T. L. Harvey, D. L. Seifers and K. D. Kofoid. Kansas State University Agricultural Research Center, Hays, Kansas USA

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1 Effect of Sorghum Hybrid and Imidacloprid Seed Treatment on Infestations by Corn LeafAphid and Greenbug (Homoptera: Aphididael and the Spread of Sugarcane Mosaic Virus Strain MDMV-Bl T. L. Harvey, D. L. Seifers and K. D. Kofoid Kansas State University Agricultural Research Center, Hays, Kansas USA J. Agdc. EnwmoJ. 13(l): 9-15 (January 1996) ABSTRACT The effects of sorghum hybrids and imidacloprid seed treatment on infestations by corn leaf aphids (CLA), Rhopalosiphum nwidis Fitch, and greenbugs (GB), Schiza,phis graminum (Rhondani), and on the spread of sugarcane mosaic virus strain MDMV-B (SCMV) were evaluated in tests at I-lays, Kansas, in 1993 and In both years, imidaclopl'id controlled CLA for 3 to" but not for 7 wk after planting. Imidacloprid reduced the spread of SCMV in a OS-susceptible hybrid (Northrup King 89750) in 1993 bul not in Differences among hybl;ds in the incidence of SCrvlV did not appear to be related to the hybrids' reaction to GB. However, one GB-resistant hybrid (Dekalb DK-39Y) appeared to be highly resistant to natural infection by SCMV, even though it was susceptible when inoculated mechanically. KEY WORDS Homoptcm, Aphididae, greenbug, corn leaf aphid, sugarcane mosaic virus MDMV-B, imidacloprid, sorghum, vector, resistance Sugarcane mosaic vilus strain IVIDMV-B (SCMV), fonnerly maize dwarf mosaic virus strain B (McKern et ), is recognized as one of a complex of important viral pathogens of sorghum worldwide (Toler et al. 1968). It is vectored by at least 13 aphid species (Toler & Frederiksen 1971), including the corn leaf aphid (ela), Rhopalosiphum maidis Fitch, and the greenbug (GB), Schizaphis graminus (Rondani) (Stoner et al. 1964, Nault & Bradley 1969, Daniels & Toler 1969), which are the most common aphids infesting sorghum in Kansas. Sorghum hybrids have not been classified for resistance to CLA, but over one third of all commercially available sorghum hybrids were resistant to biotype E GB in 1990 (Kofoid et al. 1992). However, the effect of resistance to GB on the control of viral diseases of sorghum is unknown (Harvey et a ). Mechanical inoculation of 152 commercially available sorghum hybrids ""rith SCMV resulted in a wide range of symptom expression from mild to severe, but none of the hybrids was immune (Seifers & Kofoid 1992). I Accepted for publication 18 July

2 10 J. Ag-ric. Entomol. Vol. 13, No.1 (1996) Imidacloprid,1-[(6-chloro-3-pyridinyl) methy1]-4,5-dihydro-n-nitro-1-himidazol-2-amine, when applied as a seed treatment, is effective in reducing the incidence of barley yellow dwarf virus and virus yellows of sugar beets, which are vectored by aphids (Schmeer et al. 1990, Leclercq-Ie Quillec & Dedryver 1992, Knaust & Poehling 1992, Dewar 1992, Bluett & Birch 1992, Heatherington & Meredith 1992, Gourmet et al. 1994). The effect of imidacloprid on the incidence of SCMV in sorghum has not been reported. The objectives of this study were to determine imidacloprid's effectiveness when applied as a seed treatment to reduce the spread of SCMV in sorghum and to determine the effect of GB resistance in selected sorghum hybrids on infection rates of SCMV. Materials and Methods In 1993, two sorghum hybrids, Dekalb 'DK-39Y' (GB resistant) and Northrup King '80750' (OB susceptible), were compared with and without imidicloprid seed treatment for percentages of plants infested with CLA and infected with SCMV. The imidicloprid (Gaucho) seed treatments were applied at a rate of 2.5 g AI/kg (4 oz AIICWT) by Gustafson Inc., Dallas, Texas. The hybrids were selected for their known resistance or susceptibility to GB injury and their comparable susceptibility to SCMV. When mechanically inoculated with SCMV, both hybrids respond with severe necrotic red-leaf reactions and continuous necrosis covering 80%-100% of infected leaves (Seifers & Kofoid 1992). The sorghum hybrids were planted in randomized complete blocks with eight replications on 16 June The plots were single rows 6.1 m long and spaced 0.8 m apart. 'When emergence was complete, plants were thinned to about 32 per row. The soil type was McCook silt loam, and standard practices of fertilization, weed control, and irrigation were followed. To ensure an abundant source of virus 1 on 24 June every other plant in all 32 plots was inoculated mechanically with SCMV using previously described procedures (Seifers 1984). Uninoculated plants expressing symptoms of SCMV were recorded on 27 July and 27 August. The presence of SCMV in tissue of plants bearing symptoms not typical of SCMV was verified by indirect ELISA against antisera to maize dwarf mosaic virus, SCMV-MDMV-B, and johnsongrass mosaic virus. Leaf tissue was ground in 0.05 M carbonate buffer 1 ph 9.6 (Clark & Adams 1977). Samples were absorbed to ELISA plates (Dynatech Laboratories 1 Inc., Chantilly, Virginia) for 1 h at 37 C. Plates were rinsed and then incubated with a 5 Ilg/m1 dilution of antivirus antibody in blocking buffer (Clark & Adams 1977) for 1 h at 37 C. Plates were rinsed and blocked with a solution containing 5% (w/v) nonfat dry milk and 0.01% (v/v) antifoam A made in phosphate buffered saline, ph for 1 h at 37 C. FoIlO\ving rinsing, antirabbit antibody:alkaline phosphatase conjugate in blocking buffer (Sigma Chemical Co., St. Louis, Missoul"i) was added 0:1000, v/v dilution) and the mixture was incubated for 1 h at 37 C. Following rinsing, substrate (p-nitrophenyl phosphate) in substrate buffer (Clark & Adams

HARVEY et al.: Effects or Imidacloprid and Sorghum Hybrid on MDMV 11 1977) was added at 0.714 mg/ml, and the mixture was incubated for 30 min at 25 C to 28 C.

3 HARVEY et al.: Effects or Imidacloprid and Sorghum Hybrid on MDMV ) was added at mg/ml, and the mixture was incubated for 30 min at 25 C to 28 C. Absorbance (405 nm) values were considered positive if they were twice those of the healthy control. Uninoculated plants that were infested naturally with CLA were recorded by visual examination of the whorls of each plant on 8 July and 4 August. Plants were inspected at weekly intervals for the presence of other insects, especially GB, during June, July, and August. In 1994, the test was expanded to include six GB-resistant and six GBsusceptible hybrids, which were planted on 10 June. All hybrids were compared with and without imidacloprid seed treatment, which was applied at the same rate as in the 1993 test. All hybrids were susceptible to 8CMV when inoculated mechanically, as previously described. The location of the test and the experimental design were the same as for 1993, except that 24 treatments were used in three completely randomized blocks in Every other plant in each plot was inoculated mechanically with SCMV as previously described on 21 June when the plants were in the 2- to 3-leaf stage. Uninoculated plants that expressed symptoms of SCl\:IV were recorded on 19 July and 16 August. The presence of 8CMV in the tissues of some symptom-bearing plants was determined by EL1SA as previously described. Plants infested with CLA were recorded on 11 July and 1 August by inspection of the whorls of all uninoculated plants. The number of GB per plant was estimated by visual examination of five plants that were randomly selected from each of the 72 plots on 1 August and 8 August. Percentages of plants infested with CLA and infected with 8CMV and numbers of GB per plant were analyzed with ANOVA, and mean differences among treatments were compared with the '"Valier-Duncan multiple range test (SAS Institute 1985). Results and Discussion In both 1993 and 1994, imidacioprid seed treatment controlled CLA for 3 to 4 wk after planting but not fol" 7 wk (Table 1). Differences between the two hybrids in CLA infestation were not statistically significant. The sorghum hybrid DK 39Y had a lower percentage of plants infected with scrvrv than in both 1993 and The rate of spread of SCMV in m(-39y was so low (none in 1994) that the possible effect of imidacloprid on the incidence of 8CMV in this hybrid could not be measured. Imidacloprid-treated had a significantly lower rate of spread of BCNlV infection than untreated S9750 in 1993 but not in 1994 (Table 1). A possible explanation for this difference is that the CLA inrestations were much higher in 1994 than in The larger numbers of CLA in 1994 may have overwhelmed the early effect of imidacloprid control of CLA on transmission of SCM\'. Only traces of GB were observed in the test during 1993, and GB are known to be inefficient vectors of SCMV (Seifers & Harvey 1989), so it is questionable as to whether the OB resistance of DK-39Y could account for its resistance to the spread of SCMV infection. However, to test this possibility, six hybrids with GB resistance were compared with six susceptible hybrids in 1994 (Table 2).

4 Table 1. Effect of imidacloprid seed treatment and sorghum hybrid on infestation of corn leaf aphid (CLA) and spread of sugar cane mosaic virus strian MDMV-B (SCMV) at Hays, Kansas, in 1993 and % Plants Infested CLAe % Plants Infested SCMVc Hybrid G, Treatment b 1993 d 8 July 4 Aug d 11 July 1 Aug. 1993d 27 July 27 Aug, 1994d 19 July 16 Aug. DeKaJb DK39Y DK39Y T U 12.0 b 6.6 a 11.0 a 80.7 b a 2.4 a 3.4 a 4.0 a orthrup-king T U 7.9 b 10.6 a 14.1 a 76.4 b b 14.5 b 37.2.c 9.9 a 6.3 a 23.9 b 25.2 b a OK 39Y resistant and susceptible to E biotype grcenbug, Schizaphi.~ graminum (Rondnni), planted 16 June 1993 and 10 June b T = Seed treated with imidac10prid (Gaucho) 2 5 g AIlkg (4 OZ AlIC\VT). U = Untreated seed. c Means within each column fouowed by the arne letter are not signilicanlly djlterent at the 0.05 level of probability. WaJler-Duncan multiple range test (SAS Institute 1985). d Dates =3 4 wk and 7 wk after planting.

5 HAnVEY cl a\.: Eflects of Imidacloprid and Sorghum Hybrid on MDMV 13 Table 2. Effect of imidacloprid seed treatment and sorghum hybrid on infestation of greenbug and incidence of plants infected with sugar cane mosaic virus strain MDMV-B (SCMV). Hays, Kansas No. Greenbugsb per Plant % Plnnts b Infected SCMV Hybrid and Trcatmcnl U 1 AugY 8 Aug. c 19 JulY" 16 Aug" Resistant Treated Oro Ultra a 25.2 a DeKalb DK 39Y 15.0 a 8.3 a 0.0 e Oeltapine a 28.3 a 9.4 abe 26.5 a Casterline SR 31' a 13.3 a 2.0 ed 3.8 de Northrup King KS 7] a 48.3 a 8.4 abc 2\.9 ab Golden Acres T-E a 3.8 bed 15.9 abed Mean 15.5 a 27.5 a 6.1 a 15.5 a Susceptible-Treated Golden Acres Dinero 3\.7a 37.3 a 0.0 d 17.8 abed IC a 97.0 a 6.0 abed 16.5 abed Triumph Two a a 6.1 abed 19.1 abe Asgrow Topaz 26.3 a a 9.2 abc 18.7 abed Northrup King a 82.0 a 9.9 ab 24.0 ab Delange DBA a a 1.7 ed 15.0 abede Mean 48.1 b 88.1 b 5.5 a 18.5 a Resistant-Untreated Oro Ultra 23.3 " 18.3 a 4.7 bed 25.0 ab DeKalb DK 39Y 14.0 a 56.7 a 0.0 d 0.0 e Del tapi ne a 32.3 a 4.2 bed 10.0 bede Casterline SR 3 VI EC 49.3 " 26.3 a 0.0 d 4.5 cdc Northrup King KS a 26.7 a 4.9 bed 2\.7 ab Golden Acres T-E 77E 66.7 a 7\.3 a 3.9 bed 11.7 abede Mean 34.8ab 38.6 a 3.0 a 12.2 a Susceptible Uotreated Golden Acres Oi nero 2\.6 a bed 14.8 abede IC \.7 a 92.0a 13.2 a 26.4 a Triump Two a 7.4 abed 13.3 abcde Asgrow Topaz 41.7 a 48.0 a 6.1 abed 26.5 a Northrup King a 6.3 abed 25.2 a Delange D5A a 86.7 a 3.9 bed 2\.3 ab Mean 44.3b b 6.6 a 21.3 a 11 Resistant - Hybrids resistant to biotype E greenbug. Treated:: Seed of hybrids treated with imidncloprid <Gaucho). All hybrids planted 10 June. b fl.'ieans between individual h}'brids or groups of hybrids within u column followed by the same letter are not significantly different at the 0.05 Ic"cl of probability. Waller-Duncan multiple range test (SAS Institute 1985). t Dates = 3-4 wk and 7 wk after planting.

6 14 J. AbJ'yic. Entomol. Vol. 13, No. 1(1996) The GB populations were higher in 1994 than in 1993, but the numbers were still so low and variable that it was not possible to detect significant differences among individual hybrids. When the hybrids were grouped into resistant and susceptible or treated and untreated classes, group differences in GB numbers were generally significant between J'esistant and susceptible hybrids but not between treated and untreated hybrids (Table 2). Imidacloprid did not seem to have an effect on the small numbers of GB present 7 wk after planting. Resistant hybrids as a group had fewer GB than susceptible hybrids. Several significant differences occurred among hybrids in percentages of plants naturally infected with SCMV on both 19 July and 16 August. These differences did not appear to be related to GB resistance because the resistant and susceptible classes did not differ significantly in degree of SClvIV infection (Table 2). All of the plants evaluated by ELISA tested positive for SCMV only. None of the DK-39Y plants was infected with SCMV in 1994, and no more than 4% was infected in 1993, indicating that DK-39Y is highly resistant to infection by vectors, even though it is susceptible when mechanically inoculated. Nault et al. (1971) also found that inbred lines of corn varied in susceptibility according to whether they were inoculated mechanically or by aphids. Some of the other sorghum hybrids did not differ significantly from DK-39Y in percentage of plants infected with SCMV, and 'Castedine SR 314' appeared to be the second most resistant of the 12 hybrids tested. Our results indicate that field tests involving mechanical inoculation of sorghum hybrids to evaluate their resistance to SCMV may not accurately predict their vulnerability to field infections. Further work is needed to determine why DK-39Y, and probably other hybrids, are resistant to vectorinduced SCMV infections but not to mechanical inoculation. Acknowledgment Partial funding was provided by the Kansas Sorghum Commission. Contribution No J from the Kansas Agricultural Expel'iment Station. Mention of a proprietary product does not constit.ute a recommendation or endorsement by Kansas State University. References Cited Bluett, D. J. & P. A. Birch Barley yellow dwarf virus (BYDV) control with imidacloprid seed treatment in the U. K. Pllanzenschutz-Nachrichten Bayer 45: Clark, M. F. & A. N. Adams Characteristics of the microplate method of enzyme linked immunosorbent assay for the detection of plant vil'uses. J. Gen. Viral. 34: Daniels, N. E. & R. W. Toler' Transmission of maize dwarf mosaic by the greenbug, Schi.zaphis grnminuf/l.. Plant Dis. Reptr. 53: Dewar, A. M The effects of imidacloprid on nphids and virus yellows in sugar beet. Pllanzenschutz-Nachrichtcn Bayer 53:

$HARVEY et al.: Effects of 1midacloprid and Sorghum Hybrid on MD;\'fV 15 Gourmet, C. A., A. D. Bewings, ]1'. L. Kolb & C. A. Smith. 1994.$

7 HARVEY et al.: Effects of 1midacloprid and Sorghum Hybrid on MD;\'fV 15 Gourmet, C. A., A. D. Bewings, ]1'. L. Kolb & C. A. Smith Effect of imidacloprid on non night movemenl of Rhopalosiphum padi and the subsequent!:lpread of barley yellow dwarfvil us. Plant Dis. 78: Harvey, T. L., T. J. Martin & D. L. Seifers Importance of plant resistance to insect. and mite vectors in controlling \~irus discases of plants: Resistance to the wheat curl mite (Acaria: Eriophyidae). J. Agric. Entomol. 11: Heatherington, P. J. & R. H. Meredith United Kingdom ficld trials with Gaucho for pest and virus control in sugar beets, pnanzenschutz Nachrichten Bayer 45: Knnust, H. J. & H. M. Poehling Effect of imidacloprid on cereal aphids and their efficiency as vectors of BVD virus. Pflanl,cnschutz-Nachrichten Bayer 45: Kofoid, K. D., T. L. Harvey & P. E. Sloderbcck A new gl'cenbug, biotype t, damaging sorghum spp. Botto. lit Proceedings, 46th Annual Corn and Sorghum Hesearch Conference, American Seed Trade Association, Washington, D. C. Leclercq le QuiUec F. & C. A. Dedryver Spread of yellow dwarf virus in winter barley as a function of thc dc\'c1opment of vector aphid populations. Action of an aphicidc applied as a seed treatment. pnanl,cnschutz-nachl'ichtcn Bayer 45: McKern, N. M., D. D. Shukla, R. W. Toler, S. G. Jensen, M. Tosic, R. E. Ford, O. Leon & C. W. Ward Confirmation that the sugarcane mosaic virus subgroup consists of four distinct potyvil-uses by using peptide profiles of coat proteins. Phytopathology 81: Nault, L. R. & R. H. E. Bradley Acquisition of maize dwnrf mosaic virus by the greenbug, Sc.hizaphis graminum. Ann. Entomol. Soc. Am. 62: Nault, L. R., H. J. Harlan & W. R. Findley. 197J. Comparative susccptibility of corn to aphid and mechanical inoculation of maize dwarf mosaic virus. J. Econ. Eotomol. 64: SAS Institute, Inc SAS/STAT guide fol' personal computers, vcrsion 6 cd_ SAS Institute, Cary, North Carolina, 378 pp. Schmecr, H. E., D. J. Bluett, R. Meredith & P. J. Heatherington Field evaluation of imidncloprid as an insecticidal seed treatment in sugar beet and cereals with particular reference to virus vector- contl"ol pp In Proceedings Brighton CI'OP Protection Conference, Pests and Diseases, Brighton, England. Seifers, D. L. & T. L. Harvey Effect of carbofuran on trnnsmission of maize dwarf mosaic virus in sorghum mechanically inoculated and by the aphid, SchizaphisgramillulU. Plant Dis. 73: Seifers, D. L Optimum conditions for st.udies of maize dwarf mosaic virus strains A and B in sorghum. Plant Dis. 68: L Seifers, D. L. & K. D. Kofoid Symptom response of sorghum hybrids infected by sugarcane mosaic virus strain MDl\!IV B. Kansas Agr. Exp. Stn_ Keeping 'p With Research 10:1,5 pp. Stonc.., W. N., L. E. Williams & L. J. AlexandcJ Transmission by the corn leaf aphid, RhopalosipJwm mniclis (Fitch) of a virus infecting corn in Ohio. Ohio Agri. Exp. Sta. Res. eirc., pp. Toler, R.W., A. J. Blockholt. & R. H. Leis)'_ Effect of maize dwarf mosaic on grain sorghum performance. Phytopathology 58: 731. Toler, R. W. and R. A. FI edel"iksen Sorghum diseases. Tex. Agric. Exp. Stu. PH pp.

Synergism in Cereals Between Corn Leaf Aphid-Specific and Aphid-Nonspecific Isolates of Barley Yellow Dwarf Virus C. C. Gill and A.

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