subsp. nigra, Vicia tetrasperma, Vigna unguiculata, Withania somnifera, Youngia japonica, Zinnia

GEOGRAPHICAL DISTRIBUTION 2021-07-09

ToCV was first identified in North-Central Florida (USA) in 1996 in the greenhouse on tomato plants with symptom yellow leaf disorder. This symptom was previously thought to be not virus-related but physiological or nutritional disturbances and has been reported in tomato plants since 1989. Shortly after this the symptoms of ToCV were detected in Spain. Since then, the virus has been detected infecting tomato in many areas around the world (Fiallo-Olivé et al., 2019).

EPPO Region: Cyprus, France (mainland), Greece (mainland, Kriti), Hungary, Israel, Italy (mainland, Sardegna, Sicilia), Jordan, Morocco, Netherlands, Portugal (mainland), Spain (mainland, Islas Baleares, Islas Canárias), Tunisia, Turkey
Africa: Egypt, Kenya, Mauritius, Mayotte, Morocco, Nigeria, Reunion, South Africa, Sudan, Tunisia
Asia: China (Beijing, Hebei, Jiangsu, Shandong, Yunnan), Indonesia (Java), Israel, Japan (Honshu), Jordan, Korea, Republic, Lebanon, Pakistan, Saudi Arabia, Taiwan
North America: Mexico, United States of America (Colorado, Connecticut, Florida, Georgia, Louisiana, New York, Virginia)
Central America and Caribbean: Costa Rica, Cuba, Puerto Rico
South America: Brazil (Bahia, Distrito Federal, Espirito Santo, Goias, Minas Gerais, Parana, Rio de Janeiro, Rio Grande do Sul, Sao Paulo), Uruguay

BIOLOGY 2021-07-09

ToCV is one of two criniviruses that are transmitted locally by whiteflies of the genera Bemisia and Trialeurodes. Since 1998 the number of studies have been carried out (Navas-Castillo et al., 2000; Wisler et al., 1998b, Shi et al., 2018; Wintermantel, Wisler, 2006), that showed that the virus is transmitted by several species of the whitefly: B. tabaci, T. vaporariorum, and T. abutiloneus. The efficiency of transmission differs among whitefly species and is associated to differences in virus acquisition and accumulation rate (Fiallo-Olivé et al., 2019) and differs following the order B. tabaci MED> B. tabaci MEAM1 ≈ T. abutiloneus > B. tabaci NW > T. vaporariorum (Shi et al., 2018; Wintermantel, Wisler, 2006). T. vaporariorum is common in glasshouses throughout the EPPO region and is also found outdoors in the summer months. B. tabaci, which is on the EPPO A2 List (EPPO/CABI, 1997), is present in glasshouses in many EPPO countries. It is also found in the field in Southern Europe in the summer months. T. abutiloneus is found in the USA and Cuba (CABI, 2000). Older tomato crops are probably the most important sources of ToCV inoculum to tomato crops (Souza et al., 2020). ToCV is unlikely to be seedborne (www.cabi.org, 2021).

DETECTION AND IDENTIFICATION 2021-07-09

Symptoms

Tomato plants infected with ToCV show an irregular chlorotic mottle that develops first on lower leaves and gradually advances toward the growing point. In the initial stage of the infection, chlorotic areas are frequently polygonal in shape, and are limited by main veins (Fiallo-Olivé et al., 2019). In advanced stages, interveinal yellow areas on leaves also develop red and brown necrotic flecks. No obvious symptoms develop on fruit and flowers, but fruit ripening is affected and flower abortion occurs (Fortes et al., 2012), fruit size and numbers are reduced due to a loss of photosynthetic area. Significant yield losses occur as a result. Other symptoms include rolling of lower leaves and thickened crispy leaves, while the upper leaf canopy appears normal. Symptoms of ToCV are very similar to those of Tomato infectious chlorosis virus (TICV) (Wisler et al., 1998a, 1998b). 

N. physalodes, C. coronarium, G. globosa and N. physalodes infected with ToCV have no obvious symptoms of viral infection, whereas infected A. viridis, N. benthamiana, P. angulata, P. pubescens, S. americanum exhibit symptoms of interveinal chlorosis, D. stramonium and N. tabacum cv. TNN develop chlorotic spots (Souza et al., 2020). 

Symptoms caused by ToCV, are easily attributed to other causes, such as physiological or nutritional disorders, or phytotoxicity of plant protection products.

Morphology

ToCV particles are filamentous and slightly flexuous with a normal length of about 850 nm (Wisler et al., 1996). Virions encapsidate two molecules of positive-sense and single-stranded RNA denoted RNA-1 and RNA-2, whose complete nucleotide sequence has been determined (Martelli et al., 2008). Cross-banding patterns seen are typical of members of the family Closteroviridae (Wisler et al., 1998b). ToCV RNAs 1 and 2 are 8595nt and 8247nt, respectively. RNA1 contains four open reading frames (ORFs), which encode proteins for replication. RNA2 codes nine ORFs comprising theHSP70 homolog, a 59 kDa protein, CP, and CPm, that express proteins involved in viral encapsidation, movement and broad vector transmissibility of the virus (Martelli et al., 2008, Lee et al., 2018).

Detection and inspection methods

Fully developed leaves, showing mild interveinal yellowing, should be sampled (EPPO, 2013). For bioassay using whitefly, efficient transmission of ToCV is obtained by allowing adult insects (T. vaporariorum) a 48 h acquisition access period on samples and a 48 h inoculation access period on test plants of tomato, Nicotiana benthamiana or Physalis wrightii. Subsequently, the positive reaction on the indicator plants need to be assigned to the responsible virus using suitable identification tests (EPPO, 2013). ToCV can be distinguished from TICV by symptoms on the indicator plants Nicotiana benthamiana and N. clevelandii. Whereas both species show interveinal yellowing when infected with either virus, only TICV causes necrotic flecking in these hosts (Wisler et al., 1998b). Antisera to ToCV have been produced mainly for research purposes and may be used for screening tests for ToCV (EPPO, 2013).

Conventional RT-PCR and real-time RT-PCR can be used for both detection and identification. In addition, sequence analysis of amplicons can be used for identification (EPPO, 2013). Several real-time RT-PCR tests have been developed to test for ToCV. Protocol based on the best ToCV primers and ToCV probes by Morris et al. (2006), were validated in a test performance study involving five laboratories (EPPO, 2013).

Nucleic acid hybridization has proved to be reliable and sensitive in particular for mass screening of samples but this is not commonly used, and for routine diagnosis the method can be replaced by RT-PCR tests (EPPO, 2013).

Guidance for detection and identification of this virus are given in the EPPO Diagnostic Protocol PM 7/118 (1) Tomato chlorosis virus and Tomato infectious chlorosis virus (EPPO, 2013).

PATHWAYS FOR MOVEMENT 2021-07-09

In international trade, ToCV may be carried by infected plants for planting. The high number of natural plant hosts and ready transmission by several whitefly species have contributed to emergence of ToCV worldwide. In Spain, outbreaks of ToCV have been associated with the main spread of B. tabaci populations during the summer months (Navas-Castillo et al., 2000). Field investigations conducted in Brazil on tomato have shown that the main dispersal mechanism of the disease caused by ToCV is primary spread, with epidemics being caused by successive influxes of viruliferous whiteflies (Macedo et al., 2019). Viruliferous whiteflies could be carried long distances on plants of hosts or non-hosts.

PEST SIGNIFICANCE 2021-07-09

Economic impact

Criniviruses emerged as a major problem for world agriculture at the end of the twentieth century with the establishment of some of their whitefly vectors in temperate climate (Fiallo-Olivé et al., 2019).

There are no estimates of yield losses, although since ToСV discovery, the virus represents a serious problem for tomato production in many parts of the world (Martelli et al., 2008). ToCV is very important in tomatoes, in peppers and potatoes (Mituti T. et al., 2018). New cases of virus detection on these crops in new regions are noted every year. Outbreaks in tomato fields in Málaga and Almería provinces in Southern Spain in 1998 and 1999 were associated with high populations of B. tabaci and were described as epidemics. Incidences of over 30% symptomatic plants in individual fields were frequent (Navas-Castillo & Moriones, 2000; Navas-Castillo et al., 2000). Hanafi (2002) reports that ToCV caused significant damage in tomato glasshouses in Spain. The severity of symptoms and damage vary according to the cultivar.

It is known that with a mixed virus infection ToCV and Tomato spotted wilt virus (TSWV) synergism is observed, that leads to the rapid death of plants (Fiallo-Olivé et al., 2019).

Control

As with other virus diseases, once a plant is infected with a virus there is no cure, and measures should be taken to eradicate sources of inoculum and eliminate the presence of vectors to minimise the risk of further transmission therefore, control of whitefly vectors is key.

Regarding chemical control, B. tabaci appears to develop resistance to all groups of insecticides. A rotation of insecticides that offer no cross resistance must therefore be used to control B. tabaci infestations. The biocontrol agent Encarsia formosa (parasitic wasp) is used to control T. vaporariorum, but it is less efficient against B. tabaci. Repeated releases of large numbers of E. formosa against B. tabaci are necessary if eradication is required. The predatory beetle Delphastus pusillus is very effective against B. tabaci (MAFF, 2000). Roguing of severely infested plants reduces whitefly populations.

Using containment structures, for example adding nets to the greenhouse ventilation windows limiting the access of the whitefly vectors to the plants, results in an efficient protection of the crop from ToCV infection (Fiallo-Olivé et al., 2019).

Tomato seedlings for transplanting should be kept free from infection. There are no resistant tomato cultivars as no resistance to ToCV has yet been identified in tomato. No differences in the incidence of yellowing due to ToCV in fields containing different cultivars of tomato were observed in southern Spain (Navas-Castillo et al., 2000).

Eradication of isolated outbreaks in glasshouse-grown tomatoes can probably be achieved by destruction of affected hosts and of the vector(s). However, it is difficult to envisage that eradication could be achieved for outbreaks in the field in Southern Europe. Weed hosts may act as reservoirs for ToCV.

Phytosanitary risk

ToCV presents a significant risk of further spread in the EPPO region. The risk to the tomato industry is high since T. vaporariorum, a known vector, is present and widespread in glasshouses and in the field in Northern and Southern Europe in summer (CABI, 2000). In addition, B. tabaci, another known vector of ToCV, occurs in many EPPO countries. This whitefly is found on outdoor crops in Southern Europe in summer and in glasshouses in Northern Europe. It is frequently intercepted on plants and plant products. The recent detection of ToCV in Northern Europe (in the Netherlands and the United Kingdom) and in Africa (in Nigeria, Kenya, Egypt) raises serious concerns because the climatic conditions in these countries were not thought to be conducive to the transmission of the virus. ToCV would be expected to cause considerable damage to glasshouse tomato crops in EPPO countries. Outdoor crops in Mediterranean countries are also at risk.

PHYTOSANITARY MEASURES 2021-07-09

At present, there are no specific measures against ToCV in Europe and in particular there are no restrictions on the movement of tomato seedlings from areas where the disease occurs. Possible measures would be equivalent to those proposed for CVYV (EPPO, 2005).

REFERENCES 2021-07-09

CABI (2000) Crop Protection Compendium, Global Module, 2nd edn. CAB International CD-ROM Database. CAB International, Wallingford (GB).

EPPO (2005) Data sheets on quarantine pests – Cucumber vein yellowing ipomovirus. EPPO Bulletin 35, 419–421.

EPPO (2013) PM 7/118 (1) Tomato chlorosis virus and Tomato infectious chlorosis virus. EPPO Bulletin 43, 462–470.

EPPO/CABI (1997) Bemisia tabaci. In: Quarantine Pests for Europe, 2nd edn, pp. 121–127. CAB International, Wallingford (GB).

Fiallo-Olivé E, Navas-Castillo J (2019) Tomato chlorosis virus, an emergent plant virus still expanding its geographical and host ranges. MolecularPlant Pathology 20(9), 1307-1320. https://doi.org/10.1111/mpp.12847

Fortes IM, Navas-Castillo J (2012) Potato, an experimental and natural host of the crinivirus Tomato chlorosis virus.  Plant Pathology 134, 81–86.

García-Cano E, Navas-Castillo J, Moriones E, Fernández-Muñoz R (2010) Resistance to Tomato chlorosis virus in wild tomato species that impair virus accumulation and disease symptom expression. Phytopathology 100, 582–592.

Hanafi A (2002) Invasive species: a real challenge to IPM in the Mediterranean region. European Whitefly Studies Network Newsletter 13, p. 4. John Innes Centre, Norwich (GB).

Kil E-J, Lee J-J, Cho S, Auh C-K, Kim D, Lee K-Y, Kim M-K, Choi H-S, Kim C-S, Lee S (2015) Identification of natural weed hosts of Tomato chlorosis virus in Korea by RT-PCR with root tissues. European Journal of Plant Pathology 142, 419–426.

Lee Y-J, Kil E-J, Kwak H-R, Kim M, Seo J-K, Lee S, Choi H-S (2018) Phylogenetic characterization of Tomato chlorosis virus population in Korea: evidence of reassortment between isolates from different origins. Plant Pathology 34(3), 199–207. https://doi.org/10.5423/PPJ.OA.10.2017.0220 [accessed on 4 May 2021]

Liu Wei, Shi XiaoBin, Tang Xin, Zhang Yu, Zhang DeYong, Zhou XuGuo, Liu Yong (2018) Molecular identification of Tomato chlorosis virus and Tomato yellow leaf curl virus in Yunnan Province. Acta Horticulturae Sinica 45(3),552-560.

Lozano G, Moriones E, Navas-Castillo J (2004) First report of sweet pepper (Capsicum annuum) as a natural host plant for Tomato chlorosis virus. Plant Disease 88, 224.

Macedo MA, Inoue‐Nagata AK, Silva TNZ, Freitas DMS, Rezende JAM, Michereff Filho M, Nascimento AR, Lourenção AL, Bergamin Filho A (2019) Temporal and spatial progress of the diseases caused by the crinivirus Tomato chlorosis virus and the begomovirus Tomato severe rugose virus in tomatoes in Brazil. Plant Pathology 68, 72–84.

MAFF (2000) Current recommendations for eradication and containment. PHSI Handbook of Instructions. MAFF, London (GB).

Martelli GP, Gallitelli D (2008) Emerging and Reemerging Virus Diseases of Plants. Encyclopedia of Virology (Third Edition), Editor(s): Brian W.J. Mahy, Marc H.V. Van Regenmortel. Academic Press, 90.

Mituti T, Molina JPE, Rezende JAM (2018) Bioassays on the role of tomato, potato and sweet pepper as sources of Tomato chlorosis virus transmitted by Bemisia tabaci MEAM1. European Journal of Plant Pathology 152, 613–619.

Morris E, Steel E, Smith P, Boonham N, Spence N, Barker I (2006) Host range studies for Tomato chlorosis virus and Cucumber vein yellowing virus transmitted by Bemisia tabaci (Gennadius). European Journal of Plant Pathology 114, 265–273.

Navas-Castillo J, Camero R, Bueno M, Moriones E (2000) Severe yellowing outbreaks in tomato in Spain associated with infections of Tomato chlorosis virus. Plant Disease 84, 835–837.

Navas-Castillo J, Moriones E (2000) ToCV: a new threat to European horticulture. In: European Whitefly Studies Network Newsletter 3. John Innes Centre, Norwich (GB).

Trenado HP, Fortes IM, Louro D, Navas-Castillo J (2007) Physalis ixocarpa and P. peruviana, new natural hosts of Tomato chlorosis virus. European Journal of Plant Pathology 118, 193–196.

Tsai WS, Shih SL, Green SK, Hanson P & Liu HY (2004) First report of the occurrence of Tomato chlorosis virus and Tomato infectious chlorosis virus in Taiwan. Plant Disease 88, 311.

Shi X, Tang X, Zhang X, Zhang D, Li F, Yan F, Zhang Y, Zhou X, Liu Y (2018) Transmission efficiency, preference and behavior of Bemisia tabaci MEAM1 and MED under the influence of Tomato chlorosis virus. Frontiers in Plant Science 8, 2271.

Souza TA, Macedo MA, Albuquerque LC (2020) Host range and natural infection of tomato chlorosis virus in weeds collected in Central Brazil. Trop. plant pathology 45,84–90 https://doi.org/10.1007/s40858-019-00323-x [accessed on 4 May 2021]

Wintermantel WM, Wisler GC (2006) Vector specificity, host range, and genetic diversity of Tomato chlorosis virus. Plant Disease 90, 814–819.

Wisler GC, Duffus JE, Liu HY, Li RH (1996) A new whitefly-transmitted virus infecting tomato from Florida. Phytopathology 86 (Suppl.): S71.

Wisler GC, Duffus JE, Liu HY & Li RH (1998a) Ecology and epidemiology of whitefly-transmitted closteroviruses. Plant Disease 82, 270–280.

Wisler GC, Li RH, Liu HY, Lowry DS & Duffus JE (1998b) Tomato chlorosis virus: a new whitefly-transmitted, phloem-limited, bipartite closterovirus of tomato. Phytopathology 88, 402–409.


CABI resources used when preparing this datasheet

CABI. Crop protection compendium. https://www.cabi.org/isc/datasheet/54069#todistributionDatabaseTable [accessed on 4 May 2021]

ACKNOWLEDGEMENTS 2021-07-09

This datasheet was extensively revised in 2021 by Elena Karimova and Yuri Shneyder from All-Russian Plant Quarantine Center. Their valuable contribution is gratefully acknowledged.

How to cite this datasheet?

EPPO (2021) Tomato chlorosis virus. EPPO datasheets on pests recommended for regulation. Available online. https://gd.eppo.int

Datasheet history 2021-07-09

This datasheet was first published in the EPPO Bulletin in 2005 and revised in 2021. It is now maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.

EPPO (2005) Tomato chlorosis virus. Datasheets on quarantine pests. EPPO Bulletin 35(3), 439-441. https://doi.org/10.1111/j.1365-2338.2005.00888.x