New Whitefly-Transmitted Closterovirus Identified in Tomatoes

Home , Greenhouse whitefly, Tomatillo

A new virus of tomato, tomato infectious chlorosis virus (TICV), has been identified in both field- and greenhouse-grown tomatoes in California, North Carolina and Italy. TICV is transmitted by the greenhouse whitefly (Trialeurodes vaporariorum) in a semipersistent manner. TICV infects a wide range of plant hosts, and has been found naturally infecting Petunia and Ranunculus in greenhouses, and tree tobacco, commercial artichoke and bristly oxtongue in the southern coastal region of Califor- nia. Because of its wide host range, the prevalence of the greenhouse whitefly in fields and First outbreak of tomato infectious chlorosis virus infecting tomatoes in the lrvine area. greenhouses, and the movement The virus was responsible for severe crop losses of tomato in the entire area during fall of susceptible plant hosts within 1993. High populations of the greenhouse whitefly were also observed in the area at that time. Tomato plants infected with tomato infectious chlorosis virus typically show and among countries around the interveinal yellowing, leaf rolling and necrosis. world, TICV is a potential problem for the world’s tomato industry. TICV caused an estimated $2 million loss in Orange County in New whitef ly-transmitted 1993. Control measures include whitefly control, confirmation of closterovirus identified in TICV infection by a diagnostic test tomatoes and roguing of infected plants. In the fall of 1993, Bill Glover of Crop Gail C. Wisler James E. Duffus Hsing-Yeh Liu Production Services, Inc. (Riverside), o o brought to our attention a serious dis- Ruhui Li o Bryce W. Falk ease of field tomatoes in the Irvine area of Orange County. This disease, which appeared to be associated with high populations of the greenhouse whitefly (Trialeurodes vaporariorurn), occurred in epidemic proportions at the time. Subsequent greenhouse and laboratory experiments using symptomatic tomato leaf tissues revealed a new closterovirus to be the causal agent of this disease. This virus, named tomato infectious chlorosis virus (TICV), induces severe yellowing and/or reddening, stunting, rolling and brittleness of leaves on infected plants. TICV caused an estimated $2 million loss the year it was detected in Orange County. In addition to tomato, Red leaves in foreground are from bristly Greenhouse-grown Ranunculus asiaticus TICV affects a wide array of weed, oxtongue (Picris echioides L.) plants in- L. (Persian buttercup) plant infected with crop and ornamental species. This ar- fected with tomato infectious chlorosis vi- tomato infectious chlorosis virus. This in- ticle reports some basic biological as- rus. These infected plants were found grow- fected plant was found in a greenhouse ing in weedy areas surrounding the tomato where infected tomatoes and petunias pects of TICV, including host range, fields where the virus was first detected. were also growing. geographic distribution and recom-

24 CALIFORNIA AGRICULTURE, VOLUME 51, NUMBER 2 mendations for management of TICV positive samples were older green- destructive in greenhouses and fields, in tomatoes. house-grown tomato plants that were particularly in warmer climates being used for seed production. The throughout the world. The susceptibil- Whitefly-transmitted viruses few TICV-positive field samples were ity of several ornamentals, and their TICV is one of several whitefly- from experimental plots that had been movement from one area to another, transmitted viruses that belong to an established using transplants from certainly pose a potential risk for dis- emerging subgroup of the plant greenhouses. Greenhouses that were tribution of TICV. It is possible that closteroviruses. Of the whitefly-trans- surveyed also contained older TICV- TICV is moving through greenhouse mitted closteroviruses currently recog- infected plants and abundant white- plant populations and transplant sys- nized, only beet pseudo yellows virus flies (T.vaporariorum) - a perfect sce- tems. Susceptible hosts like tomatillo, (BPYV) and TICV are known to be nario for TICV transmission from old Petunia, potato, Ranunculus and lettuce transmitted by the greenhouse white- plants to seedlings. breeding lines are often present in fly. Although BPYV and TICV induce TICV has recently been identified in such greenhouse situations, and symp- almost identical symptoms on several greenhouse-grown and field-grown toms could be mistaken for cultural or common hosts, TICV can be distin- tomatoes in North Carolina. Through physiological conditions and thus guished from BPW in that TICV does collaboration with researchers in Eu- ignored. not infect members of the Cucurbi- rope, we have also positively identi- taceae, and BPYV has never been fied TICV in greenhouse-grown toma- Detection and control shown to infect tomato. Studies at the toes in Italy. The origins of this virus Because TICV-induced symptoms USDA Agricultural Research Service are unknown. can be likened to natural senescence, in Salinas show that BPYV is retained The TICV host range is quite large physiological or nutritional disorders in the whitefly vector twice as long and includes weed, crop and orna- and even phytotoxicity from pesti- (6 days) as TICV (3 days). Other mental plants, all of which show char- cides, it is extremely important to whitefly-transmitted closteroviruses acteristic yellowing symptoms similar monitor plants with characteristic or clostero-like viruses are distinct to those seen in tomato (table 1).The symptoms for infection by TICV. from TICV and are transmitted by vector T. vaporariorum is abundant and Symptoms generally appear as the sweet potato whitefly (Bemisia tabaci), the silverleaf whitefly (B. argentifolii) and the banded-wing whitefly (T. abutilonea). Distribution of TICV TICV was first detected in trans- planted field tomatoes in Irvine. It was recovered from surrounding symptomatic tree tobacco, globe artichoke and bristly oxtongue, which are common plants in that region. Although TICV now seems to be established in perennial weed species in the southern coastal region of California, it is not known if it was present in these hosts prior to its introduction in tomato. Subsequent surveys have shown that TICV is present in greenhouse-grown tomato seedlings as well as in Ranun- culus and Petunia species, which have been found in the same greenhouses with tomato-breeding programs in northern and central California. We performed limited surveys for TICV in greenhouse and commercial tomatoes throughout California. In 1995,396 samples from tomato plants from Yolo, San Joaquin, Stanislaus and Monterey counties were analyzed for TICV infection. Of these, 57 were TICV-positive. Most of these TICV-

CALIFORNIA AGRICULTURE, MARCH-APRIL 1997 25 interveinal yellowing or reddening on lecular weight of the viral coat protein. choke, which is primarily vegetatively the older leaves, while new growth Relatively simple sample preparation propagated, could also serve as a po- continues to appear normal. Leaves of is needed for both serological assays. tential source of movement for TICV. species such as bristly oxtongue and Molecular probes produced from Major commercial artichoke produc- anthocyanin-containing cultivars of to- TICV-specific clones developed in tion occurs in the central coastal areas mato and petunia show intensified red Salinas and at UC Davis have also of California and the coastal areas of color when infected. As the disease been used for diagnosis of TICV in to- Italy, where TICV has also been found. progresses, interveinal necrosis can oc- matoes using a dot blot hybridization. TICV is similar to BPYV with re- cur, and the leaves become character- In this test, plant samples are extracted spect to transmission by the green- istically brittle, thick and crisp. for total nucleic acid, spotted onto ny- house whitefly. However, TICV is dis- Transmission is an important step lon membranes and hybridized with a tinct from BPYV as seen by the lack of in the initial diagnosis of TICV, espe- nonradioactively labeled nucleic acid serological and molecular cross-reac- cially from new geographic areas. Be- probe that is complementary to the vi- tivity, differences in longevity in the cause TICV is not mechanically trans- ral RNA sequence. Positive reactions insect vector and specific differences mitted, methods of transmission by are seen as black spots that develop on in host range. BPYV has been respon- the greenhouse whitefly are routinely X-ray film corresponding to the in- sible for severe losses in greenhouse- used. These methods entail collecting fected plant sample. grown cucurbit and lettuce crops approximately 30 whiteflies, which Another diagnostic test that can be throughout North America, Europe have been reared on healthy Pkysalis used to detect TICV is the polymerase and Asia. By comparison, TICV has wrigktii Gray, in small-screen leaf chain reaction (PCR). Many laborato- the same potential to be dispersed cages, which are then attached to ries are now equipped for diagnostic throughout the world in greenhouse symptomatic leaves of infected plants. assays using PCR. Genomic sequence and field-crop production. Insects are allowed a 24-hour acquisi- data generated at both the USDA-ARS Recognition of characteristic symp- tion/feeding period and are then and UC Davis have provided for the toms of TICV, early detection by one transferred to healthy indicator plants, development of a very sensitive test or more of the diagnostic tests avail- which usually consist of P. wrightii using the reverse transcriptase-PCR able, whitefly control and elimination Gray and Nicotiana clevelandii Gray, (RT-PCR). Positive reactions in ELISA, of TICV-infected plants from affected among others. After allowing the Western blots, dot blot hybridizations areas are critical in its prevention and whiteflies a 48-hour inoculation period and RT-PCR have been obtained in to- control. on indicator plants, the leaf cages are mato plants as early as 7 days follow- Since this work on TICV was initi- removed and the plants are sprayed ing inoculation by the greenhouse ated, another distinct bicomponent, with the insecticide resmethrin to kill whitefly. whitefly-transmitted closterovirus has the whiteflies. The plants are then been detected in tomato. This virus is placed in the greenhouse and ob- TICV management practices named tomato chlorosis virus (ToCV), served for 3 to 5 weeks for characteris- Once growers are aware of the typi- and it produced symptoms very simi- tic symptoms to develop. cal TICV symptom expression, they lar to those produced by TICV: How- Once TICV was identified as being can maintain a good virus-control pro- ever, unlike TICV, which is transmit- a new whitefly-transmitted clostero- gram. Minimizing exposure to TICV ted only by the greenhouse whitefly, virus, the virus was purified for anti- by avoiding overlap with other sus- ToCV is transmitted by the green- serum development and the genomic ceptible crops, controlling whiteflies house, sweet potato, silverleaf and RNA of the virus was cloned for pro- and roguing infected plants are critical banded-wing whiteflies. ToCV is also duction of molecular, or nucleic acid, to avoiding this virus problem. It is es- distinct from TICV based on serologi- probes. Clones of the virus were used pecially important to avoid overlap cal and nucleic hybridization assays. to establish new information on the between young and old tomatoes or ToCV has been found in greenhouse- nucleotide sequence of this growing other susceptible crop populations, grown tomatoes in north-central group of plant viruses. Several sero- particularly when tomatoes are grown Florida and also has a wide host logical and molecular probes have in greenhouses in the vicinity of sus- range, including several ornamental been developed for specific diagnosis ceptible crops. Because we do not species. Research will continue to de- of TICV in tomatoes. Antiserum to the know the complete host range of termine the worldwide distribution of purified virus, developed by Dr. TICV, growers should be aware of the these viruses of tomato and the pos- Hsing-Yeh Liu at the USDA-ARS in possibility of transmission to or from sible existence of additional viruses. Salinas, has been used to detect TICV other susceptible hosts. Although po- in tomatoes from greenhouse and field tat0 is susceptible to TICV, there is no G.C. Wisler, J.E. Duffus, H. Liu and R. Li collections in serological tests such as indication of the natural occurrence of are all Plant Pathologists located at the ELISA and Western blot assays. The a closterovirus infecting potato at this USDAAgricultural Research Station, Western blot assay is the preferred se- time. However, potato could serve as Salinas; and B. W. Falk is Professor and rological analysis because of its sensi- an important vehicle for movement of Plant Pathologist, Department of Plant tivity and its ability to confirm the mo- TICV throughout the world. Arti- Pathology, UC Davis.

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