THE SPREAD OF BEET YELLOWS AND BEET MOSAIC VIRUSES IN THE SUGAR-BEET ROOT CROP I. FIELD OBSERVATIONS ON THE VIRUS DISEASES OF SUGAR BEET AND THEIR VECTORS MYZUS PERSICAE SULZ. AND APHIS FABAE KOCH

A survey of aphids and virus diseases of sugar-beet root crops in eastern England was made between 1940 and 1948. Prior to 1943 the observations were made on fertilizer experiments; from 1943 onwards they were made on commercial fields selected for position in relation to beet and mangold seed crops. The incidence of beet yellows increased with increasing numbers of Myzus persicae , but not of Aphis fabae. The relation with M. persicae was sufficiently close to suggest that it is the most important, possibly the only important, vector of beet yellows virus. Beet mosaic virus also increased with increasing numbers of M. persicae , but the relation was not close enough to exclude the possibility of other vectors.
Numbers of A. fabae on sugar beet were slightly, but consistently, depressed by the use of salt as a fertilizer. Other fertilizers had variable effects. Neither aphids nor virus are likely to be greatly affected by fertilizers.
Beet yellows is most prevalent in areas where seed crops are grown, but within these areas nearness to individual seed crops did not appear to increase its incidence. M. persicae were more numerous on sugar beet in seed-crop areas than elsewhere, and this alone might account for the prevalence of yellows. Beet mosaic virus is more closely associated with seed crops than is beet yellows. It is most prevalent near to seed crops within the seed-crop areas.     

SUGAR-BEET YELLOWS: FURTHER STUDIES ON VIRUSES AND VIRUS STRAINS AND THEIR DISTRIBUTION IN EAST ANGLIA, 1958-59

Experiments have shown that, as in the years 1955-57, two yellowing viruses, beet yellows virus (SBYV) and sugar-beet mild yellowing virus (SBMYV), were present in commercial sugar-beet crops in East Anglia in 1958 and 1959. The evidence that they are not closely related viruses has been confirmed. In both years the prevalence of the two viruses was estimated by aphid transmissions from yellowed sugar-beet leaves to healthy sugar beet and Chenopodium capitatum seedlings in the glasshouse, and in 1959 additionally by examination of symptoms on field plants. SBMYV was more common than SBYV over the whole region in 1958, but in 1959 SBYV was slightly more prevalent than SBMYV. In both years SBYV was found more often in the southern than in the northern parts of the region. The results described in this paper suggest that breeding for tolerance to SBMYV may be at least as important economically in East Anglia as breeding for tolerance to SBYV. A wide range of SBYV strains was present in East Anglia in 1959, most of the strains being those which caused severe symptoms in sugar beet and C. capitatum.     

Some observations on the economic importance of sugar-beet downy mildew in England

Sugar-beet downy mildew is most prevalent in England in the sugar-beet and mangold seed-growing area of South Lincolnshire and West Norfolk. The most widespread and severe recent outbreaks were in 1957, and in 1965 when 6412 acres were reported with more than 10% infected plants. The fungus usually overwinters in sugar-beet and mangold seed crops, and in England other ways of overwintering are seldom important. Steckling beds are infected in the autumn, and the disease may increase rapidly in the seed crop in early spring. Summer-sown stecklings get more downy mildew than stecklings sown in spring under a cereal cover crop, and direct-drilled seed crops get more downy mildew than transplanted crops.     

Experiments on the time of application of insecticide to decrease the spread of yellowing viruses of sugar beet, 1954-66

Sprays of demeton-methyl insecticide decreased the spread of yellowing viruses by aphids in sugar-beet crops in England. Between 1957 and 1960, when yellows was prevalent, the incidence, assessed as ‘infected-plant-weeks’, was decreased by 36–41 % by one spray, depending on when it was applied, and by 55 % by two sprays, giving average yield increases of 1½ and 2 ton/acre of roots respectively. Between 1962 and 1966, when yellows spread less, a spray at the time when growers were advised to spray by the British Sugar Corporation decreased yellows incidence by 37 %, whereas sprays 2 weeks earlier or later decreased it by 24 % and 25 % respectively. Between 1958 and 1966 an annual average of 160000 of the country's 440000 acres of sugar beet has been sprayed, often to control Aphis fabae as well as to check the spread of yellows. A spray gives a profitable yield increase when yellows incidence in unsprayed plots is 20 % at the end of August.     

Some effects of spraying with thiabendazole on the susceptibility of sugar beet to yellowing viruses and on their vector, Myzus persicae (Sulz.)

In a field experiment fewer sugar-beet plants became infected with aphid-transmitted yellowing viruses in plots that had been sprayed with solutions of thiabendazole lactate than in water-sprayed plots, after exposure to natural infestation with aphids. Subsequent glasshouse tests showed that foliar sprays of o·o1 % thiabendazole lactate in water significantly reduced the proportion of inoculated sugar-beet plants which became infected with beet yellows virus (BYV) or beet mild yellowing virus (BMYV) after inoculation with viruliferous Myzus persicae (Sulz.). This effect on virus transmission was not apparently due to a direct insecticidal action of thiabendazole, because adult aphids usually survived equally well on sprayed and unsprayed plants. Treatment of test plants with thiabendazole did not affect the transmission of beet mosaic virus to them by M. persicae. The fecundity of M. persicae was greatly reduced by transferring them to plants which had been sprayed with thiabendazole or by spraying them with thiabendazole before transfer to unsprayed plants. The fertility of adult Aphis fabae Scop, was also reduced by spraying with thiabendazole. The mechanisms whereby thiabendazole affected fecundity of aphids and transmission of viruses are not understood.     

Studies on beet western yellows virus in oilseed rape (Brassica napus ssp. oleifera) and sugar beet (Beta vulgaris)

Oilseed rape (Brassica napus L. ssp. oleifera) was studied as a potential overwintering host for the sugar-beet yellowing viruses, beet yellows virus (BYV) and beet mild yellowing virus (BMYV), and their principal vector, Myzus persicae. In spring 1982, plants infected with a virus which reacted positively in enzyme-linked immunosorbent assay (ELISA) with BMYV antibody globulin were found in oilseed-rape crops; none of the plants contained virus which reacted with BYV antibody globulin. This virus was subsequently identified as beet western yellows virus (BWYV). No leaf symptoms could be consistently associated with infection of oilseed rape, but the virus was reliably detected by sampling any leaf on an infected oilseed-rape plant. Some isolates from oilseed rape did infect sugar beet in glasshouse tests, but the proportions of inoculated plants which became infected were low. Apparently there is therefore little danger of much direct transmission of BWYV by M. persicae from oilseed rape to sugar beet in spring. BWYV was introduced to and spread within oilseed-rape crops in autumn by M. persicae, and autumn-sown oilseed rape proved to be a potentially important overwintering host for M. persicae. In a survey of 80 autumn-sown crops of oilseed rape in East Anglia, northern England and Scotland in spring 1983, 78 were shown to be extensively infected with BWYV. Experimental plots of oilseed rape with 100% BWYV-infection yielded approximately 13.4% less oil than plots with 18% virus infection, the result of a decrease in both seed yield and oil content.     

THE INFLUENCE OF DENSITY OF PLANT POPULATION ON THE INCIDENCE OF YELLOWS IN SUGAR-BEET CROPS

The incidence of yellows virus in sugar-beet crops was reduced by increasing the density of plant population. The variations in plant population were obtained by differences in row width and singling distance. The differences in susceptibility between large- and small-topped varieties, and between early and late sown crops, could not be attributed solely to differences in plant size. It is suggested that close planting would increase the yields of sugar beet and reduce the losses caused by yellows virus. Roguing infected plants during the early part of the growing season did not reduce the incidence of disease.     

Experiments with fungicide sprays in late summer and early autumn on sugar-beet root crops

Fentinhydroxide and benomyl sprayed on to sugar-beet root crops in July, August and September frequently increased yield of tops. Sugar yield was increased only if either powdery mildew or virus yellows was prevalent, when on average a single fentinhydroxide spray at 0·7 kg a.i./ha increased sugar yield by 8% and yield of tops by 13%. The mildew specific fungicide fluotrimazole also increased yield, but it could not be determined whether this was due to controlling powdery mildew or secondary parasitic fungi attacking yellows-infected plants. Repeated sprays of both fentinhydroxide and fluotrimazole, but not benomyl, appeared to be phytotoxic when applied in hot dry weather.     

Some factors affecting germination of Peronospora farinosa conidia in water

The germination of conidia of Peronospora farinosa f. sp. betae, collected from sugar beet and suspended in deionized water, was inhibited by dilution with 10% solutions of glycerol, glucose or sucrose and with sap from sugar-beet leaves. Germination was stimulated by diluting with deionized water but not with tap water or biological saline. Substances that diffused from excised buds of sugar-beet plants into deionized water also stimulated germination of conidia but diffusates from leaves did not. This may partly explain why buds are more susceptible to downy mildew than leaves in sugar beet. Germination of conidia was apparently stimulated more by diffusates from buds of seedlings than by those from buds of older plants; this may help to explain why sugar-beet seedlings are more susceptible to downy mildew than older plants. Diffusates from plants of four sugar-beet stocks, that differed from each other in susceptibility to downy mildew, had very similar effects on germination of P. farinosa conidia. Stimulation of spore germination on the surfaces of buds and leaves did not seem, therefore, to be an important factor in determining resistance or susceptibility to downy mildew in these stocks.     

EXPERIMENTS ON THE CONTROL OF BEET YELLOWS VIRUS IN SUGAR-BEET SEED CROPS BY INSECTICIDAL SPRAYS

Field experiments made in eastern England between 1943 and 1951 showed that Myzus persicae lived on the stecklings throughout some winters, and that most plants with yellows in transplanted seed crops were from infections that occurred in the steckling bed. A larger proportion of stecklings sown at the end of July or in early August became infected than of those sown about a month later. The incidence of yellows was reduced by nicotine sprays which cleared the stecklings of aphids after autumn migrations had ceased, thus preventing spread of the disease during the winter. A greater reduction was obtained with persistent and systemic organo-phosphorous insecticides; in one experiment three applications of E 605 reduced incidence to one-ninth that in unsprayed plots. However, in years when stecklings were exposed to large migrations of aphids, even plots sprayed three times had 78% of the plants with yellows. Although spraying often greatly reduces the incidence of yellows, it is unlikely to give adequate control in years and districts in which many viruliferous aphids move in the autumn. Spraying in September and October was usually more effective than in August.     

Breeding for resistance to infection with yellowing viruses in sugar beet

Differences in resistance to infection with beet yellows virus (BYV) and beet mild yellowing virus (BMYV) have been observed in virus-tolerant sugar-beet breeding material. The results of glasshouse virus-susceptibility tests usually agreed well with those of field experiments in which plants were exposed to artificial, or natural, infestation with viruliferous aphids. Breeding lines and varieties, which showed resistance to BYV when Myzus persicae Sulz, was used as vector, generally showed a similar resistance to this virus when Aphis fabae Scop. was used. Varieties which were resistant to infection with one virus were not necessarily resistant to the other, although some showed resistance to both BYV and BMYV. Preliminary results suggest that resistance to infection may be controlled by recessive genes which occur widely in sugar-beet cultivars. The mechanism of this form of resistance is not understood, but it does not appear to be closely associated with resistance to the aphid vectors of the viruses. The observed differences in resistance to infection demonstrate the possibility of breeding a sugar-beet variety in which two forms of resistance to virus yellows, tolerance and resistance to infection, are combined.     

Effects of sucrose sprays and darkness on aphid colonization of sugar beet and on aphid transmission of yellowing viruses

In the glasshouse, adult, apterous Myzus persicae (Sulz.) and Aphis fabae Scop, settled better and deposited more larvae on sucrose-sprayed sugar-beet plants than on water-sprayed plants. M. persicae settled badly and deposited few larvae on plants that were kept in the dark before or after infestation. The effects of darkness on aphids were reduced by spraying the host plants with 10% solutions of sucrose before infestation. Viruliferous M. persicae transmitted beet yellows virus (BYV) and beet mild yellowing virus (BMYV) less efficiently to dark-treated plants than to those grown in normal daylight. Spraying sugar beet with sucrose before inoculation with viruliferous M. persicae increased the proportion of successful BYV transmissions but only when the plants were dark-treated. The effects of sucrose and darkness on settling and larviposition of aphids and on virus transmission may be related to changes in the concentration of carbohydrates, particularly sugars, in the leaves.     

The use of weather data and counts of aphids in the field to predict the incidence of yellowing viruses of sugar-beet crops in England in relation to the use of insecticides

Partial regression equations were calculated that relate the mean percentage of plants infected with yellowing viruses (beet yellows and beet mild yellowing viruses) in sugar-beet crops at the end of August to the number of days during January, February and March when temperatures fell below – 0.3 °C (31-5 °F) and the mean temperatures in April, for the 21 yr, 1951–71, using weather records from Rothamsted Experimental Station. Regression analyses were also made to find the effect of other factors including mean and minimum temperatures for the same months, and also mean counts of ‘green aphids’, mainly of the vector Myzus persicae, on sugar-beet plants during May and June. Significant relationships were established with all factors, but ‘frost-days’ and April mean temperatures accounted for the greatest percentage of the variance in yellows incidence. The calculations were made separately for the years from 1951 to 1958, when no routine advice was given to farmers about aphid control, and 1959–71 when a ‘spray-warning scheme’ was in operation, and many crops were sprayed at critical times to prevent aphid- and virus-spread. Weather factors had the same effects in both periods, but for any particular weather less virus was spread in the second period than in the first, although there were sufficient aphids, i.e. the numbers expected from the prevailing weather conditions. There was no evidence that insecticide treatment used in any one year affected aphid-incidence in subsequent years. Regression analyses on weather variables were also calculated separately for each of seventeen beet-sugar factory collection-areas, using weather records from local weather stations, and also the Rothamsted weather records. Unexpectedly, the fit of the regressions was always better with Rothamsted weather data than with local weather records. Mean yellows-incidence for the different factory areas declined from south to north, and there was a linear relationship with the square root of the latitude above 50 °C. At the same time the correlation coefficients relating yellows-incidence to ‘frost-days’ became smaller and less significant, and those showing dependence     

Field experiments on sugar-beet powdery mildew, Erysiphe betae

Sugar-beet powdery mildew, Erysiphe betae appeared in East Anglia in late July 1976 and became wide-spread in eastern England during August and September but was scarce in crops in the north and west of England. Fentinhydroxide, sulphur, benomyl and ethirimol controlled the disease but benomyl applied once only and ethirimol were less effective than the other materials. In heavily infected crops two sulphur sprays, the first applied at the onset of the mildew attack, increased sugar yield by 13%. A single early sulphur spray increased yield on average by 9% giving a return of six to seven times the cost of treatment. When the first spray was delayed, mildew control was less effective.     

SUGAR BEET YELLOWS: A PRELIMINARY STUDY OF THE DISTRIBUTION AND INTERRELATIONSHIPS OF VIRUSES AND VIRUS STRAINS FOUND IN EAST ANGLIA, 1955-57

Aphid transmissions to sugar beet seedlings from yellowed sugar beet leaves collected from commercial fields in East Anglia during the summers of 1955, 1956 and 1957, showed the occurrence of two yellowing viruses. One was sugar beet yellows virus (SBYV) and produced vein-etch and yellowing symptoms on beet seedlings in the glasshouse; the other produced yellowing but no etch. These two viruses were apparently unrelated, so that sugar beet tolerant to one of them would not necessarily be tolerant to the other. The second virus, called 'sugar beet mild yellowing virus' (SBMYV), decreased the root yield of sugar beet plants grown under glass, by as much as did the milder SBYV strains, but less than did the severe SBYV strains. The proportions of the two viruses in the samples differed from year to year and from place to place.     

The use of menazon seed dressing to decrease spread of virus yellows in sugar-beet root crops

Menazon, an organophosphorus insecticide (only slightly toxic to mammals), applied to sugar-beet seed, decreased the proportion of seedlings infested with aphids during May and early June and the number of aphids per plant during June and early July to one-third of that in the control plots. It also checked the spread of virus yellows. Of eight field trials in 1965, 1966 and 1967 in which more than 10% of the plants in plots not treated with insecticide had yellows, menazon seed dressing increased sugar yield by about 8 cwt per acre. Spraying with demeton-methyl when ‘a spray warning’ was issued in the area gave a similar increase, and had no further effect on plots sown with menazon-treated seed. Menazon-dressed sugar-beet seed is recommended in regions where yellows is usually prevalent, or where there is reason to expect a large aphid infestation.     

THE DISTRIBUTION OF VIRUSES IN DIFFERENT LEAF TISSUES AND ITS INFLUENCE ON VIRUS TRANSMISSION BY APHIDS

Exposing both surfaces of leaves systemically infected with cabbage black ring spot virus (CBRSV) or henbane mosaic virus to ultra-violet radiation decreases the infectivity of expressed sap to about one-fifth. As irradiation probably inactivates virus mainly in the epidermis, which occupies about one-quarter the volume of the leaves, these viruses seem to occur at much higher concentrations in sap from the epidermis than in sap from other cells. By contrast, tobacco mosaic virus seems not to occur predominantly in the epidermis.
CBRSV and henbane mosaic virus are normally transmitted most frequently by previously fasted aphids that feed for only short periods on infected leaves, but aphids treated like this transmit rarely from leaves that have been exposed to ultraviolet radiation. Irradiation has relatively little effect on the proportion of aphids that transmit after long infection feedings. Fasting seems to increase transmission by increasing the probability that aphids will imbibe sap from the epidermis of leaves they newly colonize. With longer periods on infected leaves, the ability of fasted aphids to transmit probably decreases because they then feed from deeper cells and their stylets contain sap with less virus. Only virus contained in the stylets seems to be transmitted, not virus taken into the stomach. About half the transmissions of henbane mosaic virus by aphids that have colonized tobacco leaves for hours may be caused by insects that temporarily cease feeding on the phloem and newly penetrate the epidermis.
Irradiating infected leaves affected the transmission of sugar-beet mosaic virus in the same way as that of henbane mosaic virus, but had little effect on the transmission of beet yellows virus, whose vectors become more likely to transmit the longer they feed on infected plants.     

THE EFFECT OF SUCROSE SPRAYING ON SYMPTOMS CAUSED BY BEET YELLOWS VIRUS IN SUGAR BEET

When leaves of sugar-beet plants infected with beet yellows virus were sprayed daily with 10% sucrose solution, yellowing symptoms were intensified. When glasshouse plants were shaded so that the light intensity was reduced to less than half of full daylight, yellowing symptoms were suppressed more completely on un-sprayed than on sprayed plants. Spraying with 2–5 % sucrose solution had similar, but slightly smaller effects.
Spraying with sucrose solution increased the carbohydrate content of the leaves, and the effects on symptom intensity and carbohydrate content were closely correlated. The regression coefficients of symptom score on total sugar content were nearly the same for shaded and unshaded plants. As the severity of symptoms was increased by supplying carbohydrate without change in the light conditions, it is concluded that light intensity affects symptom expression by varying the carbohydrate content of the leaves through its influence on photosynthesis.
Sucrose spraying increased the yield of roots of healthy and infected plants, and most of the increase was sucrose. This shows that sprayed sugar was translocated to the roots from the leaves of both healthy and infected plants.
Measurements of changes in carbohydrate content between evening and morning samplings confirmed that movement of carbohydrate out of infected leaves is not stopped by infection.     

The influence of foliar applications of sugars on the susceptibility of sugar beet to downy mildew

Spraying sugar-beet seedlings in the glasshouse, with 1% or 10% solutions of sucrose, 24 h before inoculation with Peronospora farinosa, significantly reduced their susceptibility to downy mildew. The proportion of inoculated plants that became infected was reduced by spraying with sucrose but the main effect was the inhibition of sporulation. Applications of glucose or fructose also increased the resistance of beet seedlings to P. farinosa. Spraying with sucrose 1 or 2 days before inoculation was much more effective than was spraying shortly before inoculation, or 24 h afterwards, or adding sucrose to the inoculum. Washing sucrose-sprayed seedlings with distilled water 1–2 h before inoculation removed only part of the effect of sucrose on sporulation. Although the mechanism by which applications of sugars affected susceptibility to downy mildew is not understood, the results suggest that the main effects occurred inside the host plant rather than externally. The possible significance of these results, in breeding for resistance to downy mildew and in the control of this disease in the field, is discussed.     

The use of monoclonal antibodies to detect beet mild yellowing virus and beet western yellows virus in aphids

Information on infectivity of the aphids which invade sugar beet root crops each Spring is required for forecasting incidence and providing advice on control of virus yellows. Monoclonal antibodies, produced in the USA to barley yellow dwarf virus (BYDV) and in Canada to beet western yellows virus (BWYV), were used to distinguish between sugar-beet-infecting strains of the luteovirus beet mild yellowing virus (BMYV), and the non-beet-infecting strains of the closely-related BWYV in plant and aphid tissue. Totals of 773 immigrant winged Myzuspersicae and 124 Macrosiphum euphorbiae were caught in water traps in a crop of sugar beet between 25 April and 5 August 1990. Using the monoclonal antibodies and an amplified ELISA, 67%M. persicae and 19%M. euphorbiae were shown to contain BWYV; 8%M. persicae and 7%M. euphorbiae contained BMYV. In studies with live winged aphids collected from the same sugar beet field during May, 25 of 60 M. persicae and two of 13 M. euphorbiae transmitted BWYV to the indicator host plant Montia perfoliata; two M. persicae and two M. euphorbiae transmitted BMYV. In another study three of 65 M. persicae and one of three M. euphorbiae in which only BWYV was detected, transmitted this virus to sugar beet.