113Ann. appl. Biol. (2004), 144:113-119Printed in UK

*Corresponding Author E-mail: mark.stevens@bbsrc.ac.uk

© 2004 Association of Applied Biologists

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

By MARK STEVENS*, PHILIPPA B HALLSWORTH and HELEN G SMITH

Broom�s Barn Research Station, Higham, Bury St. Edmunds, Suffolk IP28 6NP, UK

(Accepted 21 October 2003; Revised Version Received 17 August 2003)

Summary

The separate effects of the aphid-transmitted poleroviruses; Beet mild yellowing virus (BMYV) andBeet chlorosis virus (BChV), on the yield of field-grown sugar beet were studied following differentinoculation dates from May to July in 1997, 1999 and 2000. Each sugar beet plant within the appropriateplots was infected with virus using at least 10 wingless viruliferous Myzus persicae per plant. In all 3years, overall yield losses caused by BMYV were negatively correlated with time of infection withearly 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 lessdamaging compared to BMYV. However, inoculations with BChV in July of each year caused greaterroot and sugar losses than inoculations with BMYV at that time. Both poleroviruses increased thesodium content of the roots early in the season, although neither virus had an effect on potassiumlevels at any stage.

Key words: Luteoviridae, Polerovirus, Myzus persicae, yield trial

Introduction

One of the most important diseases of the UKsugar beet crop is �virus yellows� which decreasesthe root weight and sugar percentage of infectedplants and also has a detrimental effect on the sugarextraction process at the factories. The viruses mostcommonly involved in the disease complex are Beetmild yellowing virus (BMYV), which belongs to thegenus Polerovirus in the Luteoviridae family, andBeet yellows virus (BYV, family Closteroviridae,genus Closterovirus); BMYV is found morefrequently than BYV in commercial beet crops innorth-west Europe (Smith & Hinckes, 1987; Stevenset al., 1997). Both viruses are transmitted by aphids,primarily Myzus persicae. In trials conducted in 1985and 1987, Smith & Hallsworth (1990) found thatearly inoculation of sugar beet with BMYVdecreased sugar yield by up to 29%, althoughinoculations after the end of July had no significanteffect on yield.

In 1989, a virus which exhibited symptoms of paleyellowing rather than the normal golden yellowdiscoloration associated with BMYV infection wasfound in the UK, and was identified as a strain ofBMYV on the basis of its biological, serological andmolecular properties (Stevens et al., 1994; Hauseret al., 2000b). Surveys of British sugar beet crops inthe early 1990s showed that this strain of BMYVwas present in 11% of infected leaves. Its host range

is narrower and appears to be confined to Betaspecies; the traditional indicator species for BMYV,Capsella bursa-pastoris and Montia perfoliata, arenot susceptible. Further studies of the biological andmolecular properties of this strain showed that itdiffers significantly from BMYV, and has recentlybeen ratified as a new species within the Polerovirusgenus, for which the name Beet chlorosis virus(BChV) has been accepted (Hauser et al., 2000b,2002).

Each year the sugar beet industry requiresinformation on the effect of virus yellows on thenational yield of sugar, and the occurrence anddistribution of the yellowing viruses. The effects ofBChV on the yield of UK sugar beet are unknownand this paper describes the results of field trials in1997, 1999 and 2000 to compare the effects ofBMYV and BChV on yield of sugar beet wheninoculated at different times during the growingseason, so that the economic importance of this newdisease can be assessed.

Materials and Methods

Virus sources and aphid inoculationBMYV and BChV cultures were maintained in

separate compartments of the glasshouse and all plantswere kept inside clear aphid-proof Perspex® cages.Prior to inoculating the field trials, BMYV originatingfrom several UK isolates collected from different

114 MARK STEVENS ET AL.

growing regions and that exhibited the samebiological, serological and molecular characteristicswere mixed to produce a stock culture that wasmaintained in C. bursa-pastoris which is a better hostthan sugar beet for BMYV. BChV originating from acommercial crop of sugar beet at Broom�s Barn in1994 was kept in sugar beet since it does not infect C.bursa-pastoris. M. persicae, which had previouslybeen raised on chinese cabbage (Brassica pekinensisRupr. cv. Pe-Tsai), were placed on the virus-infectedC. bursa-pastoris and sugar beet plants and allowedto feed for up to 10 days. In the field, each plant in theappropriate plots was inoculated by placing into itsheart leaves a piece of BMYV-infected C. bursa-pastoris or BChV-infected sugar beet leaf on whichthere were at least 10 wingless M. persicae. To avoidcross-contamination the viruses were inoculated ondifferent days. The aphids were subsequentlycontrolled 48 h after inoculation by spraying with theaphicide pirimicarb at 280 g a.i. ha-1. To minimise therisk of virus spread to the untreated plots andneighbouring field experiments, the trial was sprayedwith the same insecticide each month, from May toAugust. The crops received standard treatments offertiliser and herbicide.

Field trialsIn 1997, the field trial was sown on 2 April with the

sugar beet variety cv. Zulu at Broom�s Barn ResearchStation. Plots were drilled to stand with a seed spacingof 18.2 cm and a row width of 50 cm. Plots, 6 rowsby 12 m, were inoculated with BMYV on 22 May, 17June and 16 July and with BChV on 21 May, 18 Juneand 17 July respectively. Control plots were leftuninoculated. In each trial there were four replicatesof each treatment and all guard rows of sugar beetsurrounding the virus and control plots were sownwith sugar beet seed treated with the insecticideimidacloprid (Gaucho) at 90 g a.i. unit-1 of seed tominimise virus spread. The trial was harvested bymachine on 14 January 1998, which sampled 4 rowsby 8 m of the inoculated area of each plot.

The second trial was sown on 2 April 1999, usingthe variety Roberta; the same trial design was used asin 1997. The appropriate plots were inoculated withBMYV on 19 May, 15 June and 14 July followed byBChV on 20 May, 16 June and 15 July respectively.On 9 November four rows by 9.7 m were machineharvested.

In 2000, the trial was sown on 21 March using thesame layout and sugar beet variety as in 1999. As inprevious years four replicate plots were inoculatedwith BMYV on 19 May, 14 June and 11 July andwith BChV on 17 May, 13 June and 10 Julyrespectively. Due to the wet autumn the trial had tobe harvested by hand on 11 December when six rowsby 8 m were sampled per plot.

Monitoring of infectionIn 1997 all plants in the trial plots were assessed

for symptoms on 6 October. In 1999 and 2000, allplants in the plots were examined each month fromJune to September, and the number of beet with yellowleaves recorded. To determine whether the BChV plotshad also become cross-infected with BMYV, 10-20randomly-selected leaves were harvested fromindividual plants in each plot and tested by ELISAusing monoclonal antibodies MAFF 24 (Smith et al.,1996) and BYDV-PAV-IL-1 (D�Arcy et al., 1989).Antibody MAFF 24 detects all polerovirus strains,but BYDV-PAV-IL-1 does not react with BChV(Stevens et al., 1994).

Assessment of yieldAll roots from each plot (approximately 120) were

washed and weighed and their sugar concentrationdetermined polarimetrically (Le Docte, 1927).Impurities were also determined (milliequivalents per100 g of storage root), amino-nitrogen colori-metrically using the ninhydrin method (Detavernier,1979), and sodium and potassium by flame-emissionphotometry (Carruthers & Oldfield, 1961). All datawere analysed using the statistical package, GenstatTM 5, Release 3 (Payne et al., 1993) and the three trialswere analysed as four blocks of seven treatments.Multiple regression analyses were performed on rootand sugar yields by treating the viruses and years asfactors. The inoculation dates were converted intovariate with the first date of inoculation being recordedas day zero. A general regression model wasformulated and analysed statistically.

Results

Symptom assessmentsOn 6 October 1997, the percentage number of sugar

beet plants showing typical symptoms that had beeninoculated between May and July ranged from 87%to 100% (Table 1). Virus symptoms were alsoobserved in the uninoculated plots and by October34% of the uninoculated plants were showing typicalpolerovirus symptoms; ELISA was used to confirmthat the yellow symptoms were caused by bothpoleroviruses (data not shown).

In 1999 and 2000, plots were assessed monthly fromlate June until late September to determine the rate ofsymptom development during the season (Table 1).Again the early inoculated plots (May and June)exhibited the highest levels of virus incidence. Bythe end of July each year up to 6% of the uninoculatedplants were showing yellow symptoms; however bythe end of September this had increased to 28% in1999 and 13% in 2000 despite regular applicationsof pirimicarb.

115Effects of yellowing viruses on yield of sugar beet

Effect of BMYV and BChV on root qualityIn 2000, both BMYV and BChV significantly

increased the sodium content of the roots regardlessof inoculation date (Tables 2-4). However, in 1999only the earlier inoculations with the two viruses hada significant impact on sodium content, and in 1997only the May inoculation with BMYV had the sameeffect. In 1999 and 2000 BMYV significantlyincreased the amino-nitrogen content of roots,although this effect was only observed with earlyBChV inoculations in 2000. No clear trend wasobserved with the potassium content of the roots butin most circumstances virus infection did notsignificantly increase or decrease this impurity in theroots.

Discussion

These trials have shown that both BMYV andBChV significantly decreased the root weights andsugar yields of field-grown sugar beet, and increasedthe juice impurity levels, particularly of sodium, inthe roots in 2 of the 3 years. Overall, highest yieldlosses were experienced when sugar beet plants wereinoculated at an early growth stage. However, theeffects of BChV on yield were more variable thanBMYV during the 3 years. From these results itappeared that BChV was less damaging than BMYVwhen plants were inoculated in mid-May, but Julyinoculations with BChV had a greater effect on yieldthan BMYV, particularly on the variety Zulu. BChVproduces paler symptoms than BMYV and often leaftissue around the midrib and lateral veins remainsgreen, which could enable such leaves to maintain agreater photosynthetic potential than BMYV-infectedleaves early in the season. However, it is unclear why

Confirmation of BChV infectionIn 1997 and 1999 between 7.5% and 30% of leaves

collected from plants originally inoculated with BChVreacted with both monoclonal antibodies, indicatingthat these samples also contained BMYV (Fig. 1). In2000, the level of mixed infection in plants rangedfrom zero to 7.5%. More than 97% of plantsinoculated with BChV in May and June, irrespectiveof year, were found to contain this virus in Septemberwhen tested by ELISA. Up to 12.5% of the samplescollected in 1997 and 1999 from the BChV plotsinoculated in mid-July did not react with eitherantibody; this increased to 21% in 2000, even thoughmost leaves exhibited yellow symptoms.

YieldEarly infection with BMYV, especially at the 4-6

leaf stage, significantly decreased root weight, sugarconcentration and therefore the sugar yields of theroots by 19-27% in the three trials (Tables 2-4)compared to the uninoculated controls. Laterinoculations with BMYV had progressively less effecton yield (Tables 2-4), but the size of these yield lossesvaried between years. Throughout the trials BChVhad a more variable effect on sugar yield; for example,May inoculations decreased sugar yield between 7.9%to 24.1%. However, in all 3 years BChV had a greatereffect on yield than BMYV following inoculation inmid-July, significantly different compared to BMYVin 1997. Regression analyses on root and sugar yieldwere performed using GENSTAT (version 5) with theregression model: yield (root or sugar) = constant +virus + year + days + virus*days. The obtainedregression formulae accounted for 78.2% and 70.6%of the variability of the root and sugar yield datarespectively (Figs 2 and 3).

Inoculation DateDate of Virus May June July UninoculatedAssessment BMYV BChV BMYV BChV BMYV BChV control

19976/10 100a 90.7 92.2 92.7 87.7 91.2 34.2199923/6 81.4 88.6 1.4 3.2 1.5 2.9 0.726/7 93.4 88.9 97.6 100 6.4 18.2 4.526/8 100 98.6 100 97.8 43.7 84.5 26.027/9 100 100 100 100 95.4 97.8 28.1200026/6 84.9 81.0 0.6 2.6 3.1 0 0.725/7 100 100 100 100 10.3 1.8 6.229/8 100 100 100 100 81.8 99.3 7.625/9 100 100 100 100 94.5 100 12.9

Table 1. Proportion of plants within each plot exhibiting virus yellows symptoms

a Figures in bold indicate inoculated plots at time of virus count

116 MARK STEVENS ET AL.

BChV was more damaging to the crop compared toBMYV later in the season. There was no differencein the rate of symptom development during the season,and further work is required to examine the effectsthese poleroviruses have on the physiology andphotosynthetic efficiencies of infected plants.

Alignment of the full length nucleotide sequencesof BMYV (Guilley et al., 1995) and BChV (Hauseret al., 2002) shows that the two virus species areclosely related within the 3' end of their genomes.This region includes the coat protein and readthroughdomain as well as an open reading frame whichencodes a protein (ORF4) that has been shown to beinvolved in virus movement for certain poleroviruses(Taliansky & Barker, 1999). In contrast, there is less

than 30% sequence homology within the 5' end ofthe two genomes; it is thought that the pathogenicityand host range determinants of the beet polerovirusesare located within this region (Sadowy et al., 2001),which could explain the differences in host specificity.

The trials were sprayed with insecticide after eachset of inoculations and the seed used for the guard

Fig. 3. The effects of BMYV and BChV on sugar yield in1997, 1999 and 2000. Day 0 is equivalent to the first in-oculations undertaken in mid-May and subsequent pointsat approximately day 30 and day 60 relate to infectionsundertaken in June and July each year. R2 = 70.65%

13.0

12.5

12.0

11.5

11.0

8.5

8.00 10 20 30 40 50 60

Days

t ha-1

10.5

10.0

9.5

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BChV, 2000BChV, 1999BChV, 1997BMYV, 2000BMYV, 1999BMYV, 1997

100

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60

40

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0

100

80

60

40

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0

May June July

May June July

May June July

1997

1999

2000

Inoculation dateFig. 1. Contamination of plots originally inoculated withBChV as measured by ELISA at the end of September.Grey shading = BChVBlack shading = BMYV/BChVNo shading = No virus

% p

lant

s in

fect

ed

Fig. 2. The effects of BMYV and BChV on root yield in1997, 1999 and 2000. Day 0 is equivalent to the first in-oculations undertaken in mid-May and subsequent pointsat approximately day 30 and day 60 relate to infectionsundertaken in June and July each year. R2 = 78.2%

80

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BChV, 2000BChV, 1999BChV, 1997BMYV, 2000BMYV, 1999BMYV, 1997

117Effects of yellowing viruses on yield of sugar beet

rows surrounding the plots was treated with theinsecticide imidacloprid which protects the plantsfrom aphid colonisation for up to 10 wk after sowing(Westwood et al., 1998). However, each year plantswithin the control plots became infected with virus,and some of the beet inoculated with BChV alsocontained BMYV. Winged virus-carrying migrantaphids alighting in these plots between insecticidetreatments could have established sources of infectionand spread the virus across the plots. However, most

of the virus infection recorded in the untreated plotsdid not appear until August and hence would not haveaffected the yield of these plots significantly; any yieldloss in the untreated plots would actually cause anunderestimation of the effects of BMYV and BChVon final yield. These problems indicate the difficultiesof undertaking such trials with aphid-borne viruses,even when strict hygiene control measures arefollowed.

In these trials, it was not possible to determine the

Table 3. The effects of sequential inoculations with BMYV and BChV on root and sugar yields, and juiceimpurities (milliequivalents per 100 g storage root) during 1999

aDates when sugar beet plots were inoculated with either BMYV or BChVbMean effect of both viruses for each set of inoculations between May and JulycAverage effect of each virus for all inoculation dates

Date Root Yield t ha-1 Sugar % Sugar yield t ha-1 Sodium Potassium Amimo-N

Control 76.9 17.20 13.22 0.72 3.38 0.6419 Maya 61.9 15.61 9.66 1.31 3.53 0.9015 June 64.9 15.93 10.34 1.12 3.33 0.91

BMYV

14 July 76.0 16.61 12.62 0.76 3.18 0.6820 Maya 65.1 16.27 10.59 1.14 3.58 0.7416 June 64.7 16.21 10.48 0.98 3.41 0.69

BChV

15 July 72.8 16.31 11.87 0.80 3.40 0.69SED (17 df) 2.61 0.230 0.455 0.108 0.133 0.105

Mayb 63.5 15.94 10.12 1.22 3.55 0.82June 64.8 16.07 10.41 1.05 3.37 0.80July 74.4 16.46 12.25 0.78 3.29 0.69

SED (17 df) 1.85 0.163 0.322 0.076 0.094 0.074BMYVc 67.6 16.05 10.87 1.06 3.34 0.83BChV 67.5 16.26 10.98 0.97 3.46 0.71SED (17 df) 1.51 0.133 0.263 0.062 0.077 0.061

a Dates when sugar beet plots were inoculated with either BMYV or BChVb Mean effect of both viruses for each set of inoculations between May and JulycAverage effect of each virus for all inoculation dates

Table 2. The effects of sequential inoculations with BMYV and BChV on root and sugar yields, and juiceimpurities (milliequivalents per 100 g storage root) during 1997

Date Root Yield t ha-1 Sugar % Sugar yield t ha-1 Sodium Potassium Amimo-N

Control 67.4 16.34 11.02 1.84 3.50 1.8622 Maya 58.1 15.45 8.97 2.04 3.37 1.9017 June 59.6 15.68 9.34 1.89 3.32 1.82

BMYV

16 July 66.1 15.95 10.56 1.71 3.47 1.7821 Maya 63.2 16.07 10.15 1.77 3.40 1.7918 June 61.8 16.05 9.92 1.86 3.50 1.93

BChV

17 July 60.0 16.06 9.63 1.94 3.20 1.53SED (18 df) 1.81 0.194 0.306 0.146 0.141 0.077

Mayb 60.6 15.76 9.56 1.90 3.39 1.84June 60.7 15.87 9.63 1.87 3.41 1.88July 63.1 16.01 10.10 1.82 3.34 1.65

SED (18 df) 1.28 0.137 0.216 0.103 0.100 0.054BMYVc 61.2 15.69 9.62 1.88 3.39 1.83BChV 61.7 16.06 9.90 1.85 3.37 1.75SED (18 df) 1.05 0.112 0.177 0.084 0.081 0.044

118 MARK STEVENS ET AL.

level of cross-contamination of BChV within theBMYV plots, or to assess whether plants were doublyinfected in the untreated plots because BChV-specificantibodies were unavailable; this is a current researchtarget. Recently PCR primers have been designed forthe two polerovirus genomes that can be used in RT-PCR to detect and distinguish BMYV and BChV(Hauser et al., 2000a) and these will be used in futureexperiments to confirm mixed infections.

All recommended and provisionally-recommendedsugar beet varieties are assessed for disease resistancein trials conducted by the National Institute ofAgricultural Botany (NIAB). At present, there are nocommercial varieties available that are resistant toBMYV, although this is a target for the breedingcompanies. Currently-grown varieties have not beenassessed for resistance to BChV because C. bursa-pastoris (a non-host species for this virus) has beenused as the source plant to rear the viruliferous aphids.However, these trials have shown that there weredifferences in the reaction of the variety Zulucompared to Roberta when infected, especially withBChV. Future varieties that exhibit virus resistance,ideally to both poleroviruses, would provide analternative to the current reliance on chemical controlmethods. Such varieties could be sown in areasidentified at greatest risk from virus infection asindicated by the virus yellows forecasting scheme(Werker et al., 1998) to provide an integrated diseasecontrol strategy.

Each year British Sugar requires information on thefactors affecting the growth of the UK beet crop inorder to predict the national sugar yield at the end ofthe season. Actual losses attributed to virus yellows

vary from year to year, and are influenced by the levelsand timing of infection, causal virus (i.e. BMYV orBYV) and environmental conditions that influenceplant growth. These trials have shown that thevariation in yield losses will also be dependent on thespecies of polerovirus present in the crop.

Acknowledgements

We thank the Broom�s Barn field experiments teamfor setting up and harvesting the trials, Kathy Beanand colleagues for sugar and impurities analyses andAlan Todd for statistical analysis of the data. Thiswork was sponsored by the British Beet ResearchOrganisation (BBRO). Broom�s Barn ResearchStation, a division of Rothamsted Research, receivesgrant aided support from the BBSRC.

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a Dates when sugar beet plots were inoculated with either BMYV or BChVb Mean effect of both viruses for each set of inoculations between May and Julyc Average effect of each virus for all inoculation dates

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