Tospoviruses are "emerging " viruses not only in the sense of their increasing economic importance as pathogens on a worldwide basis, but also in that our understanding of the complexity of this new viral taxon only began to emerge during the last decade. Although diseases attributed to tomato spotted wilt virus (TSWV), the type species for the Tospoviruses, were first reported in Australia about 1915, it was not until after 1990 that we came to realize that TSWV was not unique. Prior to 1990, TSWV was considered a monotypic group of plant viruses. There are now at least twelve distinct viruses (species) in the Tospovirus genus. The genus has been classified in the Bunyaviridae family of viruses. Tospoviruses are the only viruses in that family that infect plants.

Economic Importance
Viruses in this genus are collectively of worldwide importance causing significant economic losses on a wide range of crops. During the 1980’s TSWV caused significant losses on peanuts, tobacco and tomatoes in the Southeastern United States (Figures 1 & 2). It has also caused significant losses on these crops in Eastern Europe and South America. In the late 1980’s a new virus was recognized, Impatiens necrotic spot virus (INSV), which caused severe losses in the floral crop industry (Figure 3) in the United States and Europe.

Figure 1. Click the image for a larger view.	Figure 2. Click the image for a larger view.	Figure 3. Click the image for a larger view.

Since then several new viruses have been discovered such as peanut bud necrosis virus that causes significant disease losses to peanut production in India and other similar viruses have caused serious diseases of cucurbits in Japan and Taiwan. Additional viruses have also been identified from vegetables and ornamentals in the United States, Israel and Brazil (eg., Figure 4).

Figure 4. Click the image for a larger view.

Host Range
TSWV has a host range spanning several hundred species in both monocotyledonous and dicotyledenous plants. However, the TSWV host range is not typical of all Tospoviruses, most of which have moderate or small host ranges. Although host ranges tend to vary from virus to virus, Nicotiana benthamiana is a good assay host for most Tospoviruses. Symptoms range from the classical chlorotic spots and concentric rings to veinal necrosis in the leaves and stems. The virus is frequently lethal in young plants. Symptoms may be present on leaves, stems, petioles and flower petals. The symptoms are sufficiently similar so as to be of little diagnostic value. In addition, symptoms exhibited by some hosts mimic symptoms caused by bacterial and fungal pathogens and chemical injury. The lack of diagnostic symptoms has driven efforts to develop specific confirmatory tests that can be easily performed by growers or in diagnostic laboratories as a first step in control.

Dissemination by Insects
Tospoviruses are spread by small insects called  thrips (thysanoptera: thripidae). Less than ten species of thrips have been confirmed as vectors of Tospoviruses and specificity between thrips and tospovirus species has been shown. Tospoviruses replicate in their thrips vectors, thus the insects not only spread the virus, but serve as a virus host. Thrips cannot transmit Tospoviruses unless they acquire the virus during their immature stages (Figure 5).

Figure 5. Click the image for a larger view.

When larvae feed on infected plants, ingested virus crosses the midgut barrier and enters the salivary glands. Transmission then occurs when the virus moves into the plant with the saliva during feeding. A midgut barrier in adults prevents virus ingested during this stage from moving to the salivary gland. While the insects remain infective for life, there is no evidence of transovarial passage from one generation of thrips to the next. Seed transmission of Tospoviruses is not known to occur, but some of these viruses are commonly spread in infected propagation material when crops are vegetatively propagated.

Control
Control of Tospoviruses remains problematic. Cultural practices and varietal selection have proven effective in minimizing losses due to TSWV in some field crops. See, for example this University of Georgia Cooperative Extension Service document, Tomato Spotted Wilt of Peanut: Identifying and avoiding high-risk situations. A series of risk factors including prior history, planting date, cultivar selection and plant and row spacing have been identified as critical factors in peanuts. In other high-risk areas, such as Hawaii, highly susceptible crops cannot be grown profitably. In greenhouse grown crops, such as floral crops, extreme measures including screening of production areas with fine-meshed cloth, preventative thrips management strategies and use of propagation material shown to be free of TSWV and INSV are necessary for control of these viruses. While forms of resistance have been introduced into various crops, they have nearly always been overcome by the rapid occurrence of resistance-breaking strains of the virus. TSWV is thought to exist in nature as a complex heterogeneous mixture of distinct isolates that can exchange genetic information through reassortment of genome segments. This provides a readily available reservoir of genetic information to facilitate adaptation.

Figure 6. Click the image for a larger view.

The Virus Genome
Tospoviruses are one of only two known plant virus taxa whose virions are bounded by a membrane-like envelope (Figure 6). The viral genome is divided among three segments of RNA, which are contained within the envelope. The genome has an interesting organization in that the large RNA codes for the RdRp in the viral complementary sense while the middle and small RNAs each code for two proteins in an ambisense orientation (Figure 7).

Figure 7. Click the image for a larger view.

One or a small number of RNA-dependent, RNA polymerase (RdRp) molecules are associated with each segment of the genome. As the RdRp is required in the initial stages of infection, its activity must be preserved during the transmission process and therefore these viruses have well defined tolerances for the transmission process. This characteristic results in a relatively unstable virus. The ambisense genome organization consists of one open reading frame in the viral sense at the 5’ end of the molecule and a second open reading frame near the 3’ end in the viral complementary sense. A large A-U rich intergenic region separates the two open reading frames. Interestingly, nonstructural proteins on the small (NSs) and middle NSm) genome segments are located near the 5’ end and the open reading frames nearer the 3’ end code for structural proteins (N and G1/G2). The N protein encapsidates the RNA genome segments and may have other functions involved in replication. G1/G2 are found in the envelope and may be involved in recognition of receptors in the vector. NSm has been associated with cell-to-cell movement. NSs accumulates to very high concentrations in infected cells, but its function remains a mystery.

Future Challenges
Many challenges remain as investigations of Tospoviruses continue. New viruses in this group continue to be identified. More effective and efficient control strategies are required in almost every group of crops, especially field crops. The genome organization has slowed progress in elucidating fundamental knowledge regarding gene function. At the present time there is still no system for routine reverse genetics for any member of the Bunyaviridae.

Selected References:

Best, R. J. 1968. Tomato Spotted Wilt Virus. In Advances in Virus Research, ed. K. M. Smith, M. A. Lauffer, 13:65-145. Academic Press New York.

De Avila, A. C., de Haan, P., Kormelink, R., Resende, de O., Goldbach, R. W., and Peters, D. 1993. Classification of tospoviruses based on phylogeny of nucleoprotein gene sequences. J. Gen. Virol. 74:153-159.

German, T. L., Ullman, D. E., and Moyer, J. W. 1992. Tospoviruses: Diagnosis, molecular biology, phylogeny, and vector relationships. Annu. Rev. Phytopathol. 30:315-348.

Prins, M., and Goldbach, R. 1998. The emerging problem of tospvirus infection and nonconventional methods of control. Trends   Microbiol. 6:31-35.

Ullman, D.E., Sherwood, J.L., and T.G. German. 1997. Thrips As Vectors of Plant Pathogens, pp. 539-565, In (ed.) T.L. Lewis, Thrips As Crop Pests, CAB International, London.

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