Tomato infectious chlorosis virus

Abstract

EPPO BulletinVolume 39, Issue 1 p. 62-64 Free Access Tomato infectious chlorosis virus First published: 11 March 2009 https://doi.org/10.1111/j.1365-2338.2009.02239.xCitations: 2 European and Mediterranean Plant Protection Organization Organisation Européenne et Méditerranéenne pour la Protection des Plantes AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Identity Name: Tomato infectious chlorosis virus Synonym: Tomato infectious chlorosis crinivirus (TICV) Taxonomic position: Virus, Closteroviridae, Crinivirus Common name of the disease: Infectious chlorosis of tomato EPPO code: TICV00 Phytosanitary categorization: EPPO A2 list no. 348. Hosts Lycopersicon esculentum (tomato) is the major host of TICV. The following cultivated plants have also been recorded as natural hosts of TICV in California (US) (Wisler et al., 1998a): Lactuca sativa (lettuce), Physalis ixocarpa (tomatillo), Cynara scolymus (artichoke), Petunia hybrida (petunia), Ranunculus sp., Callistephus chinensis (China aster). Zinnia elegans (zinnia) has been found to be a natural host in Taiwan, but not apparently tomato (Tsai et al., 2004). In Italy, tomato and artichoke have been identified as crop hosts (Caciagli, 2001), but in Spain only tomato (Font et al., 2002). The same authors have noted the weeds Picris echioides, Nicotiana glauca and Cynara cardunculus as natural hosts in California, Chenopodium album and Chenopodium murale in Spain. Species recorded as experimentally susceptible by Duffus et al. (1996) were Chenopodium capitatum, C. murale (Chenopodiaceae), C. cardunculus, C. scolymus, L. sativa, P. echioides, Senecio vulgaris, Sonchus oleraceus, Z. elegans (Asteraceae), Capsella bursa-pastoris (Brassicaceae), Erodium cicutarium, Geranium dissectum (Geraniaceae), Trifolium subterraneum (Fabaceae), Anoda cristata (Malvaceae), L. esculentum, Nicotiana benthamiana, Nicotiana clevelandii, P. hybrida, Physalis alkekengi, Physalis floridana, P. ixocarpa, Physalis wrightii, Solanum tuberosum (Solanaceae), Conium maculatum (Apiaceae). Many other species were tested and found not to be susceptible. Geographical distribution EPPO region: Greece (Dovas et al., 2002); Italy (Calabria, Campania, Lazio, Liguria, Sardegna) (Wisler et al., 1998a; Caciagli, 2001; Vaira et al., 2002; Parrella & Scassillo, 2006); Jordan (Anfoka & Abhary, 2007); Spain (Castellón and Alicante provinces in Comunidad Valenciana; Murcia) (Font et al., 2002, 2003, 2004). In 2003, TICV was detected in two tomato samples collected near Nice, but the virus was not considered as established in France (Dalmon et al., 2005). Asia: Indonesia (Verhoeven et al., 2003); Japan (Hartono et al., 2003); Jordan (Anfoka and Abhary, 2007); Taiwan (Tsai et al., 2004). North America: USA (California, North Carolina) (Wisler et al., 1998a). EU: Greece, Italy, Spain. Biology TICV is found in both field and glasshouse crops of tomato. It is transmitted by the whitefly Trialeurodes vaporariorum. In experiments, the virus was acquired by T. vaporariorum after feeding for 1 h, but was transmitted with greater efficiency after longer feeding periods. Similarly, T. vaporariorum could transmit TICV to healthy plants after feeding for 1 hour, but efficiency of transmission increased after longer feeding times. TICV was not found to be transmitted by Bemisia tabaci, Trialeurodes abutilonea or Myzus persicae (Duffus et al., 1996). TICV has been detected in various weeds (see Hosts) and these may serve as a reservoir of inoculum. Detection and identification Symptoms Interveinal yellowing, necrosis and yield reduction are symptoms of infected tomato plants in the field. In inoculated plants, the first indication of infection is a bright interveinal yellowing symptom on the older leaves. As the disease progresses, the yellowing develops acropetally and the leaves thicken, become brittle and roll. Bronzing and necrosis of older leaves is accompanied by a decline in vigour and a reduction in fruit yield (Duffus et al., 1996). These symptoms are very similar to those caused by Tomato chlorosis virus (ToCV) (Wisler et al., 1998a) (EPPO A2 list no. 323). Symptoms in other crop hosts and weeds are reported to be similar. Severe yellowing and/or reddening symptoms, stunting rolling and brittleness have been noted (Duffus et al., 1996). Morphology TICV has flexuous, filamentous particles of variable lengths. Measurements of over 200 particles indicated that the average length was in the 800–850 nm range with some in the 1550–1600 nm range. Particles were estimated to be 12 nm wide. Sap from TICV infected leaves of Nicotiana clevelandii contained long flexuous rod-shaped particles with an average length of 850–900 nm (Duffus et al., 1996). Detection and inspection methods Polyclonal antibodies have been produced against TICV (Duffus et al., 1996). TICV-specific probes have also been used for diagnosis (Tian et al., 1996; Wisler et al., 1998b). Methods used in a comparison of diagnostics have been indirect ELISA, Western blot, dot-blot hybridization and RT-PCR assays. RT-PCR was found to be 100-fold more sensitive than ELISA, Western blot and dot-blot hybridization assays. The highest concentrations of TICV in infected plants were found to be in the young tomato leaves just before the onset of yellowing (Li et al., 1998). TICV can also be detected by vector transmission to indicator plants but is not transmitted mechanically. It can be distinguished from ToCV by symptoms on the indicator plants N. 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). TICV induces cytoplasmic vesicles characteristic of closterovirus infection in the phloem of infected plants (Li et al., 1998). Pathways for movement Over short distances, TICV can be carried by its vector T. vaporariorum. Over longer distances and in international trade, it can be carried in young plants for planting of tomato, and possibly other crop hosts which are traded in this form. These plants may also carry viruliferous whiteflies. Like almost all viruses in the Closteroviridae, TICV is unlikely to be seed-borne. Pest significance Economic impact When TICV was first found in the Irvine area of Orange County, California (US) in 1993, symptoms of the disease affected virtually 100% of tomato plants in every field. The disease was associated with a high incidence of T. vaporariorum (Duffus et al., 1996). In one season in Orange County, growers suffered 2 million USD in losses (Wisler et al., 1998a). Losses by some growers have been estimated to be 20–50%. However, TICV is now described as generally causing only minor losses. In Liguria (IT), TICV was found in back-garden tomato crops at the end of the growing season in 1995 and 1997, but damage was not very high. Incidence was associated with high populations of T. vaporariorum. Although TICV has also been reported in artichokes in the same area (Caciagli, 2001), the pathogen is not regarded as a serious problem on this crop. Tomato is not grown commercially on a year round basis in Liguria, there is a host-free period in the winter and populations of T. vaporariorum are slow to build up in the summer after being reduced significantly in open fields during the winter. These factors are believed to have diminished the impact TICV has on the tomato industry in this locality. More recently, TICV has been found in tomato in Lazio, Campania and Sardegna. Yellowing and reddening leaf symptoms have been reported to be severe and widespread. Plants were said to be less vigorous, with fruits that sometimes showed delayed ripening. TICV was described as a severe threat to tomato crops in Europe (Vaira et al., 2002). In Greece, 80–100% infection incidence was reported in some glasshouse tomato crops (Dovas et al., 2002). Control Control of TICV is centred on the control of T. vaporariorum, its whitefly vector. It is particularly important to protect young plants for transplanting. Many insecticides give some control of T. vaporariorum (Heungens & Buysse, 1991), but strains of T. vaporariorum resistant to one or other of them have become established. Imidacloprid, fenpropathrin, bifenthrin (Zhu & Ju, 1990), buprofezin (Stenseth & Singh, 1990), deltamethrin, fenvalerate, dimethoate, endosulfan, methamidophos and pymetrozine are all currently used in many countries for whitefly control, dependent on resistance levels. Most insecticides used are only effective against adults, so that repeated treatments at 3–5-day intervals are necessary for several weeks before control can be achieved. Biological control has been widely used against T. vaporariorum in glasshouses, especially since the development of insecticide-resistant whiteflies. It is chiefly based on the chalcid wasp Encarsia formosa (Osborne & Landa, 1992), and gives very successful control if the parasite is established on plants when natural infestations are minor. Other biological control agents used for pest control in glasshouses (the predatory beetle Delphastus pusillus and the lacewings Chrysoperla spp.) also consume whiteflies. It is important to choose insecticides and methods of application in glasshouses that are not damaging to biological control agents (Hayashi, 1996). The fungal pathogen Verticillium lecanii attacks whiteflies and thrips and can be a useful control agent in situations where the crop is grown under high humidity conditions (Masuda & Kikuchi, 1993). The fungus attacks young as well as adults, taking about 1–2 weeks to develop. Commercial preparations are available (Ravensberg et al., 1990, 1994). Microbial insecticides based on the entomopathogenic fungus Paecilomyces fumosoroseus have also been used for the control of T. vaporariorum (Sterk et al., 1996). Cultural measures may also be used to reduce and delay initial infestation of the crop. It is important, for glasshouse tomatoes, to ensure that young plants are not infested with T. vaporariorum before being taken into the glasshouse. A suitable insecticide can be applied as a routine precaution. Ensuring a crop-free period for some time during the year may break the cycle of the vector. T. vaporariorum can survive on weeds, in and around glasshouses or in the field, so adequate weed control reduces the risk that crops become infested with the vector of TICV. There are currently no commercial cultivars of tomato or other host species with TICV resistance. Phytosanitary risk TICV is absent from most of the EPPO region. It causes a serious disease of tomato crops under glass or in the field. Tomato is among the most important vegetable crops of the EPPO region, grown in and out of doors in the south, and in glasshouses in the north. Other hosts (lettuce, artichoke) are less affected by the disease, but are also of considerable economic importance. The vector of TICV, T. vaporariorum, is a very widespread pest of glasshouse crops in the EPPO region and also occurs on field crops in the summer months. The possibility thus exists that TICV can establish and spread practically throughout the EPPO region. Where TICV already occurs in the EPPO region (Greece, Italy, Jordan, Spain), severe symptoms and high incidences have been reported in some tomato crops. However, trials to determine yield reduction or quality losses have not yet been reported, so no figure can be put on the potential of TICV to cause damage. Spread of the pest into new areas within the EPPO region is most likely to occur with young plants of tomato, but natural spread with the vector is also possible over shorter distances. Conditions thus exist which may allow the existing infestations to be contained. Phytosanitary measures TICV was added in 2007 to the EPPO A2 action list, and endangered EPPO member countries are thus recommended to regulate it as a quarantine pest. Suitable measures would be to require that young tomato plants for planting should be produced in a crop or place of production free from the pest, under conditions which exclude the vector. Eradication of isolated outbreaks in glasshouse-grown tomatoes could be achieved by destruction of affected hosts and of the vector T. vaporariarum. Acknowledgement This datasheet was prepared by Dr I M Smith (former Director General of EPPO). References Anfoka GH & Abhary MK (2007) Occurrence of Tomato infectious chlorosis virus (TICV) in Jordan. Bulletin OEPP/EPPO Bulletin 37, 186– 190. Wiley Online LibraryGoogle Scholar Caciagli PC (2001) Whitefly-borne viruses in continental Europe. In: Virus-Insect-Plant Interactions ( Ed. Harris KF, Smith OP & Duffus JE). Academic Press, New York (US), pp. 279– 292. CrossrefGoogle Scholar Dalmon A, Boyer S, Cailly M, Girard M, Lecoq H, Desbiez C et al . (2005) First report of Tomato chlorosis virus and Tomato infectious chlorosis virus in tomato crops in France. Plant Disease 89, 1242. CrossrefWeb of Science®Google Scholar Dovas CI, Katis NI & Avgelis AD (2002) Multiplex detection of criniviruses associated with epidemics of a yellowing disease of tomato in Greece. Plant Disease 86, 1345– 1349. CrossrefCASPubMedWeb of Science®Google Scholar Duffus JE, Liu HY & Wisler GC (1996) Tomato infectious chlorosis virus – a new clostero-like virus transmitted by Trialeurodes vaporariorum. European Journal of Plant Pathology 102, 219– 226. CrossrefWeb of Science®Google Scholar Font MI, Juárez M, Martínez O & Jordá C (2004) Current status and newly discovered natural hosts of Tomato infectious chlorosis virus and Tomato chlorosis virus in Spain. Plant Disease 88, 82CrossrefCASPubMedWeb of Science®Google Scholar Font MI, Martínez-Culebras P, Jordá MC, Louro D, Vaira AM & Accotto GP (2002) First report of Tomato infectious chlorosis virus in Spain. Plant Disease 86, 696. CrossrefGoogle Scholar Font MI, Vaira AM, Accotto GP, Lacasa A, Serra J, Gomila J et al . (2003) Yellowing of tomato crops associated with Tomato chlorosis virus (ToCV) and Tomato infectious chlorosis virus (TICV) in Spain. Boletín de Sanidad Vegetal, Plagas 29, 109– 121. Google Scholar Hartono S, Natsuki T, Sayama H, Atarashi H & Okuda S (2003) Yellowing disease of tomatoes caused by Tomato infectious chlorosis virus newly recognized in Japan. Journal of General Plant Pathology 69, 61– 64. CrossrefCASGoogle Scholar Hayashi H (1996) Side effects of pesticides on Encarsia formosa. Bulletin of the Hiroshima Prefectural Agriculture Research Center 64, 34– 43. Google Scholar Heungens A & Buysse G (1991) Control of the greenhouse whitefly, Trialeurodes vaporariorum, in azalea culture with buprofezin and methamidophos. Mededelingen van de Faculteit Landbouwwetenschappen, Rijksuniversiteit Gent, 56, 1211– 1215. CASGoogle Scholar Li RH, Wisler GC, Liu HY & Duffus JE (1998) Comparison of diagnostic techniques for detecting tomato infectious chlorosis virus. Plant Disease 82, 84– 88. CrossrefWeb of Science®Google Scholar Masuda T & Kikuchi O (1993) Control of whitefly, Trialeurodes vaporariorum, by a Verticillium lecanii preparation. Annual Report of the Society of Plant Protection of North Japan 44, 191– 193. Google Scholar Osborne LS & Landa Z (1992) Biological control of whiteflies with entomopathogenic fungi. Florida Entomologist 75, 456– 471. CrossrefWeb of Science®Google Scholar Parrella G, Scassillo L (2006) [First report of Tomato chlorosis virus (ToCV) in Campania and of Tomato infectious chlorosis virus (TICV) in Calabria (Southern Italy)]. Informatore Fitopatologico 3, 33– 34 (in Italian). Google Scholar Ravensberg WJ, Malais M & Van De Schaaf DA (1990) Applications of Verticillium lecanii in tomatoes and cucumbers to control whitefly and thrips. Integrated control in glasshouse. Contributions to the meeting at Copenhagen (Denmark), Guyancourt (FR). pp. 173– 178. Google Scholar Ravensberg WJ, Buysen AC & Berns R (1994) Side-effects of pesticides on Verticillium lecanii: in vivo tests on whitefly [Trialeurodes vaporariorum] and aphids [Aphis gossypii]. Bulletin OILB/SROP 17, 234– 238. Google Scholar Stenseth C & Singh HM (1990) Buprofezin against the glasshouse whitefly and the cotton whitefly. Gartneryrket 80, 18– 19. Google Scholar Sterk G, Bolckmans K & Eyal J (1996) A new microbial insecticide, Paecilomyces fumosoroseus strain Apopka 97, for the control of the greenhouse whitefly. Brighton Crop Protection Conference: Pests and Diseases – 1996, pp. 461– 466. British Crop Protection Council, Farnham (GB). Google Scholar Tian T, Klaassen VA, Soong J, Wisler G, Duffus JE & Falk BW (1996) Generation of cDNAs specific to lettuce infectious yellows closterovirus and other whitefly-transmitted viruses by RT-PCR and degenerate oligonucleotide primers corresponding to the closterovirus gene encoding the heat shock protein 70 homolog. Phytopathology 86, 1167– 1173. CrossrefCASWeb of Science®Google Scholar Tsai WS, Shih SL, Green SK & Hanson P (2004) First report of the occurrence of Tomato infectious chlorosis virus in Taiwan. Plant Disease 88, 311. CrossrefCASPubMedWeb of Science®Google Scholar Vaira AM, Accotto GP, Vecchiati M & Bragaloni M (2002) Tomato infectious chlorosis virus causes leaf yellowing and reddening of tomato in Italy. Phytoparasitica 30, 290– 294. CrossrefWeb of Science®Google Scholar Verhoeven JTJ, Willemen TM, Roenhorst JW & Van Der Vlugt RAA (2003) First report of Tomato infectious chlorosis virus in tomato in Indonesia. Plant Disease 87, 872. CrossrefWeb of Science®Google Scholar Wisler GC, Duffus JE, Liu HY & Li RH (1998a) Ecology and epidemiology of whitefly-transmitted closteroviruses. Plant Disease 82, 270– 280. CrossrefCASPubMedWeb of Science®Google Scholar 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. CrossrefCASPubMedWeb of Science®Google Scholar Zhu G & Ju Z (1990) Study on applied techniques for controlling greenhouse whitefly with bifenthrin. Chinese Vegetable 5, 14– 15. Web of Science®Google Scholar Citing Literature Volume39, Issue1April 2009Pages 62-64 ReferencesRelatedInformation