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In Beta vulgaris, BYV induces vein clearing or vein yellowing 3-4 weeks post-infection, then leaves become thick, brittle and yellow with necrotic spots. In Chenopodium capitatum, BYV causes vein clearing of young leaves accompanied by twisting and distortion. Older leaves show interveinal reddening, plants are stunted and sometimes die.
In Montia perfoliata, characteristic symptoms are chlorosis of older leaves and red-rimmed necrotic spots on systemically infected younger leaves. In Tetragonia expansa [T. tetragonioides] young leaves show vein clearing, then interveinal yellowing develops and the plants become dwarfed.
Control of 'virus yellows', and of BYV as one of the viruses forming this complex, includes physical separation of beet root and seed crops, elimination of the overwintering sources of the virus inoculum between seasons, and control of the aphid vectors (Duffus et al., 1983; Steven et al., 2006). Seed treatment with imidacloprid gave the best control of aphid vectors (Myzus persicae) over aphicidal granules applied at drilling or aphicidal sprays (Dewar et al., 1996). In the UK, seed treatments have been adopted as the standard method for the control of virus yellows (Dewar and Cooke, 2006). New neonicotinoid treatments such as clothianidin have also been developed to control Myzus persicae and hence BYV (Ayala and Bermejo, 2001; Dewar et al., 2002, 2003).
BYV has no significant weed reservoirs of infection (Stevens et al., 1994); unlike BMYV and BWYV, it is transmitted semi-persistently, i.e. BYV is retained in aphids for a much shorter time, and the only sources of the virus are overwintered beet plants left in the field. Consequently, systematic use of the control measures described shifts the relative proportion of different viruses in the virus yellows complex. Indeed, in Europe the relative incidence of BYV in disease-affected sugarbeet decreased while the incidence of BMYV increased (Bjorling and Mollerstrom, 1974).
There are no BYV-resistant varieties available within Europe, although resistance to BYV has been identified in 600 accessions of closely related wild and cultivated Beta species (Luterbacher et al., 2000, 2004). However, sugarbeet germplasm lines have been registered in the USA that have resistance to BYV, BWYV and BChV (Lewellen, 2000a, 2000b, 2002, 2004)
Beet yellows virus (BYV) is the type member of the genus Closterovirus. The members of this group are characterized as aphid-transmitted viruses with flexuous, filamentous particles.
At least 121 species in 15 families are experimentally susceptible to BYV (Duffus, 1973; Peters, 1988) and most potential host species occur in the Amaranthaceae, Aizoaceae, Caryophyllaceae or Chenopodiaceae. The last family contains over half of the known hosts of BYV as well as the susceptible crop species (sugarbeet, fodder beet, beetroot, Swiss chard and spinach). By far the most important crop host is sugarbeet (Beta vulgaris ssp. vulgaris) which is primarily grown in temperate regions between 30° and 60°N in Europe, Asia, North America and Africa, with a small amount produced in South America. Annual beet sugar production is approximately 40 million tonnes which supplies about 37% of the world sucrose demand (Cooke and Scott, 1993). BYV is frequently found in association with beet mild yellowing virus (BMYV; genus Polerovirus) because they share Myzus persicae as their principal vector. These viruses are responsible for virus yellows disease which is one of the most important diseases of sugarbeet. The two viruses were not distinguished until 1958 (Russell, 1958) and therefore research before this date must be interpreted with caution.
In the field, BYV is maintained between seasons in a variety of reservoirs such as sugarbeet clamps, seed crops and groundkeepers as well as weed species such as Senecio vulgaris and Capsella bursa-pastoris (Costa et al., 1959). More recent work has suggested that weed hosts are of limited importance (Stevens et al., 1994). Alate aphids carry BYV from the overwintering host to the sugarbeet crop in spring, while apterous aphids and later alates spread the virus from the primary focus of infection within the crop (Hull, 1963). The aphid loses infectivity when it moults at ecdysis which, combined with the short retention time of the virus, means that the incidence of the disease is high adjacent to the virus source but decreases rapidly with distance. These characteristics frequently lead to the development of yellow patches in infected fields. BYV is transmitted semi-persistently by at least 22 aphid species; M. persicae is the principal vector (Watson et al., 1951) although Aphis fabae, Macrosiphum euphorbiae, Myzus ascalonicus and M. certus are also important. Brief aphid feeding does not spread semi-persistently transmitted viruses and there is no latent period during which the aphid is non-infective following acquisition. In the case of BYV, optimum acquisition occurs when aphids have fed for more than 12 hours on infected plants; transmission is optimised if infected aphids are allowed to feed for at least 6 hours on healthy plants (Russell, 1970). BYV is not seed-transmitted and is only spread mechanically with difficulty in vitro.
The first symptoms of BYV infection appear as a yellow patch at the point of infection that spreads to cover the whole leaf. Cytological studies of infected sugarbeet seedlings have shown that the virus is initially restricted to the phloem and parenchyma from which it spreads to adjacent mesophyll cells and eventually to the epidermal layer (Esau, 1960). Systemic movement of the virus follows the path of photosynthate transport in the phloem, thus the older leaves which, at the time of infection, are exporters of photosynthates do not become infected (van der Werf, 1989a). The virus is also moved much more slowly between cells via the plasmodesmata (Esau et al., 1967). In the most pathogenic strains, vein clearing or yellowing is followed by vein chlorosis and etching on the undersurface of leaves (Russell, 1970). As time progresses, the older leaves turn pale yellow, and reddish or brown necrotic spots often appear. Eventually the leaves turn bronze and become thickened and brittle. Leaves in the early stages of development will become infected but do not exhibit yellowing symptoms until maturity. Thus, in infected plants, three distinct whorls of leaves can often be recognised: young infected but symptomless leaves, mature uninfected leaves, and mature leaves showing marked symptoms. Less pathogenic strains do not cause vein etching during early development of symptoms and show less marked necrosis of the leaves (Peters, 1988). The incubation period before symptom expression varies during the season, being ca three weeks in young plants (van der Werf et al., 1989b). BYV also has marked effects on sugarbeet physiology and significantly reduces growth and yield. This reduction in growth is due to decreases in both net photosynthesis and the amount of radiation intercepted by green leaves (Hall and Loomis, 1972; de Koeijer and van der Werf, 1995; Clover et al., 1999a) rather than a decrease in total leaf area. Therefore, there is no evidence that the yield loss of infected plants is compensated for by improvements in the yield of surrounding healthy plants.
As sugarbeet is the most important crop host of BYV, research on the economic impact of the virus has concentrated on this crop and no information is available regarding its effect on other crops such as spinach or beetroot. Frequent references are made in the scientific literature to the economic significance of BYV but these are rarely quantitative and few attempts have been made to express these losses in financial terms. This is due to the inherent problems of estimating yield losses in the field and assessing the true value of these losses in the regulated markets under which sugarbeet is generally produced. However, there are a number of studies which report the incidence of the disease in different locations and periods together with research on the effect of the virus on artificially-infected individual plants or stands in the glasshouse or field, respectively. Together these data suggest potential losses that might occur in heavily infected crops. To describe the economic impact of BYV fully, the factors which determine losses caused by the virus, the constituent components of these losses, the potential and actual yield losses caused by the virus and finally indirect losses which are attributable to the virus must be considered.
Factors Determining Losses
There are large variations between studies in the size of the losses caused by BYV infection in sugarbeet. These variations result from differences in experimental conditions, principally the susceptibility of crop cultivar, pathogenicity of virus strain, the time of infection and to a lesser extent, the plant's nutritional status and environmental conditions.
Together with the virus strain, this is the most important determinant of the effect of BYV on yield and yield losses reported in one cultivar may not be representative of other cultivars (Russell, 1964a, b). For example, in an experiment in 1961, Russell (1964b) demonstrated that the 'Bungay' BYV isolate decreased the sugar yield of six varieties by between 10-18%. In the UK, the losses in storage root and sugar yield of five cultivars infected with BYV varied between 13-47% and 16-47% respectively (Smith and Hallsworth, 1990). While in California, USA, the root and sugar yield of six infected sugarbeet cultivars was reduced by between 16-43 and 20-52% respectively (Hall et al., 1972).
The pathogenicity of the virus strain is clearly of crucial importance in determining the effect of BYV on yield. Russell (1964b) showed that different isolates of BYV produced symptoms of different severity on sugarbeet and caused different yield losses in both the glasshouse and field. For example, three English BYV isolates reduced the yield of an inbred sugarbeet line by between 25-30% in the glasshouse. Experiments in the field in 1961, 1962 and 1963 showed that a panel of between three to ten different English isolates of BYV decreased the sugar yield of commercial varieties of sugarbeet by between 7-31, 19-29 and 0-30%, respectively (Russell, 1964b). Furthermore, simultaneous inoculation with two isolates generally gave a yield loss of intermediate severity but, in some cases, the losses were either greater or less than expected. For example, separate infection with two BYV isolates from Doddington and Sutton, UK, reduced sugar yield by 9 or 13% but simultaneous infection reduced yield by 15% (Russell, 1964b).
Time of infection
Early studies concluded that the yield loss caused by BYV infection was directly proportional to the period of infection and proposed the use of infected plant weeks over the whole season to predict such yield losses (Watson et al., 1946; Hull, 1953). However, although there is no particular growth stage of sugarbeet during which BYV infection is particularly damaging, infection after about the 18-20 leaf stage (approximately the end of July in Europe) does not significantly reduce yield. This has been demonstrated in the Netherlands (Heijbroek, 1988), UK (Smith and Hallsworth, 1990) and USA (Tamaki et al., 1978). Before this time, there is a linear correlation between the period of infection and the size of yield loss and this has been calculated to equate to a loss of 5.9% per infected plant week in the Netherlands (Heijbroek, 1988). In the UK, BYV infection at the 4-6 leaf stage in early June reduced sugar yield by 22%, at the 18-20 leaf stage in mid-late July infection reduced yield by 9% and infection in August did not affect yield (Smith and Hallsworth, 1990). Late infection (mid-July in the northern hemisphere) has little effect on yield losses but early infection can decrease yield by up to 47% and increases the level of impurities which makes sugar extraction at factories more difficult.
Nutritional status of plant
Although it is clear that BYV infection radically disturbs the nutritional status of sugarbeet (Rimsa and Rysánek, 1992), it is not known whether specific nutritional deficiencies alter the response of sugarbeet to BYV infection. However, Heijbroek (1988) showed that application of either liquid potassium or nitrogen fertilisers to sugarbeet infected with virus yellows reduced sugar yield losses by 15%. However, the concomitant increase in the concentration of storage root impurities more than outweighed any reduction in yield loss.
The exact role of environmental conditions in determining the effect of BYV on sugarbeet is not clear but field experiments suggest that temperature may influence the severity of disease losses. For example, Heijbroek (1988) and Smith and Hallsworth (1990) suggested that greater yield losses occurred when air temperatures were higher, especially during spring and early summer, possibly because of the effect of temperature on virus multiplication. This hypothesis is supported from glasshouse studies that generally show that symptoms of BYV infection are less under cooler, winter conditions than during the warmer spring or summer. Similarly, glasshouse experiments have also suggested that light may play an important role in the disease process since under such conditions, infected sugarbeet gives few or any symptoms during the winter months unless supplied with additional light. The effect of environmental factors is suggested from the results of Clover et al. (1999a) who reported root yield losses of 24, 16 and 20% in three consecutive years using the same cultivar of sugarbeet, virus strain and experimental methods.
Interaction with other stresses
Infection of sugarbeet with BYV is frequently associated with infection by BMYV because the two viruses share common aphid vectors. However, the yield effect of the two viruses in combination is not simply the addition of their individual effects and the yield reduction is generally less than expected in such instances (Russell, 1964b). Co-infection of sugarbeet lines with BYV and Beet mosaic virus caused severe stunting as measured by plant biomass when compared to single infections with these viruses (Wintermantel, 2005). Infection with BYV is thought to predispose sugarbeet to infection by other pathogens, in particular fungi that may invade the leaves through necrotic lesions caused by the virus.
With regard to abiotic stresses, drought is the major constraint on sugarbeet yield in many areas (for example see Jaggard et al., 1998) but the effect of BYV infection and drought on yield is simply additive and no interaction occurs (Clover et al., 1999b). The accurate prediction of the yield of stressed plants requires knowledge of their infection and drought status (Clover et al., 2001). Little is known about the interaction of BYV with other abiotic stresses.
Components of Yield Loss
The reduction in sugar yield from BYV-infected sugarbeet results from a decrease in storage root weight, a reduction in storage root sugar concentration and an increase in juice impurities in the storage roots.
Storage root weight
Infection with BYV decreases the overall weight of sugarbeet plants. As an illustration, Clover et al. (1999a) concluded from the results of three field and two glasshouse experiments that infection reduced total dry matter yield of sugarbeet by 20% from 18.7 to 15.1 t/ha. The decrease was primarily due to the reduction in the yield of storage roots (3.3 t/ha; 25%) rather than foliage (0.4 t/ha; 7%). It is the reduction in the size of storage roots in diseased plants which is the main cause of yield loss in BYV-infected sugarbeet. For example, in field experiments during 1985 with five cultivars in the UK, Smith and Hallsworth (1990) observed decreases in fresh storage root and sugar yield of 13, 20, 23, 39 and 47% and 16, 22, 27, 40 and 47%, respectively. In California, USA, Hall et al. (1972) reported that BYV reduced the fresh root and sugar yield of six sugarbeet cultivars by between 16, 26, 27, 36, 40 and 43% and 20, 31, 33, 41, 46 and 52%, respectively. In these examples it can be calculated that the decrease in storage root yield accounts for about 84% (Hall et al., 1972) and 91% (Smith and Hallsworth, 1990) of the total decrease in sugar yield.
A minor component in the loss of sugar yield in BYV-infected sugarbeet results from the decrease in the concentration of sugar in infected storage roots. The size of the decrease in sugar concentration in infected sugarbeet is very dependent on cultivar and the time of infection and frequently little or no effect may be observed (Russell, 1964b). For example, in field experiments with five UK cultivars, Smith and Hallsworth (1990) observed a reduction in the sugar concentrations of fresh storage roots of between 0 and 0.5 percentage points. There was no reduction in sugar concentration in plants infected after the end of July. Clover et al. (1999a) reported similar reductions (0-0.3 percentage points) in sugar concentration in three field experiments on one cultivar infected with BYV in the UK. In the USA, virus yellows has been reported to reduce sugar concentration by between 0.1-0.3 percentage points (Tamaki et al., 1978) .
Storage root impurities
Sugar is extracted from the storage root of sugarbeets by a complex industrial process that involves clarification using lime, evaporation and crystallization. The pH value is critical during each of these stages and the presence of impurities such as sodium and potassium that increase pH during lime clarification, and amino-nitrogen which decreases pH during evaporation, affects extractability. BYV-infection significantly increases the concentration of sodium, potassium and amino-nitrogen impurities in the storage roots of sugarbeet (Russell, 1964b; Smith and Hallsworth, 1990). In common with other components of yield loss, the extent of this loss in quality is determined by the time of infection and sugarbeet cultivar. Thus, Smith and Hallsworth (1990) reported that in the UK, infection increased the concentration of sodium, potassium and amino-nitrogen in cultivar Regina by 86, 20 and 22% respectively, but in the cultivar Primo, the concentrations of sodium and potassium were unaltered and amino-nitrogen was increased by 18%. In three field experiments on the cultivar Celt in the UK, the concentrations of sodium, potassium and amino-nitrogen were consistently increased by a mean of 24, 27 and 13% respectively (Clover et al., 1999a).
Potential and Actual Yield Losses
Reports on the effect of BYV on yield generally derive from experiments in which plants or crops were artificially infected. Such experiments provide information on potential yield losses that the virus may cause under those specific circumstances, rather than on the actual losses observed in agricultural conditions.
Potential yield losses
BYV reduces the yield of infected sugarbeet by decreasing storage root yield and sugar concentration and by increasing root impurity concentrations. This section will deal with the effects of BYV on storage root and sugar yield but not root impurity concentrations since the precise effect of changes in their concentrations are difficult to quantify. Smith and Hallsworth (1990) reported that early BYV-infection reduced the fresh root and sugar yield of five cultivars of sugarbeet in the UK by 6.92, 10.67, 12.06, 20.35 and 21.6 t/ha (13, 20, 23, 39 and 47%) and 1.61, 2.23, 2.44, 3.86 and 4.18 t/ha (16, 22, 27, 40 and 47%), respectively, that is mean reductions in root and sugar yield of 14.28 (28%) and 2.86 (28%) t/ha. Clover et al. (1999a) similarly reported that dry storage root yield of one UK sugarbeet cultivar was reduced by a mean of 3.25 t/ha (25%) during three field and two glasshouse experiments and sugar yield was reduced by a similar proportion. Hall et al. (1972) reported that in California, USA, BYV reduced fresh storage root and sugar yield of six sugarbeet cultivars by between 16-43% (mean 31%) and 20-52% (mean 37%), respectively. Similarly in glasshouse experiments, a Californian BYV isolate reduced the dry storage root yield of an American sugarbeet cultivar by 45% (Hull, 1968a). During experiments in Washington state, USA, on the effect of virus yellows on sugarbeet, the fresh root and sugar yield of infected beet was reduced by 12.2 (15%) and 6.04 t/ha (17%) respectively (Tamaki et al., 1978).
Actual financial losses
To estimate yield loss caused by BYV in agricultural situations by extrapolation from the potential yield losses observed under experimental conditions, it is necessary to know the disease incidence, time of infection and the quantitative yield effect of the infecting virus strains on the affected crop cultivars. Bearing in mind the cost and complexity of gathering this information, it is of little surprise that few estimates of actual financial losses have been made. The only studies that have been made for BYV are in combination with BMYV and report the yield losses caused by virus yellows. Unfortunately, it is not possible to separate the individual contributions made by the two viruses on the total loss because their relative incidence has not generally been reported and their effect on yield in combination is not additive (Russell, 1964b). However, such studies do give an indication of the scale of the problem. Early studies on the effect of virus yellows on sugarbeet yield in the UK suggested that the virus decreased mean annual storage root yield by 355,000 t and 302,000 t between 1946-1952 (Hull, 1953) and 1970-1975 (Heathcote, 1978), respectively. At a typical storage root sugar concentration of 16%, this suggests losses in sugar yield of 57,000 (1946-1952) and 48,000 t (1970-1975). However, it is likely that neither estimate is particularly accurate because both studies assumed that losses due to virus yellows were linearly correlated with time throughout the season. A more rigorous analysis by Jaggard et al. (1998) used experimental relationships between yield loss and the timing of infection in combination with annual survey data of disease incidence and calculated infection dates from the national aphid suction trap network, to calculate actual annual losses to virus yellows in the UK between 1980-1985. They estimated that on average, the disease decreased sugar yield by 24,700 t annually. This represents 1.8% of the national yield and at the 1996 world raw sugar price of £200 per tonne was worth approximately £5 million. The reduction in processing quality caused by the increase in root impurities in virus yellows-infected sugarbeet was estimated to increase total losses to £5.5 million. However, average potential losses in the absence of measures to control the aphid vectors of the disease were estimated to be approximately double this (Jaggard et al., 1998). A less rigorous study by Roturier (1991) estimated that in France, in 1989, virus yellows infected about 11% of the crop and decreased national sugar yield by 83,000 t (2.1%). This loss in production was worth FF 116 million in production costs in 1989 (FF 1400 per tonne of sugar) or £16.5 million at the 1996 world raw sugar price. In common with Jaggard et al. (1998), Roturier (1991) recognised that disease losses would be much higher in the absence of measures to control the disease.
Unfortunately, estimates of the actual financial losses caused by BYV or virus yellows have only been made in France and the UK. However, reviewing the distribution and incidence of the virus can make an indication of the scale of the problem. The distribution of BYV is well known and the virus has been reported from almost all of the sugarbeet growing areas of the world, in total some 39 countries in Europe, North and South America, Asia and Australia. The knowledge of disease incidence is incomplete because of changes in annual incidence, lack of surveying and confusion with other sugarbeet disorders (for example, BMYV, nutrient deficiencies) (Smith and Hinckes, 1987). The disease is widespread in Austria, Belarus, Belgium, Bulgaria, Czech Republic, Denmark, Finland, France, Germany, Hungary, Italy, Luxembourg, Netherlands, Romania, Russian Federation, Spain, Sweden, Switzerland, Ukraine, UK and the former Yugoslavia in Europe, Japan in Asia, and Canada and the USA in North America. Specific figures are generally only available for the incidence of the virus yellows complex, for example in Washington state, USA, a survey of commercial fields in 1976 showed that 15% of plants were infected with virus yellows (Tamaki et al., 1978). While in the UK, the incidence of virus yellows varied between 6-48%, <1-66% and 0.8-19.8% (mean 7.2%) during 1942-1952, 1965-1985 and 1980-1985, respectively (Hull, 1953; Dunning, 1988; Harrington et al., 1989; Jaggard et al., 1998). The incidence of virus yellows in most European countries between 1946-1985 was reviewed by Dunning (1988). This study reveals that, despite extensive control measures, virus yellows infection remains common, especially in countries such as Belgium and Spain and therefore causes significant damage. However, in this context it should be noted that BMYV is the more common virus in the virus yellows complex in Europe (Smith and Hinckes, 1987; reviewed by van der Werf et al., 1989b).
Apart from the direct losses caused by BYV infecting sugarbeet and reducing yield, the virus also causes a number of indirect losses which are mainly related to attempts to control the disease and ameliorate its effect. Disease controls are primarily aimed at the aphid vectors of the disease, principally by chemical means either as aphicidal sprays (for example, carbamates or pyrethroids) or seed treatments (for example, imidacloprid). Between 1970-75 the annual cost of chemical treatments to control virus yellows in the UK was estimated to be £0.9 million and this was thought to have prevented yield loss worth three times this amount (Heathcote, 1978). More recently, the cost of these treatments was estimated to be similar to the mean actual losses observed, i.e. between £5 and 7 million per annum (Jaggard et al., 1998). In France, the cost of such treatments was estimated to be FF 213 million during 1989 (Roturier, 1991). These treatments were aimed at the control not only of BYV but also BMYV while seed treatments such as imidacloprid have the additional benefit of controlling other deleterious insects (for example, flea beetles). However, there are also additional costs of such treatments that are difficult to quantify, for example, effects on non-target organisms, accumulation of pesticide residues and the developments of insecticide resistance. In many countries such as the UK (Hull, 1968b; Harrington et al., 1989) and the Netherlands (Heijbroek, 1988), application of aphicidal sprays is dependent upon aphid monitoring and spray warning schemes which also clearly have an associated cost.
Cultural methods have also been adopted to reduce the sources of BYV infection, for example the physical separation of root crops and autumn-sown seed crops, rigorous hygiene of root clamps and removal of groundkeepers left after harvesting. Although not a particular focus of attention, there have been breeding programmes to develop BYV resistance and these have led to the introduction of such cultivars as Maris Vanguard. More recent research has been directed into transgenic sugarbeet which express virus-derived genetic material, for example, coat protein mediated resistance. It is not possible to estimate the cost of these cultural control measures or breeding programmes. One further indirect cost of BYV that should be considered is the cost of research programmes to investigate the biology of the disease and the cost of disseminating the results of this research and advising growers.