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 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.     

Identification of a second distinct strain of beet mild yellowing luteovirus using monoclonal antibodies and transmission studies

The variation among isolates of beet mild yellowing luteovirus (BMYV), collected from commercial crops of sugar beet during 1990, 1992 and 1993, was studied using monoclonal antibodies and transmissions to indicator species. The common strain of BMYV, which occurs throughout the sugar-beet root growing area, reacts with monoclonal antibodies MAFF 24, BWYV-BC-510H and BYDV-PAV-IL-1, and infects Capsella bursa-pastoris. A second strain, which failed to react with monoclonal antibody BYDV-PAV-IL-1 and which did not infect C. bursa-pastoris, was identified in 11% of sampled infected plants. The implications of the properties of this strain for the epidemiology of BMYV are discussed.     

The influence of size and duration of aphid infestation on host plant quality, and its effect on sugar beet yellowing virus epidemiology

This paper studies the influence of previous infestation on the host quality of sugar beet (Beta vulgaris L.) for aphids and the influence of previous infestation on sugar beet yellowing virus epidemiology. Sugar beet previously infested with Myzus persicae (Sulzer) or Aphis fabae Scopoli (Homoptera: Aphididae) had an improved host quality for subsequently infesting aphids of the same species. There was a significant negative relationship between the number of M. persicae infesting a plant and the proportion of those that died with a dark deposit in their stomachs, and a significant positive relationship between the number that settled on a plant and the number that infested it previously. Nymphs feeding on previously infested plants grew more rapidly than those on control plants. The beneficial effect of previous infestation persisted for at least 2 weeks and prolongation of the infestation beyond 2 weeks was of no further benefit to the aphids. Field grown sugar beet, previously colonised by M. persicae, was more susceptible to natural infestation by M. persicae up to 5 days after exposure. Previously infested plants were also more susceptible to infection with beet mild yellowing virus (BMYV) but not beet yellows virus (BYV), suggesting that the aphids on the previously infested sugar beet settled more readily and were more inclined to feed (and thus transmit BMYV) than aphids on the previously uninfested plants. The consequences for the control of sugar beet yellowing virus vectors are discussed.     

Detection of BMYV and BWYV isolates using monoclonal antibodies and radioactive RNA probes, and relationships among luteoviruses

In order to discriminate between sugar beet infecting beet mild yellowing virus (BMYV) and other isolates of beet western yellows virus (BWYV), monoclonal antibodies (MAbs) and radioactive riboprobes were used. With MAbs prepared against BMYV or potato leafroll virus (PLRV) no distinction could be established between BMYV and BWYV. Seven probes were synthesised from a lettuce infecting BWYV isolate; their localisation in the genome is known and they cover almost its entire length. Probes from the '3 part of the genome hybridised with all BMYV and BWYV isolates whereas those from the '5 part did not recognise BMYV isolates, showing that a divergent '5 region exists in the genomes of BMYV and BWYV. Probes also readily detected the virus in single aphids. The relevance of this finding for epidemiological studies is discussed.
MAbs and riboprobes were also tested against other luteoviruses (PLRV; barley yellow dwarf virus (BYDV) MAV, PAV and RPV strains). The serological relationship between BMYV and PLRV was confirmed and an epitope common to PLRV and BYDV-RPV was found. Using probes, PLRV and BYDV-RPV were found to share domains of homology with BWYV. BYDV-PAV showed weak homology with BWYV, while BYDV-MAV showed none.     

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.     

The effects of Beet mild yellowing virus and Beet chlorosis virus on the yield of UK field-grown sugar beet in 1997,1999 and 2000

The separate effects of the aphid‐transmitted poleroviruses; Beet mild yellowing virus (BMYV) and Beet chlorosis virus (BChV), on the yield of field‐grown sugar beet were studied following different inoculation dates from May to July in 1997,1999 and 2000. Each sugar beet plant within the appropriate plots was infected with virus using at least 10 wingless viruliferous Myzus persicae per plant. In all 3 years, overall yield losses caused by BMYV were negatively correlated with time of infection with early season (May) inoculations causing 18–27% losses in sugar yield but late season losses only 4–15%. BChV decreased the sugar yield and sugar content of beet following early season inoculations, although the effects on sugar yield were more variable (range 8–24%) and the virus appeared to be less damaging compared to BMYV. However, inoculations with BChV in July of each year caused greater root and sugar losses than inoculations with BMYV at that time. Both poleroviruses increased the sodium content of the roots early in the season, although neither virus had an effect on potassium levels at any stage.     

The effects of yellowing viruses on yield of sugar beet in field trials, 1985 and 1987

The separate effects of beet yellows virus (BYV) and beet mild yellowing virus (BMYV) on yield of sugar-beet cultivars inoculated at different growth stages were assessed in field trials in 1985 and 1987. Early or mid-season inoculation decreased sugar yield by up to 47% for BYV, and up to 29% for BMYV. Infections after the end of July had no significant effect on yield. Both viruses caused significant increases in the juice impurities sodium, potassium and amino-nitrogen after infecting plants early in the season. Yield losses associated with infection were determined by the causative virus, the time of infection, and susceptibility of the sugar-beet cultivars.     

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.     

Intraspecific variation of Myzus persicae on sugar beet (Beta vulgaris)

Differences in inherited resistance among seven sugar-beet stocks had similar effects on Myzus persicae clones representing the range of variation in aphid response to resistant and susceptible sugar beet observed in fifty-eight clones collected between 1969 and 1971. Three sugar-beet stocks were consistently resistant. Statistically significant interactions between beet stocks and aphid clones did not indicate the existence of biotypes with specific abilities to overcome resistance. M. persicae clones differed in their vigour of colonizing sugar beet, irrespective of the differences between beet stocks. The readiness of adult aphids to settle determined the size of aphid population produced and included a component related to the response of the aphid clone to sugar beet as a host, and a component related to the resistance ranking of the beet stock. Breeding sugar beet with resistance to aphids will be simplified, as the results indicate that, at present, differences between aphid biotypes need not be considered a problem.     

The occurrence of beet mild yellowing virus in Czechoslovakia

The occurrence of beet mild yellowing virus (BMYV) on feeding- and sugar-beet in Czechoslovakia has been proved. The virus was transmitted by aphidMyzus persicae (Sulz.) on indicator plantsSinapis alba L.,Capsella bursa-pastoris Medik, andClaytonia perfoliata Donn and from these plants back to sugar-beet cv. ‘Dobrovická A.’ A weed plantRaphanus raphanistrum L. was identified as a new natural host plant of BMYV. The virus was identified in ten of twelve biologically examined samples of beet with BMYV-like symptoms, which were collected at various places in Czechoslovakia     

Aphids from mangold clamps and their importance as vectors of beet viruses

Mangold clamps are over-wintering sources of the aphid-transmitted beet mosaic, beet yellows and beet mild yellowing viruses, and of several species of aphid, three of the most common in clamps being Myzus persicae, Rhopalosiphoninus staphyleae tulipaellus and R. latysiphon. This study attempted to assess the relative importance of the different species in spreading viruses from clamps. Compared with M. persicae, R. s. tulipaellus and R. latysiphon are seldom trapped in flight, except near large infestations. Alatae of M. persicae and R. s. tulipaellus become common in clamps in April, but few fly below 15d? C., a temperature seldom reached in eastern England in early spring. Flight muscle autolysis, which occurs later in R. s. tulipaellus and R. latysiphon than in some aphid species, also probably prevents many alatae in clamps from flying. We confirmed the importance of clamps as sources of beet viruses, the percentage of infected plants decreasing with increasing distance from infested clamps. M. persicae is shown to be a better vector of beet viruses than the other clamp aphids, and is probably responsible for most virus spread from clamps. R. s. tulipaellus did not transmit beet mosaic virus, but it is a fairly efficient vector of beet yellows and beet mild yellowing viruses, and, although we did not find this species on sugar beet in the field, it probably spreads these viruses from clamps. R. latysiphon did not transmit any of the viruses, and the role of Macrosiphum euphorbiae, Aulacorthum solani and Myxus ascalonicus is probably small.     

Serological Detection of Beet Western Yellows Luteovirus in the Non-vector,Brevicoryne brassicae (Homoptera: Aphididae)

The interaction between beet western yellows luteovirus (BWYV) and the aphid species Brevicoryne brassicae was investigated using virus transmission and serological detection experiments. This species failed to transmit a BWYV isolate from infected to healthy oilseed rape plants, although virus was readily detected by double-antibody sandwich enzyme-linked immunosorbent assay (DAS-ELISA) in single B. brassicae adults. When virus-carrying adults were tested by ELISA after different inoculation access periods, the number of virus-positive individuals decreased after 5 days, whereas with the efficient vector Myzus persicae, virus-positive individuals were found even after 10 days. This confirms the inability of B. brassicae to transmit BWYV, even though it may acquire the virus. It is suggested that B. brassicae, as compared with the efficient vector M. persicae, may serve as an experimental model for studying the mechanisms of the luteovirus-vector specificity     

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.     

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.     

Effects of the pyrethroid deltamethrin on the acquisition and inoculation of viruses by Myzus persicae

The pyrethroid, deltamethrin, alone or as an emulsifiable formulation, hindered infection of healthy plants with the persistent beet mild yellowing virus (BMYV) and both acquisition of, and infection with, the non-persistent potato virus Y (PVY) and the semi-persistent sugar beet yellows virus (BYV) by Myzus persicae in glasshouse tests.
Another pyrethroid, RU-15525, also protected against infection with PVY. Even sub-lethal amounts of deltamethrin decreased virus transmission by rapidly incapacitating the aphids, the effect being least with aphids most resistant to organophosphorous insecticides and to certain pyrethroids including deltamethrin. Demeton-S-methyl hindered infection only with BMYV. This work shows that deltamethrin restricts transmission of persistent, semi-persistent and perhaps more importantly of non-persistent viruses in the glasshouse, and has potential for doing the same in the field.     

Distribution and incidence of yellowing viruses in sugar beet crops in Spain from 1990 to 1993

Surveys of the principal yellowing viruses of sugar beet, beet yellows virus (BYV) and beet mild yellowing virus (BMYV) in Spain were carried out from 1990–1993. Beet yellowing viruses were detected in all provinces, although the mean percentages of plants infected with BYV and BMYV were practically zero in the southern zone. Within the northern zone high variations from one province to another could be observed. The mean percentages of plants infected with BYV were higher in the Ebro Valley than in the Duero Valley. Areas infected with BYV were very restricted, while BMYV could be found to a variable extent all over Spain, although the infection levels were lower. The incidence and distribution of these viruses in the Spanish sugar beet crop makes the study and application of control measures for beet yellowing viruses necessary.     

The influence of primary infection date and establishment of vector populations on the spread of yellowing viruses in sugar beet

In three field experiments in 1985 and 1986, we studied the effect of the date of primary infection on the spread of beet yellows closterovirus (BYV) and beet mild yellowing luteovirus (BMW) from artificially inoculated sugar beet plants. Laboratory-reared vector aphids, Myzus persicae, were placed on these sources of virus. There was no substantial natural immigration of vectors or viruses. In two experiments, one with BMYV in 1985 and the other in BYV in 1986, populations of vector aphids remained low and there was little virus spread, i.e. c. 50 infected plants from one primarily infected source. The cause of this small amount of spread was the low number of vector aphids. In the third experiment, with BYV in 1986, large populations of M. persicae developed and there was substantial virus spread: c. 2000 infected plants in the plots which were inoculated before canopy closure. In later-inoculated plots in the same experiment, there was much less spread: c. 100 infected plants per virus source plant. Differences between fields in predator impact are implicated as the most probable factor causing differences in vector establishment and virus spread between these three experiments. Virus spread decreased with later inoculation in all three experiments. A mathematical model of virus spread incorporating results from our work has been used to calculate how the initial proportion of infected plants in a crop affects the final virus incidence. This model takes into account the effect of predation on the development of the aphid populations. The processes underlying the spread and its timing are discussed.     

The control of Alternaria species on leaves of sugar beet infected with yellowing viruses

Leaves of virus-free sugar-beet plants rarely became infected with Alternaria spp. in two field experiments at Cambridge in 1965. Infection with beet yellows virus (BYV) increased susceptibility of plants to Alternaria only slightly but infection with beet mild yellowing virus (BMYV) increased it greatly. There was a close association between the severity of Alternaria symptoms, shown by different breeding lines and varieties of sugar beet, and the losses of sugar yield which they sustained after infection with BYV and BMYV. Many lines and varieties were resistant to Alternaria even when infected with BMYV and their resistance seemed to be inherited as a dominant character. Individual plants of any one line or variety differed greatly in resistance to Alternaria, suggesting that selection should improve the present level of resistance. Spraying the foliage of Alternaria-susceptible varieties with fungicides had little effect on the severity of Alternaria symptoms or on sugar yield. This was probably because the wet summer of 1965 was ideal for the spread of Alternaria and because rain washed the fungicide deposits from the sprayed leaves.     

Nucleotide sequence of beet western yellows virus RNA.

The nucleotide sequence of the genomic RNA (5641 nt) of beet western yellow virus (BWYV) isolated from lettuce has been determined and its genetic organization deduced. The sequence of the 3'terminal 2208 nt of RNA of a second BWYV isolate, obtained from sugarbeet, was also determined and was found to be very similar but not identical to that of the lettuce isolate. The complete sequence of BWYV RNA contains six long open reading frames (ORFs). A cluster of three of these ORFs, including the coat protein cistron, display extensive amino acid sequence homology with corresponding ORFs of a second luteovirus, the PAV isolate of barley yellow dwarf virus (BYDV) (1,2). The ORF corresponding to the putative viral RNA-dependant RNA polymerase, on the other hand, resembles that of southern bean mosaic virus. There is circumstantial evidence that expression of the BWYV RNA polymerase ORF may involve a translational frameshift mechanism. The ORF immediately following the coat protein cistron may be translated by in-frame readthrough of the coat protein cistron amber termination codon. Similar mechanisms have been proposed for expression of the corresponding ORFs of BYDV(PAV) (1).