Tomato spotted wilt orthotospovirus (tomato spotted wilt)

Symptoms are illustrated by reference to a selection of economically important vegetable, ornamental and industrial crop species. TSWV can induce a wide variety of symptoms that may vary on the same host species with cultivar, age and nutritional and environmental conditions. Isolates of TSWV usually do not differ in biological properties and differ only slightly in molecular and serological properties. A study of the diversity of eight TSWV isolates collected from north-eastern Spain showed a slight biological variability among the isolates when compared in 10 host species; no differences in transmission efficiencies were found among them (Roca et al., 1997).

Symptoms evoked by other orthotospovirus species do not differ principally from those caused by TSWV. The greatest care should be used to distinguish the orthotospovirus species by symptoms alone.

Inoculation of solanaceous species may result in the generation of defective interfering RNAs. These RNAs are formed by deletions in the L RNA. Isolates containing these DI RNAs usually have attenuated symptoms (Resende et al., 1991b; Inoue-Nagata et al., 1997) and are often poorly transmitted by thrips (Nagata et al., 1999).

On tomatoes, plants show bronzing, curling, necrotic streaks and spots on the leaves. Dark-brown streaks also appear on leaf petioles, stems and growing tips. The plants are small and stunted. The carotene, chlorophyll and xanthophyll levels decreased. The ripe fruit shows paler red or yellow areas on the skin. Sometimes affected plants are killed by severe necrosis. Symptoms are occasionally only found on the fruits (Pavan et al., 1996). Some fruits of TSWV-resistant plants can show peculiar ringspot symptoms caused as consequence of an insufficient hypersensitive response by the feeding of viruliferous thrips on the fruit during the early stages of development (de Haan et al., 1996; Aramburu et al., 2000).

On Capsicum, symptoms are mainly stunting and yellowing of the whole plant. Leaves may show chlorotic line patterns or mosaic with necrotic spots. Necrotic streaks appear on stems extending to the terminal shoots. On ripe fruits, yellow spots with concentric rings or necrotic streaks have been observed. On lettuces, infection starts in leaves on one side of the plant, which becomes chlorotic with brown patches. The discoloration extends to the heart leaves and cessation of growth on one side of the plant produces characteristic distortion.

On chrysanthemums, there is a wide variation among cultivars. Usually black stem streaks and wilt are observed. On gloxinias, infected leaves show yellow or brown leaf spotting, or brown oak-leaf patterns. On Impatiens, some cultivars of New Guinea hybrids infected with INSV and TSWV develop stunting, black discoloration at the base of the leaf, or brown leaf spots. On groundnuts, symptoms of the disease now attributed to a distinct orthotospovirus, groundnut bud necrosis are bud necrosis, chlorosis of foliage, limb collapse and plant death.

As there is no direct means of controlling the virus, the method of control must either be aimed at the thrips vectors or involve the application of sanitation measures. Seedling beds should be isolated from ornamental plants and susceptible crops and the surrounding areas kept free from weeds. The inside and outside of glasshouses should be kept free of weeds, thus reducing all possible sources of infection and reducing thrips populations. Fine-mesh netting may possibly be useful to exclude thrips (Lacasa et al., 1994). Susceptible decorative plants should preferably not be grown in the vicinity of the glasshouse. The glasshouse should be regularly and frequently inspected after planting. The presence of thrips in the crops should be monitored using yellow sticky cards. If the disease appears in a crop, infected plants should be rogued and destroyed immediately and the house treated with insecticide against thrips.

Similar precautions should be taken with field crops. Although chemical control is possible (Bournier, 1990), F. occidentalis has been found to develop resistant populations if certain insecticides are used repeatedly (OEPP/EPPO, 1989). It is, therefore, important to rotate insecticides with different active ingredients. For ornamental hosts (chrysanthemums, pelargoniums) for which virus-free certification schemes are applied, TSWV is now one of the most important viruses to be tested for (OEPP/EPPO, 1992). Promising results with biological and integrated control measures against thrips in glasshouses have been achieved in several countries (Gillespie, 1989; Ramakers et al., 1989; Trottin-Caudal and Grasselly, 1989; Sanchez et al., 2000). Frankliniella occidentalis, infesting plants and present in plastic houses, could be drastically reduced in number using UV-absorbing plastic sheets as cover (Antignus et al., 1996).

Reports about the virus-vector relationship and reduction in TSWV epidemics by chemical treatment are very limited. However, higher levels of control of TSWV were observed in dahlia with weekly sprays of mineral oil, polydimethylsiloxane and deltamethrin (Asjes and Blom-Barnhoorn, 2001). Host-plant resistance, intensive insecticide treatment and the use of reflective mulch significantly reduced the incidence of thrips and TSWV (Riley and Pappu, 2000). In Louisiana, USA, aluminium-surfaced mulch reduced the numbers of trapped thrips by 33-68% and the incidence of TSWV by 60-78% in tomatoes and Capsicum (Greenough et al., 1990). These results support the general view that primary transmission during adult thrips dispersal and host seeking accounted for most observed incidences of TSWV in tomato and groundnut (Camann et al., 1995) and probably also in most crops.

Yudin et al. (1990) devised disease-prediction and economic models that enable growers with lettuce fields affected by TSWV to make management decisions early in the planting cycle. Early disease incidence was a better predictor of disease incidence at harvest than thrips abundance because the proportion of infectious insects is essential to analyse the epidemics. The incidences of TSWV in early transplanted tomato crops with the highest thrips population was comparable to those found in late transplanted tomatoes with very low population densities (Aramburu et al., 1997).

The effect of the groundnut variety, planting date, plant density, insecticides used and disease history on the incidence and severity of TSWV was assessed in groundnut fields in Georgia, USA. These effects can be evaluated for each field in a risk assessment index. This index can vary between 25 and 125 points for each field. Fields with an index of 25-55 were considered to have a low risk, those between 60-80 a moderate risk, and those with more than 85 a high risk (Brown et al., 1998). Previous crops, adjoining crops, tillage practices, row patterns and weather also have effects, but were not indexed as these factors are insufficiently defined.

Screening vegetative dahlia propagation material for TSWV infections resulted in an almost healthy dahlia crop and seed tubers in the Netherlands (Schadewijk, 1996).

The growth regulators gibberellic acid, naphthalene acetic acid and chlormequat sprayed once on tomato plants either before or after TSWV inoculation inhibited the infectivity of the virus (Sapatnekar and Sawant, 2001).

Several sources of resistance to TSWV have been found in species of Solanum (Kumar et al., 1995; Cho et al., 1996). Two dominant and three recessive genes were responsible for resistance in S. pimpinellifolium and two tomato cultivars (Finlay, 1953). Introduction of these genes in tomato lines did not result in field resistance (Watterson et al., 1989). Lack of success in introducing this resistance into commercial tomato cultivars may be due to the existence of different TSWV strains or pathotypes. The tomato cv. Stevens, obtained from a cross between S. lycopersicum and S. peruvianum, has broad resistance to different TSWV isolates (van Zijl et al., 1986) and has been preferred by breeders for incorporating resistance into cultivated tomatoes. This resistance, introgressed in cv. Stevens, is conferred by a single dominant gene denoted Sw-5 with a 98.7% penetrance (Stevens et al., 1992) and also provided a high level of resistance to other members of the genus orthotospovirus, including Groundnut ringspot orthotospovirus (GRSV), Tomato chlorotic spot orthotospovirus (TCSV) and Groundnut bud necrosis orthotospovirus (GBNV). TSWV isolates, breaking this resistance, have been found in field crops in South Africa, Australia, USA (California and Hawaii) and Spain (Thompson and van Zijl, 1996; Latham and Jones, 1998; Aramburu and Marti, 2003; Batuman et al., 2017). New and selected accessions from Solanum species showed high resistance to TSWV and other viruses and seem to be of interest for enhancing the durability of the resistance to TSWV in commercial varieties (Roselló et al., 1999; Picó et al., 2002).

In lettuces, two cultivars (Tinto and Ancora) are reported to be resistant to TSWV in Hawaii, USA (O'Malley and Hartmann, 1989). This resistance was not confirmed in later studies. In groundnuts, breeding lines with a lower incidence of spotted wilt and lower disease severity ratings have been, or will be, released (Culbreath et al., 1996). Some field tolerance to GBNV occurs in Indian cultivars (Nigam et al., 1990) and could be explained by mature and tissue resistance (Buiel and Parlevliet, 1996). In tobacco, Nicotiana sanderae was immune and N. alata and N. langsdorffii were highly resistant to TSWV (Palakarcheva and Yancheva, 1989).

A gene designated Tsw, which prevents systemic spread of TSWV by a hypersensitive response has been identified in several C. chinense accessions (Black et al., 1993; Boiteux, 1995). This resistance proved to be less stable when young plants became infected and were kept at high temperatures (Roggero et al., 1996; Moury et al., 1998; Soler et al., 1998); by contrast, INSV infection was restricted to the inoculated leaves in Capsicum annuum and C. chinense under high temperatures (Roggero et al., 1999). The Tsw gene has phenotypic and genetic similarities of resistance in pepper with tomato plants carrying the Sw-5 gene; however, distinct viral gene products control the outcome of TSWV infection (Jahn et al., 2000); so, TSWV isolates that overcome tomato resistance gene Sw-5 failed to overcome hypersensitive resistance to TSWV in C. chinense PI 152225 and PI 159236 (Latham and Jones, 1998). Line 159236 was not resistant to GRSV (Boiteux and Nagata, 1993).

High levels of resistance to TSWV has been obtained in inbred lines of tomato transformed with the nucleoprotein (N) gene (de Haan et al., 1996). Similar levels of resistance have also been found in Nicotiana tabacum and N. benthamiana (Vaira et al., 1995), and chrysanthemum (Sherman et al., 1998) containing the nucleoprotein gene of TSWV. This transgenic resistance to TSWV in N. tabacum is effective in reducing the incidence of the disease under field conditions (Herrero et al., 2000). Sense or antisense copies of the N or Nsm genes can confer resistance. Groundnut lines transgenic for the antisense nucleocapsid (N) gene showed a lower TSWV incidence in field assays (Magbanua et al., 2000). Other TSWV sequences, spanning 70% of the genome, appear not to be effective in inducing resistance in transgenic tobacco (Prins et al., 1996). A broad resistance to GRSV, TSWV and TCSV was found in tobacco plants expressing the N gene sequences of these viruses (Prins et al., 1995). Transgenic plants expressing the transgene with green fluorescent protein fused to segments of the nucleocapsid (N) gene of TSWV showed multiple virus resistance (Jan et al., 2000).

The ability of TSWV isolates to overcome the resistance conferred by Sw-5 gene in tomato and the resistance conferred by the nucleocapsid gene in transgenic tobacco has been associated with the M RNA segment (Hoffmann et al., 2001).

Phytosanitary Measures

Susceptible host plants in greenhouses should be regularly inspected for orthotospovirus infections and vectors. Removal or roguing of infected plants, especially when the incidence is low, is an option to control further spread. Application of this practise may depend on the crop and its age, and the question whether the infection will or will not spread in the crop. Vectors should be actively controlled at the place of production. In general, heavily infected crops should be destroyed. Where appropriate, healthy planting material should be used. All plant residues left after harvested crops in greenhouses and fields should be eliminated. The soil has to be disinfected after the removal or harvest of severely infected crops with a high infestation of thrips. The emerging of viruliferous adults from infected pupae may form a serious threat to the new crop.

TSWV and other orthotospoviruses have become an increasingly important factor contributing to economic losses in many food and ornamental crops throughout the world; losses may be as high as 100% (Berling et al., 1990; Rodriguez, 1990; Roselló et al., 1996). TSWV incidence in Brazil, Hawaii, USA, and South Africa can be so high that farmers are forced out of production. Destructive outbreaks of TSWV have occurred in France and Spain in protected and field crops of tomatoes, Capsicum and Anemone, associated with the establishment and rapid spread of the vector Frankliniella occidentalis (OEPP/EPPO, 1989). In Liguria, Italy, Capsicum production can be severely affected while adjacent tomato and lettuce crops remain healthy. Devastating epidemics can occur in tobacco in Bulgaria, Greece and other south-eastern European countries. In some areas of Argentina, Brazil, Italy and South Africa, TSWV has become one of the most important diseases in tomato. In general, economic loss data are limited, but the following examples of economic impact have been obtained from the literature.

In groundnuts, TSWV has been shown to reduce yield in direct proportion to the intensity of infection. Healthy plants produced 50% more kernels than plants with maximum infection by TSWV (Saharan et al., 1983). The virus reduces height, root length and yield depending on the plant growth stage at the time of infection (Rao et al., 1979). In plants showing symptoms within 45 days of sowing, 100% losses were observed. Losses decreased with increasing age of plants at infection. Gopal and Uphadhyaya (1991) reported yield losses of 50% in Raichur, India. Field trials indicated that early infection with the virus caused a heavy yield loss compared with late infection. Siddaramaiah et al. (1980) reported a drastic reduction in dried pod weight, fresh fodder weight and shelling percent in plants affected at an early stage. Narendrappa and Siddaramaiah (1986) also reported that infection of plants up to 65 days old caused significant reductions in yield while no losses were recorded in plants infected after 95 days. The incidence of bud necrosis (caused by TSWV) has been shown to be lower in close plant spacings than in wide ones (Anon., 1981). Culbreath et al. (1992) reported that the number of seed produced, average weight per seed and total seed yield were lower for TSWV symptomatic plants than for healthy plants in Georgia, USA, in 1988, 1989 and 1990. TSWV has also been reported to reduce the oil content in groundnuts; earlier infection causing greater losses. Plants infected 15 days before harvest showed a 13.2% oil reduction (Ali and Rao, 1982).

Fiederow and Kralowska (1995) reported decreases in yields of tomatoes and Capsicum of 38.7 and 92.2%, respectively. In tomatoes, earlier infection has been shown to cause greater yield losses (Kumar and Irulappen, 1991). A lower number of fruits, fruits weight, and yield were recorded in tomato plants infected at an early stage than those infected at more mature stages; however, the quality of production was altered even in late-infected plants due to abnormal ripening and no difference in marketable fruit yield was obtained (Moriones et al., 1998).

The biochemical changes caused in tomato following infection with TSWV have also been studied. Chlorophyll, xanthophylls and carotene levels decreased in infected plants (Sutha et al., 1998).

In peas in India, TSWV-affected plants were pale-green and stunted with reduced leaf petioles, stipules and tendrils. Only a few pods were produced and these were necrotic. Disease incidence ranged from 10 to 25%, causing serious yield losses (Singh and Gupta, 1994). In greenhouse tests in Canada during 1989-1990 and 1990-1991, TSWV affected Lathyrus sativus and Pisum sativum var. arvense. In L. sativus, symptoms varied from loss of chlorophyll, wilting and drying-up of the foliage to bleaching and drying-up of stem segments at the nodes. In P. sativum var. arvense, purplish-brown streaks were prominent on the stems and petioles. Flower and pod abortion occurred in severely affected plants (Zimmer et al., 1992).

In cucurbit and solanaceous vegetables in Okinawa, Japan, severe losses have been caused by TSWV. Cucumber plants inoculated at the cotyledon stage were shorter, lateral shoots were fewer and shorter and yields were 40% lower than in non-inoculated plants (Hokama and Tokahashi, 1987).

Dahlias in the Netherlands in 1992, 1993 and 1994 had infection levels of 15, 5 and 2%, respectively. Yield of cuttings/tuber was reduced by up to 20% (Asjes et al., 1997).

In Hawaii, USA, TWSV has destroyed 50-90% of lettuce crops (Cho et al., 1987).

Potato crops have been affected by TSWV in India (Khurana et al., 1997), Portugal, Brazil and Argentina (Granval de Millan et al., 1998). Doubt exists as to whether infected tubers will produce healthy plants when they sprout.