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Papers in Pathology Department

2002

Bean pod mottle virus: A Threat to U.S. Production

Loren J. Giesler University of Nebraska-Lincoln, [email protected]

Said A. Ghabrial University of Kentucky

Thomas E. Hunt University of Nebraska-Lincoln, [email protected]

John H. Hill Iowa State University

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Giesler, Loren J.; Ghabrial, Said A.; Hunt, Thomas E.; and Hill, John H., "Bean pod mottle virus: A Threat to U.S. Soybean Production" (2002). Papers in Plant Pathology. 186. https://digitalcommons.unl.edu/plantpathpapers/186

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Loren J. Giesler A Threat University of Nebraska, Lincoln Bean pod Said A. Ghabrial to U.S. University of Kentucky, Lexington mottle Thomas E. Hunt Soybean University of Nebraska, Lincoln virus John H. Hill Production Iowa State University, Ames

Bean pod mottle virus (BPMV) is wide- ies each of a large (L) and small (S) coat reported (13,49). BPMV RNA-1 encodes spread in the major soybean-growing areas protein (CP) of 41 kDa and 22 kDa, re- five mature proteins required for replica- in the southern and southeastern United spectively. The S-CP occurs in two major tion (from 5‡ to 3‡: a protease cofactor States. A severe outbreak of BPMV in the size classes, the intact protein and a C- [32K], a putative helicase [58K], a viral north central and northern Great Plains terminus truncated version. As a conse- genome-linked protein [VPg], a protease states is currently causing serious concern quence of this heterogeneity, BPMV viri- [24K], and a putative RNA-dependent to soybean growers and to the soybean ons have two electrophoretic forms, a RNA polymerase, RdRp [87K]), whereas industry in this region (30). BPMV is effi- slow- and a fast-migrating form, each con- RNA-2 encodes a putative cell-to-cell ciently transmitted in nature, within and taining both M and B nucleoprotein com- movement protein and the two coat pro- between soybean fields, by several species ponents. Intact S-CP converts to the C- teins (13,49). of leaf-feeding beetles. The deleterious terminus-truncated form with ageing of the effects of BPMV infection not only reduce virions and involves a specific, yet little Historical Perspective yield but also reduce seed quality, as seeds understood, proteolytic processing at the Zaumeyer and Thomas first described from infected may be discolored. C-terminus (47). BPMV in 1948 on Phaseolus vulgaris L. Furthermore, BPMV predisposes BPMV genomic RNAs are polyade- var. Tendergreen. In 1948, the virus was to Phomopsis spp. seed infection (85), a nylated, and each has a small basic protein, noted to be readily transmitted mechani- major cause of poor seed quality in soy- VPg, covalently linked to its 5‡ terminus. cally, and the experimental host range in- bean (78). The recent BPMV outbreak is The BPMV genome is expressed via the cluded several varieties of all groups of linked to the warm winters of the past few synthesis and subsequent cleavage of large snap and dry beans. In further exploration years that have allowed the beetle vectors polyprotein precursors (47). The complete of the BPMV experimental host range, 25 to overwinter and emerge in the spring in nucleotide sequences of the two genomic species including 20 genera of plants were unprecedented numbers (Fig. 1). RNAs of BPMV strain KY-G7 have been evaluated for susceptibility. In this test, Virion Properties and Genome Organization BPMV is a member of the genus Como-  virus in the family Comoviridae (93). Like other , BPMV has a bipartite positive-strand RNA genome consisting of  RNA-1 and RNA-2, which are separately encapsidated in isometric particles 28 nm in diameter (Fig. 2). Virions can be sepa-  rated by density gradient centrifugation into three components designated top (T), middle (M), and bottom (B). The T compo-  nent contains empty particles, whereas the

M and B components contain single mole- %/%VZHHSV cules of RNA-2 (approximately 3.6 kb) or  RNA-1 (approximately 6.0 kb), respec- tively. The three components have identical protein composition, consisting of 60 cop- 

Corresponding author: L. J. Giesler, University of              Nebraska, Department of Plant Pathology, Lin-

1280 Plant Disease / Vol. 86 No. 12 some varieties of lima bean (Phaseolus incidence (73). In the mideastern region of performed in North Carolina showed that lunatus L.) and soybean (Glycine max L.) North Carolina, 37% of the fields had more infection of the plants needs to occur be- were determined to also be susceptible than 50% of the plants infected in 1983. fore the V6 growth stage to significantly (98). BPMV was first identified as a soy- More recently, BPMV incidence has in- affect yield (71). bean problem in the field in 1951 in Arkan- creased significantly in the north central Seed coat mottling. Soybeans infected sas (87). In 1958, the experimental host region. For example, 70% of 197 fields with BPMV may produce seed with mot- range list was expanded to include Lespe- sampled in Nebraska had BPMV in 2000 tled seed coats. The mottling originates at deza sp., Stizolobium deeringianum Bort., (101). In a recent survey, 73 of 80 counties the hilum and is also referred to as “bleed- and Trifolium incarnatum L. (82). in Iowa had BPMV (67). ing hilum” since hilum color appears to Between the 1960s and the 1980s, most bleed from its normal zone. The coloration BPMV research involved soybean response Impact of BPMV Infection of the hilum is the color of the mottling on and studies on inoculation timing relative on Soybean the seed (Fig. 4F). Quiniones et al. (65) to plant development and its impact on Foliage and pod symptoms. Soybean analyzed seed mottling levels as affected yield (34,55,65,70,79,96). Studies which response to BPMV infection varies. Plant by potential synergistic reactions between established the (BLB) symptoms range from a mild chlorotic SMV and BPMV. SMV-infected plants had (Cerotoma trifurcata Forster) (Fig. 3) as mottling of foliage to a severe mosaic, with 92% of the seed lot mottled, and the SMV the primary vector of BPMV were per- the most obvious symptoms appearing on and BPMV combination had 96% of the formed in the 1960s and established the younger leaves (Fig. 4A, C, D) (69,89). seed lot mottled. Soybean varieties differ BLB as the most important vector in south- Depending on the soybean variety, BPMV in the degree of seed mottling in response ern states (60,68,88). Until recently, may cause terminal necrosis and death to BPMV infection (33,100). Mottling of BPMV research was confined to the south- (79). BPMV delays maturity of soybean the seed coat is not a reliable predictor of ern United States, including the Carolinas, stems, causing “green stem” (Fig. 4B) seed coat infection by BPMV. Kentucky, Mississippi, and Arkansas. With (79). The pod mottling symptom that is BPMV has both primary and secondary the recent movement of this virus into the prominent in snap beans is not prominent effects on seed quality. The delay of matur- north central region of the United States, in many soybean cultivars due to pubes- ity of the soybean plant and/or the stress of new interest in the pathology of BPMV has cence, but appears in some (Fig. 4E). the systemic virus infection has been arisen. Yield reduction. BPMV infection can shown to have secondary effects on the reduce soybean yield. According to the plant. Phomopsis seed infection tends to be Distribution of BPMV Compendium of Soybean Diseases, yield higher in BPMV-infected soybean plants After the initial discovery of BPMV in loss ranges between 3 and 52% (24). Over (1,85). SMV infection also increases Pho- soybeans in Arkansas (87), other states a broad geographic range, yield reductions mopsis seed infection (40). Seed infection confirmed its presence. BPMV was con- between 10 and 40% have been reported by Phomopsis occurs during the R7 and R8 firmed in North Carolina and Virginia (82), (10,36,55,69,85). Impact of BPMV on growth stages, when pod and seed moisture Kentucky (27), Mississippi (62), and Lou- yield depends upon the time of virus infec- decline. BPMV infection has been shown isiana (35). In the north central region, tion relative to plant development (Fig. 5), to extend dry down periods, resulting in BPMV has been confirmed in Iowa (64), with early infection giving the highest increased levels of Phomopsis seed infec- Illinois (51), Indiana (K. Perry, personal yield reduction (25). Ross (69) showed that tion (1). communication), Kansas (29), Nebraska mixed infection with BPMV and Soybean (45), Ohio (17), South Dakota (43), and mosaic virus (SMV) reduced yield up to BPMV Diversity Wisconsin (44) and has also been reported 85%. In Louisiana, it was determined that and Synergism with SMV in Canada (50). BPMV is likely present in the BPMV infection level needs to be be- The recent BPMV outbreak has all soybean-producing states, but documen- tween 20 and 40% of the plant population prompted researchers in the major U.S. tation is incomplete. to cause economic loss (36). Research soybean production regions to undertake a BPMV is the most common viral patho- gen of soybean in several states. In Ken- tucky, BPMV was found in 66% of 382 fields in 1985 to 1987; incidence varied from low to high within fields (26). Viral incidence was highest in the last year (1987) of the Kentucky survey. In North Carolina, 56 fields were surveyed for viral

Fig. 2. Negatively stained purified Bean pod mottle virus virions (28 nm diame- Fig. 3. Bean leaf beetle. A, Common type. B, Red variant. The black triangle behind ter). Bar equals 50 nm. the thorax is used to distinguish the bean leaf beetle.

Plant Disease / December 2002 1281 concerted effort to screen available soy- from doubly infected plants reveals single allows the nonpotyvirus member of the bean germ plasm for resistance/tolerance to plant cells containing both SMV and pair to accumulate beyond its normal level. BPMV. Until recently, there was no evi- BPMV (3). The HC-Pro thus suppresses gene silencing dence that BPMV existed as multiple Although the mechanism of synergism (2). There appears to be specificity in the strains. Such evidence of genetic diversity between SMV and BPMV is not under- interaction between BPMV and SMV since is very useful as breeders and others work stood, recent studies with synergistic inter- no synergism was detected in BPMV inter- to develop germ plasm and cultivars that actions between other pairs of unrelated actions with some other potyviruses, e.g., offer broad protection against the full range viruses (in which one of the pair is a neither Bean yellow mosaic virus nor Pea- of BPMV strains as they become known. potyvirus) suggest that expression of the nut mottle virus (3). As the mechanism by The recent work of Gu et al. (30) has re- potyvirus HC-Pro (helper component–pro- which HC-Pro suppresses silencing is not vealed at least two genetically distinct tease) gene might interfere with a general known, the answers for why the HC-Pro BPMV subgroups, I and II. The two sub- antiviral system in plants. Posttranscrip- from SMV, but not from other potyviruses, groups can be clearly distinguished by tional gene silencing is a candidate for suppresses gene silencing cannot be ad- nucleic acid hybridization analysis (Fig. 6). such a host defense system. This in turn dressed as this time. Furthermore, Gu et al. (30) isolated and characterized naturally occurring reassor- tants between the two subgroups. It is of interest that isolation of BPMV reassor- tants coincided with the recent increase of both virus incidence and BLB populations. Under such conditions, one predicts an increased incidence of mixed infections and the emergence of reassortants and sequence variants, the latter possibly origi- nating by RNA recombination events. BPMV interacts synergistically with the potyvirus SMV, causing drastic reductions in yield and seed quality (3,10,69,85). It is thus prudent to use SMV-resistant cultivars in regions where BPMV is endemic (Table 1). The concentration of BPMV in soybean plants doubly infected with BPMV and SMV is significantly higher (two- to seven-fold, depending on leaf position, i.e., age of infection) than in singly infected plants. SMV titer, however, is not affected by double infection. Enhancement by SMV of BPMV titer in doubly infected plants can be demonstrated in both greenhouse and field-grown plants and is independent of the timing, sequence, or means of inocu- Fig. 5. Impact of Bean pod mottle virus (BPMV) on yield of soybean cultivars Bragg lation with the two viruses (3,10). Electron and Lee 74, as affected by time of inoculation relative to soybean development. Modi- microscopic examination of thin sections fied from Hopkins and Mueller (34).

Fig. 4. Symptoms exhibited by soybean plants infected with Bean pod mottle virus. A, Plant showing symptoms in younger leaves. B, Green stem symptom in mature field. C and D, Leaves exhibiting rugosity and mottled appearance. E, Pod mottling on cv. Essex. F, Seed coat mottling or bleeding hilum symptom.

1282 Plant Disease / Vol. 86 No. 12 Insect Vectors of BPMV tected in overwintered adults, although of commercial cultivars with BPMV resis- Several leaf-feeding beetles (Coleoptera) virus transmission by these adults may be tance. Perennial weeds, seedlings emerging in the families Chrysomelidae, Coccinelli- relatively infrequent. It is probable the from infected seeds, and overwintering dae, and Meloidae can transmit BPMV. virus does not replicate in the beetle since BLB are potential sources of BPMV early These include Cerotoma trifurcata (För- virus level decreases gradually during test in the growing season (45,53,90,91). Some ster) (bean leaf beetle), Colaspis brunnea feeding on healthy plants (28). Larvae of of these reports, however, are preliminary. (Fabricius) (grape colaspis), Colaspis lata several chrysomelid beetles transmit bee- Roles of overwintering beetles, seed trans- Schaeffer, Diabrotica balteata LeConte tle-vectored viruses (23), but it is unknown mission, and weed reservoirs (alternate (banded cucumber beetle), D. undecim- if the larval stages of the BLB can transmit hosts) in BPMV epidemiology have yet to punctata howardi Barber (spotted cucum- BPMV. Similarly, potential for transovarial be critically assessed. The potential for ber beetle), Epicauta vittata (Fabricius) transmission of BPMV is unknown. Other disease control through management of the (striped blister beetle), and Epilachna beetle-transmitted viruses are not known to principal virus vector, the BLB, will be varivestis Mulsant (Mexican bean beetle) be transmitted transovarially. HQKDQFHGE\DFFXUDWHLGHQWLILFDWLRQRIWKH (24). More recently, Diabrotica virgifera The spread of BPMV on a local (within YLUXVVRXUFH V  virgifera LeConte (western corn rootworm) and between fields) and a regional basis Alternate hosts. The agriculturally sig- and Odontota horni Smith (soybean leaf- likely reflects BLB dispersal. Three peri- nificant hosts of BPMV include soybeans miner) have been identified as potential ods of flight activity were identified in and some Phaseolus spp. and cowpea culti- vectors (94). However, in the north central North Carolina, a region with two BLB vars (24). In the north central United states, the BLB is by virtue of its preva- generations: a field colonization flight States, these are not believed to act as lence the primary BPMV vector (34,60). followed by trivial and overwintering sources of early inoculum foci from which Adult BLB overwinter in various habi- flights by the first (F1) and second (F2) potentially viruliferous BLB move to tats, preferring leaf litter in wooded areas generations (6). The colonizing population emerging soybeans. Alternatively, other in Iowa (41). Temperatures below the criti- exhibited the greatest flight activity, fol- leguminous hosts may provide a means for cal range of –5 and –10°C cause significant lowed by the fall migration to overwinter- the virus to overwinter and could serve as mortality; however, daily leaf litter tem- ing habitat. Most trivial flights were ob- virus reservoirs. In Iowa, Desmodium spp. peratures in woodlands seldom go below served to be ˆ30 m. has recently been demonstrated to be natu- –5°C (42). Ambient air temperatures corre- rally infected with BPMV (R. K. Krell and late well with leaf litter temperature above Inoculum Source J. H. Hill, unpublished). Although this is –10°C. Below –10°C, there is a low corre- for Disease Development the first report in the north central states, lation, and daily leaf litter temperature Virus diseases cause the most damage Pitre (60) suggested that in Mississippi seldom drops below –2°C. The buffered when infection occurs in early stages of beetles may become viruliferous after feed- microhabitat facilitates beetle survival. It is soybean growth (Fig. 5). Therefore, elimi- ing on Desmodium paniculatum (L.) DC. likely that the BLB behaves similarly nation of primary sources of BPMV inocu- Further exploration of potential virus reser- throughout the north central states, as other lum will facilitate disease management. voirs is necessary in the north central soy- work suggests that the beetle overwinters This is particularly so in view of the lack bean growing areas. To be a significant in trash and grass (38), under rocks (20), and in leaf litter (7,54). In the Midwest, BLB emerge from over- wintering sites in mid to late April (83) and 6XEJURXS, 6XEJURXS,, 6\PSWRP move to early legumes, such as Desmo- 51$ 51$ 51$ 51$  dium sp. (11) and alfalfa, Medicago sativa  0RGHUDWH L. (83,86). Beetles begin to colonize soy- beans as seedlings emerge. Viruliferous  0LOG beetles can potentially transmit BPMV to  6HYHUH soybeans at early growth stages, which  6HYHUH maximizes reduction in yield and seed quality (70). Phenological studies show the  Fig. 6. Bean pod mottle virus diversity based on identification of two genetically dis- BLB develops one generation per year in tinct strain subgroups (I and II) and the occurrence of reassortants. Modified from Gu much of Minnesota (48), two generations et al. (30). Symbols in table identify which RNA is present, with yellow and green rep- per year in Iowa (83), Illinois (39), and resenting subgroup I and II strains, respectively. Nebraska (97), and three generations per year in Arkansas and South Carolina (20,38). The BLB is an extremely efficient virus Table 1. Effect of combinations of (SMV) and Bean pod mottle virus vector. The beetle may acquire the virus (BPMV) on soybean yield (modified from Calvert and Ghabrial [10]) after a single bite, and transmission effi- Yield (g/hill) for soybean cultivars ciency increases with time on the virus x y source plant as well as on the healthy soy- Virus treatment Williams Essex York bean plant (61). Transmission efficiency is Control 228.2 az 236.8 a 251.4 a found to be very high in F1 and F2 beetle SMV 183.8 b 145.1 b 249.0 a populations with 70 to 80% of the beetles BPMV 147.6 c 98.6 c 134.7 b that are allowed 72 h acquisition feeding SMV-BPMV 56.1 d 57.6 d 168.4 b on source plants being able to transmit the BPMV-SMV 70.8 d 57.2 d 151.2 b virus (S. A. Ghabrial, unpublished data). x The primary leaves of all test plants, except controls, were inoculated with SMV or BPMV 20 There is no latent period in the vector (23). days after planting; in the case of double inoculation treatments, the second virus was applied The virus is not detected in the hemocoel, to the first trifoliolate leaves 1 week later. y The soybean cv. York is resistant to SMV strain G-2, used for inoculation. and transmission is therefore not circula- z Values are means for nine replications. For each cultivar, means followed by the same letter tive. The virus is presumably restricted to are not significantly different (a = 0.05) according to Duncan’s multiple range test. Hill size the digestive tract (92). Retention time is was a 45-cm row containing 20 seeds planted. considerable since the virus can be de-

Plant Disease / December 2002 1283 virus reservoir in the north central states, a be demonstrated and that the relationship vived overwintering, or 50%); however, species must serve both as an overwinter- appears to be cultivar dependent in seed none of the virus-containing beetles trans- ing host for the virus and as a source for lots that were tested and found not to have mitted BPMV to healthy plants (0/40). beetle feeding. SMV (J. H. Hill, unpublished). Further Likewise, the viruliferous beetles collected Seed transmission. Grower concerns testing of single seeds from two soybean from alfalfa fields (2 positive out of 107 often center on the risk of planting mottled cultivars for presence of virus antigen has beetles collected) failed to transmit BPMV seed and concern that mottled seed will shown that in one cultivar, 31 of 35 non- to healthy plants. These overwintered bee- introduce virus. In analysis of this issue, it mottled seeds contained BPMV while 47 tles, however, regained ability to transmit is important to distinguish between seed- of 65 mottled seeds tested positive. With virus following acquisition feeding on borne and seed-transmitted virus. Fre- the other cultivar, all 13 nonmottled seeds infected plants. However, a recent Iowa quently, seed testing laboratories prepare a tested positive and 79 of 87 mottled seeds study indicates that a low percentage of seed extract by grinding a group of seeds were positive (J. H. Hill, unpublished). It is BLB could transmit BPMV after emer- and detect virus by enzyme-linked immu- conceivable that cultivars that exhibit a gence. In this study, leaf litter was col- nosorbent assay (ELISA). This detects negative linear relationship between per- lected from areas of high BPMV incidence seedborne virus; detection of seed-trans- cent mottling and relative virus antigen in late fall and placed in outdoor cages. In mitted virus is equivocal. Determination of content produce a relatively high number spring, emerged beetles were collected seed-transmission requires grow-out tests of seeds that contain virus antigen but are from litter and placed singly on soybean where soybean seedlings are tested for not mottled. plants grown from seed of virus-indexed virus. It should be noted here that seed Overwintering BPMV in F2 beetle greenhouse plants. Over a 2-year period in transmission generally requires embryo population. Beetles transmit acquired which 182 emerged beetles were tested, infection, not infection of other seed parts. BPMV as they deposit virus-containing approximately 0.5% transmitted BPMV to However, transmission of non-embryo- regurgitant at feeding sites. Several lines of soybean plants (R. K. Krell, unpublished). borne virus is possible as exemplified by evidence suggest that beetle-transmissible These results do not necessarily conflict the transmission of Tobacco mosaic virus viruses escape inhibition by RNase at bee- with those obtained from Kentucky, as (TMV) in tomato and pepper seed (8). tle feeding wounds and that this differenti- differences could result from different TMV is restricted to seed coats, and infec- ates them from viruses that are not trans- beetle biotypes, virus strains, or ambient tion probably occurs through wounds in mitted by beetles. Beetle-transmitted vi- temperatures during overwintering. seedlings contaminated with virus from ruses are transported in xylem more readily seed coats. than non-beetle-transmitted viruses (25). In Management of BPMV Numerous efforts have failed to demon- a preliminary study in Arkansas, Walters et with Vector Management strate seed transmission of BPMV in soy- al. (91) collected beetles during the winter Controlling BLB populations is poten- beans. However, there are now two reports months from trash in or near fields with tially an effective strategy to manage of low level (<0.1%) seed transmission of high BPMV incidence the previous season. BPMV, particularly in the north central BPMV (45,71). In more recent work with Although transmission efficiency was low region where BLB is usually the only sig- field-harvested seed from two private com- (3%), Walters et al. (91) concluded that nificant spring pest. Ross (70) showed that mercial cultivars, no seed transmission was transmission was sufficient to establish insecticide applied throughout the year observed in one cultivar, but 0.037% trans- sources of BPMV inoculum in volunteer reduced BLB populations to insignificant mission was obtained in the other (J. H. soybeans and other available spring hosts. levels, preventing BPMV spread. Because Hill, unpublished). BPMV is stable, easily These authors also interpreted their data to infection after plant stage V6 has little transmitted mechanically, and is present at indicate that BPMV overwinters in hiber- effect on yield (71,96), control of the relatively high levels in seed coats from nating beetles, but they did not rule out that spring colonizing beetles may be sufficient BPMV-infected plants (S. A. Ghabrial, the beetles could have acquired BPMV by to limit yield loss caused by BPMV. unpublished). The very low levels of trans- feeding on the underground parts of dor- Foliar insecticides. BLB is commonly mission could reflect injury of seedlings mant plants. Unfortunately, the Arkansas controlled with foliar insecticides, which contaminated with virus from seed coats, observations made 30 years ago in an ab- can be particularly effective on seedlings as discussed earlier for TMV. The low stract have yet to be confirmed in a pub- when insecticide coverage can be near level of BPMV seed transmission, regard- lished journal article. complete. Because BLB transmit BPMV less of mechanism, may still provide a To study the significance of overwinter- with minimal feeding, early treatment of sufficient source of virus in the presence of ing BLB as a source of primary BPMV the colonizing beetles is likely necessary to high beetle populations to cause significant inoculum in Kentucky (S. A. Ghabrial, limit BPMV spread. Beetle colonization of virus incidence. The potential impact of unpublished), three approaches were used: soybean fields can begin at seedling emer- this low level of seed transmission is un- (i) virus-containing BLB, as determined by gence and continue through several seed- clear because there is presently insufficient ELISA of regurgitant, were collected from ling stages. Consequently, foliar insecti- information available to assess the signifi- soybean fields with high BPMV incidence cides should be applied early in the seed- cance of this relative to various BLB popu- and placed in insect-proof cages for over- ling stages and have residual action. Insec- lations. wintering; (ii) BLB were collected from ticide trials that target the colonizing Mottling of seed coats, similar to that emergence traps that were placed during beetles indicate they are susceptible to a observed with SMV, also occurs in soy- the winter in various locations in Kentucky variety of insecticides (19). Postemergence bean seed harvested from BPMV-infected with high virus incidence in the preceding applied foliar insecticides allow feeding plants. However, presence of seed coat season; and (iii) BLB were collected from and oviposition of beetles prior to insecti- mottling, as with SMV (9), is unreliable alfalfa fields early in the spring (during cide application. for predicting seedborne BPMV. One re- April and May). Regurgitant was collected Recently, the repellant properties of py- port, using a single soybean cultivar, sug- from all beetles and assayed for BPMV by rethroids (15,16,31,74) have become the gests a positive linear relationship between ELISA. Virus-containing beetles were focus of BLB management with insecti- percent mottling and amount of seedborne placed on healthy plants (one beetle per cides. Hammond (32) found that a single SMV (84). Recent work with other soy- plant). The results indicated that ELISA application of lambda-cyhalothrin provided bean cultivars demonstrates that either a readily detected BPMV antigen in regurgi- long-term control of BLB if applied at the positive or negative linear relationship tant from a high percentage of the emerg- beginning of the F2 generation beetle emer- between percent seed coat mottling and ing beetles in both the cages and traps (40 gence. If used early in the seedling stages, relative amount of seedborne BPMV can positive beetles out of 80 beetles that sur- lambda-cyhalothrin should likewise protect

1284 Plant Disease / Vol. 86 No. 12 soybeans from spring colonizing beetles. This is a function of colonization opportu- Disease Management Through An advantage to foliar-applied insecticides nity and beetle fitness (99). Bean leaf bee- Pathogen Derived Resistance is their therapeutic nature and the fact that tles typically emerge from overwintering In the absence of resistance in commer- they can be applied only when necessary. habitat well before soybean emergence, so cial soybean cultivars, researchers have Soil-applied systemic insecticides. An- the first fields to emerge will attract many resorted to transgenic resistance utilizing other option for BLB control is soil-ap- beetles simply because they are available. pathogen derived resistance (PDR). The plied systemic insecticides. Although not In addition, BLB fitness declines if soybean concept of PDR, first proposed in 1985 currently labeled for use for BLB on soy- feeding is delayed, so delaying planting/ (77), has been successfully utilized over bean, several systemic insecticides effec- emergence of soybeans increases precolo- the past 17 years to confer resistance tively reduce early season BLB numbers nization mortality and reduces oviposition, against viruses in many crop plants. PDR when applied in-furrow (carbofuran) (97) resulting in lower BLB populations. involves the expression of viral genes in a or as a band incorporated at planting Higher populations in early-planted soy- host plant and the subsequent disruption of (carbofuran, aldicarb, phorate, and disul- bean appear to relate to higher BPMV essential pathogenic processes of the chal- foton) (18). Advantages to using soil-ap- incidence based on preliminary studies in lenge virus to confer resistance. PDR has plied systemic insecticides are efficacy Nebraska (Fig. 7B). been attained by expressing various forms upon plant emergence and possible larval Trap crops. Early-planted trap crops (56) of functional or dysfunctional viral coat toxicity. The disadvantage of soil-applied are another possible BLB management protein, replicase, protease, and movement systemics is that they are preventative and option. Under this regime, portions of fields protein genes. PDR-mediated protection do not allow the flexibility of not treating are planted early, concentrating BLB phenotypes range from delayed symptom when colonization is minimal. populations. Insecticides are then applied to development, reduced symptoms, and Systemic seed treatment insecticides. the trap crop, effectively controlling beetles virion accumulation to apparent immunity. Seed treatments, like soil-applied sys- with minimal insecticide use. The dis- The variety of PDR phenotypes suggests temics, offer the advantage of BLB control advantage of this system is that machinery multiple mechanisms underlying the at- from plant emergence through seedling must be mobilized twice to plant one field. tained resistance (4,21,22,46,52). The first stages. These compounds are systemic and example of PDR was in transgenic tobacco applied prior to sale. Initial studies with Management of BPMV that accumulated coat protein (CP) of To- seed-applied imidacloprid and thiameth- with Host Plant Genetics bacco mosaic virus; the resistance oxam indicate they effectively control BLB Host plant genetics would be the most achieved was termed CP-mediated resis- on seedling soybean (37). Seed treatments economical approach for the producer to tance (5). Protection against viruses with use very small amounts of active ingredi- manage BPMV. Upon infection, suscepti- ent. However, as with soil-applied sys- ble (virus readily infects and/or replicates temics, the decision to use this technology and/or invades) or resistant (virus infection  is made prior to BLB colonization (often in and/or replication and/or invasion is re-  &RORQL]LQJ the previous year) and does not allow the stricted) plant reactions show a range of $  EHHWOHV flexibility of not treating if BLB coloniza- tolerance or sensitivity in the plant (12).  tion is low. There are currently no commercial BPMV-  (DUO\ Although managing BPMV through vec- resistant soybean cultivars. Resistance to /DWH tor (BLB) management appears promising, BPMV has been identified in the genus  it does pose problems if insecticides, par- Glycine (80) and may permit introduction  ticularly soil-applied systemics and seed of BPMV resistance with interspecific %HHWOHV P URZ  treatments, are used on a regional basis. crosses. In 1985, four soybean germ plasm   Time and again, widespread use of a single lines were released that were resistant to  management tactic to control insects has BPMV (72). Resistance to BPMV was  % selected for resistance in the target pest determined by visual symptomatology.  population. Care must be taken to develop Symptomless lines were assumed to be  an integrated pest management approach to resistant. As soybean lines can be infected   (DUO\ BPMV vector management. Because vari- without showing symptoms, it is possible  ous insecticides, and indeed various cul- that these are not resistant lines. However,  /DWH tural control options, are effective in reduc- based on what is known of other comovi-  ing early season BLB, a rotation of tactics ruses, single gene resistance should exist. %309 LQFLGHQFH   ÃÃ ÃÃ ÃÃ ÃÃ OÃÃ OÃÃ OÃÃ ÃÃ ÃÃ ÃÃ ÃÃ ÃÃ D\ D\ Q Q X X X J J J S S is recommended. This is based on single gene resistance to -X -X - - - $X $X $X 6H 6H 0 0           Planting date. Recent agronomic prac- the closely related , Cowpea           tice in the north central states has moved mosaic virus, in Vigna unguiculata (L.) 6DPSOLQJ GDWH toward early planting of soybeans in many Walp. (63). Also, the virus genetic diver- states. For example, Iowa statistics show sity identified to date (30) suggests the Fig. 7. A, Number of bean leaf beetles that 50% of the acres were planted by 30 potential for corresponding host diversity per 2 m of row for early (4 May) and late May in 1995 and by 5 May in 2000 based on what is known of other pathosys- (26 May) planted soybean near West (75,76). Although planting is delayed by tems. Screening of germ plasm will hope- Point, NE, 1989. Adapted from Witkow- weather conditions during some years, the fully reveal these resistance genes. In the ski and Echtenkamp (97). B, Bean pod mottle virus (BPMV) incidence in early trend toward early planting is associated absence of true resistance, tolerance can be (19 April) and late (25 May) planted soy- with studies showing that, in the absence utilized. Tolerance levels vary in current bean near Fremont, NE, 2001. Foliage of BPMV, best yield usually results when germ plasm (33,100), and several differ- samples were collected at growth soybeans are planted between late April ences in response have been identified stages V2, V5, and R1 (L. J. Giesler, and mid-May. Planting after mid-May among various germ plasm sources unpublished data). Percent incidence often results in decreased yields in Iowa (34,55,64,70,79,96). It is critical that germ calculated by taking the average num- and many parts of the north central region plasm evaluation consider virus strain di- ber of enzyme-linked immunosorbent versity and monitor virus titer by ELISA assay (ELISA)-positive samples per (95). However, studies have shown that strip (11 × 402 m). Ten pooled samples early planting favors increased BLB densi- since symptomology is not a reliable crite- of six trifoliate leaves were collected per ties. Later planting reduces BLB densities rion for resistance (L. J. Giesler, personal strip, with four replications of each and beetle colonization (Fig. 7A) (59,97). observation). planting date.

Plant Disease / December 2002 1285 two coat proteins (such as comoviruses) flected by symptom severity in each maturation and seedborne Phomopsis spp. could be achieved by expressing the capsid variety of soybean. BPMV variants may Plant Dis. 78:33-37. 2. Anandalakshmi, R., Pruss, G. J., Ge, X., polyprotein (pCP) or by expressing both also differ in seed transmission and ability Marathe, R., Mallory, A., Smith, T. H., and individual CP genes (14,57,58). to overwinter in beetles. Also, each diver- Vance, V. B. 1998. A viral suppressor of gene Di et al. (14) reported resistance to sity group may affect soybean production silencing in plants. Proc. Natl. Acad. Sci. BPMV by expressing the pCP in transgenic differently as environmental conditions USA 95:13079-13084. soybean plants. However, the transgene vary. Until these parameters are examined 3. Anjos, J. R., Jarlfors, U., and Ghabrial, S. A. 1992. Soybean mosaic potyvirus enhances utilized in that study was not stable, result- further, it is hard to determine the effect the titer of two comoviruses in dually in- ing in its loss in advanced generations of BPMV will have on soybean production in fected soybean plants. Phytopathology transgenic lines with a subsequent loss of the United States. 82:1022-1027. resistance (S. A. Ghabrial, unpublished One of the first goals is to determine the 4. Baulcombe, D. C. 1996. Mechanisms of data). More recently, stable transformation potential yield reduction in current soybean pathogen-derived resistance to viruses in of soybean with the BPMV pCP gene was cultivars due to BPMV infection. As per transgenic plants. Plant Cell 8:1833-1844. 5. Bendahmane, M., and Beachy, R. N. 1999. achieved via particle bombardment of so- the evaluation of germ plasm and compari- Control of tobamovirus infections via patho- matic embryo cultures. Resistance to son among studies, it is critical that in all gen-derived resistance. Adv. Virus Res. BPMV (reduced symptoms and virion publications the plant stage of inoculation 53:369-386. 6. Boiteau, G., Bradley, J. R., Jr., and Van accumulation) appeared in the T2 progeny is noted and that the rating be done based of transgenic lines in plants inoculated on 100% plants infected compared with Duyn, J. W. 1979. Bean leaf beetle: Flight and dispersal behavior. Ann. Entomol. Soc. mechanically and with viruliferous BLB noninoculated or mock inoculated controls. Am. 72:298-302. (66). The features of pCP transgenic resis- This is best done in a split-plot arrange- 7. Boiteau, G., Bradley, J. R., Jr., and Van tance (concentration of pCP in transgenic ment to account for field variation among Duyn, J. W. 1980. Bean leaf beetle: Tempo- plants is correlated with resistance level) is entries. It is also best to perform this test ral and macro-spatial distribution in North reminiscent of coat protein-mediated resis- under field conditions with adequate mois- Carolina. J. Ga. Entomol. Soc. 15:151-163. 8. Broadbent, L. 1965. The epidemiology of tance (5). Although the pCP transgenic ture as opposed to greenhouse studies, tomato mosaic. XI. Seed transmission of lines provide valuable material that could because seed quality is normally poor un- TMV. Ann. Appl. Biol. 56:177-205. be incorporated into commercial cultivars, der greenhouse conditions. In addition, 9. Bryant, G. R., Hill, J. H., Bailey, T. B., further improvement of resistance level field evaluations require the use of insecti- Tachibana, H., Durand, D. P., and Benner, H. could still be attained via strategies known cides that have residual action as suggested I. 1982. Detection of soybean mosaic virus in seed by solid-phase radioimmunoassay. to confer complete resistance in other co- in this article. It is also critical that the Plant Dis. 66:693-695. movirus–host systems, e.g., expression of BPMV strain be identified based on 10. Calvert, L. A., and Ghabrial, S. A. 1983. movement protein, replicase, or individual current diversity characteristics, as mild Enhancement by soybean mosaic virus of CP genes (58,81). The high level resistance and severe strains and reassortants are bean pod mottle virus titer in doubly infected reported in the latter studies appears to in- known to occur. soybean. Phytopathology 73:992-997. volve posttranscriptional gene silencing Through regional and interdisciplinary 11. Chittenden, F. H. 1897. The bean leaf beetle. U.S. Dep. Agric. Div. Entomol. Bull. 9:64- (PTGS). PTGS results in the degradation research projects, management strategies 71. of RNA viruses, which have an RNA ge- for BPMV will be developed. As this is a 12. Cooper, J. I., and Jones, A. T. 1983. Re- nome with nucleotide sequences similar to problem for pathologists, entomologists, sponses of plants to viruses: Proposals for the transgene used for plant transformation and agronomists, a new regional project the use of terms. Phytopathology 73:127- (4). (NCR-200) has been established to foster 128. 13. Di, R., Hu, C.-C., and Ghabrial, S. A. 1999. linkages among all states and to integrate Complete nucleotide sequence of Bean pod several areas of expertise. The North Cen- mottle virus RNA1: Sequence comparisons Concluding Remarks tral Soybean Research Program (NCSRP) and evolutionary relationships to other co- Fundamental and applied research on the has also initiated a substantial level of moviruses. Virus Genes 18:129-137. epidemiology and host resistance to BPMV funding to support research and extension 14. Di, R., Purcell, V., Collins, G. B., and is urgently needed. Few disease manage- Ghabrial, S. A. 1996. Production of trans- activities that will establish management genic soybean lines expressing the bean pod ment strategies have been developed or guidelines for soybean viruses, including mottle virus coat protein precursor gene. implemented for BPMV control, and no BPMV. These projects and individual state Plant Cell Rep. 15:746-750. resistance to BPMV has been incorporated promotion board funds are collectively 15. Dobrin, G. C., and Hammond, R. B. 1983. into commercial soybean cultivars. Com- stimulating research in this area that will Residual effect of selected insecticides prehensive studies in several locations over result in significant scientific contribu- against the adult Mexican bean beetle (Col- eoptera: Coccinellidae) on soybeans. J. at least three growing seasons are required tions. These contributions will potentially Econ. Entomol. 76:1456-1459. to critically assess roles of seed transmis- lead to increasing the profitability and 16. Dobrin, G. C., and Hammond, R. B. 1985. sion, overwintering beetles, and perennial competitiveness of soybean producers in The antifeeding activity of selected insecti- hosts and/or alternate BPMV hosts as pri- the United States by potentially increasing cides toward the Mexican bean beetle (Col- mary sources of BPMV inoculum. It is yields and seed quality. eoptera: Coccinellidae). J. Kans. Entomol. possible that all three potential sources of Soc. 58:422-427. 17. Dorrance, A. E., Gordon, D. T., Schmitthen- BPMV inoculum play more or less impor- Acknowledgments ner, A. F., and Grau, C. R. 2001. First report tant roles in BPMV epidemiology depend- We thank the North Central Soybean Research of Bean pod mottle virus in soybean in Ohio. ent on location and environment. Seasonal Program for providing support for the soybean Plant Dis. 85:1029. variations that influence the survival and virus project, which has fostered the collaboration 18. Dupree, M. 1970. Control of thrips and the that resulted in this publication. We also thank Drs. bean leaf beetle on lima beans with systemic emergence of overwintering beetles as well Leslie Lane and Robert Wright for critical review as those that affect survival of alternate insecticides. J. Ga. Entomol. Soc. 5:48-52. of this manuscript. This paper has been assigned 19. Echtenkamp, G. W., and Hunt, T. E. 2001. hosts and other putative virus reservoirs the University of Nebraska Agricultural Research Control of bean leaf beetle on soybeans, are expected to influence BPMV inci- Division Journal Series no. 13704, Kentucky 2000. Arthropod Manag. Tests 26:F90. dence. Agricultural Experiment Journal Series Paper no. 20. Eddy, C. O., and Nettles, W. C. 1930. The 02-12-89, and the Iowa Agricultural Experiment bean leaf beetle. S.C. Agric. Exp. Stn. Bull. The impact of strain diversity in BPMV Station Journal Series no. J-19904, Project 2428. is unclear. Each diversity group of BPMV 265. 21. Fagard, M., and Vaucheret, H. 2000. isolates (genetically distinct strains, reas- Literature Cited (Trans)gene silencing in plants: How many sortants, recombinants) may have a differ- 1. Abney, T. S., and Ploper, L. D. 1994. Effects mechanisms? Annu. Rev. Plant Physiol. ent level of stability or virulence, as re- of bean pod mottle virus on soybean seed 51:167-194.

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Loren J. Giesler Dr. Giesler is an assistant professor in the Department of Plant Pathology at the University of Nebraska, Lincoln. He received his B.A. degree in biology from Chadron State College, Chadron, NE, in 1992 and his M.S. and Ph.D. degrees in plant pathology, both from the University of Nebraska in 1994 and 1998, respectively. He joined the faculty at the University of Nebraska in 1999 and has crop responsibilities for soybean and alfalfa across Nebraska as primarily an extension plant pathologist. His research projects focus mostly on soybean pathogens, with the main emphasis on Bean pod mottle virus. Aspects of his research include several approaches to develop a management program for BPMV through vector management including chemical and cultural controls and screening germ plasm for tolerance to the virus. In addition to the agricultural crops, he is also responsible for pathology programming for ornamentals and trees in Nebraska.

Said A. Ghabrial Dr. Ghabrial is a professor in the Department of Plant Pathology at the University of Kentucky, Lexington. He received his B.S. degree in general agriculture from Cairo University in 1959 and his M.S and Ph.D. degrees in plant pathology, both from Louisiana State University in 1963 and 1965, respectively. He was a postdoctoral fellow at the University of California-Davis from 1965 to 1966. After serving as senior virologist at the Department of Agriculture (Egypt) for 4 years (1966 to 1970) and as a postdoctoral research associate at Purdue University for 2 years (1970 to 1972), he joined the faculty at the University of Kentucky in 1972. His main responsibilities include research on epidemiology and molecular biology of legume viruses, with emphasis on Bean pod mottle virus and Peanut stunt virus. His current work is on the molecular basis of a transmissible viral disease of the plant-pathogenic Helminthosporium (Cochliobolus) victoriae. Dr. Ghabrial served as Chairman of the Fungal Virus Subcommittee of the International Committee on of Viruses (ICTV) from 1987 to 1993. He served APS as associate editor and senior editor of Phytopathology (1994 to 1996). He was elected Fellow of APS in 2002.

Thomas E. Hunt Dr. Hunt is an assistant professor and Extension Entomology Specialist at the University of Nebraska NEREC Haskell Agricultural Laboratory, Concord, NE. He received his B.S. degree in agriculture in 1990, an M.S. degree in entomology in 1993, and a Ph.D. degree in entomology in 1999 from the University of Nebraska, Lincoln. He joined the faculty at the Uni- versity of Nebraska in 1999. Dr. Hunt’s research focuses on the management and ecology of insect pests of crops in Nebraska. His research projects fall in the general categories of economic threshold development, resistance management, insect pest biology and behavior, emerging problems, and product efficacy.

John H. Hill Dr. Hill received his B.A. in biology from Carleton College, Northfield, MN, his M.S. in plant pathology from the University of Minnesota, and his Ph.D. in plant pathology from the University of California-Davis. Since 1972, he has been a professor in the Department of Plant Pathology at Iowa State University, where his research focuses on virus diseases of plants. Although he has worked on numerous virus diseases, his most recent work has focused on applied and fundamental aspects of the soybean mosaic and bean pod mottle viruses that infect soybean. Hill is a Fellow of both APS and the American Association for the Advancement of Science. For many years, he provided guidance to the plant virus advisory committee of the American Type Culture Collection and has served on both the Board of Scientific Directors and the Executive Committee of the Board of Trustees. Dr. Hill chairs the USDA-APHIS committee that developed and manages the USDA-APHIS National Plant Virus Data Base.

1288 Plant Disease / Vol. 86 No. 12 (Abstr.) Phytopathology 54:240. van Regenmortel et al., eds. Academic Press, Nebraska soybean. J. Econ. Entomol. 89. Walters, H. J. 1970. Bean pod mottle virus New York. 89:189-196. disease of soybeans. Ark. Farm Res. 19:8. 94. Werner, B. J., Krell, R. K., and Pedigo, L. P. 98. Zaumeyer, W. J., and Thomas, H. R. 1948. 90. Walters, H. J., and Lee, F. N. 1969. Trans- 2002. New host plant and vector relation- Pod mottle, a virus disease of beans. J. Ag- mission of bean pod mottle virus from Des- ships for Bean pod mottle virus. Iowa State ric. Res. 77:81-96. modium paniculatum to soybean by the bean University. North Central Branch of the 99. Zeiss, M. R., and Pedigo, L. P. 1996. Timing leaf beetle. Plant Dis. Rep. 53:411. Entomological Society of America. On-line, and food plant availability: Effect on sur- 91. Walters, H. J., Lee, F. N., and Jackson, K. E. publication D108. vival and oviposition of the bean leaf beetle 1972. Overwintering of bean pod mottle vi- 95. Whigham, K. 2000. Soybean planting date in (Coleoptera: Chrysomelidae) Environ. Ento- rus in bean leaf beetles. (Abstr.) Phy- 2000. Integrated Crop Manag. Newsl. mol. 25:295-302. topathology 62:808. IC484:45. Iowa State University, Ames. 100. Ziems, A. D., Giesler, L. J., Graef, G. L., and 92. Wang, R. Y., Gergerich, R. C., and Kim, K. 96. Windham, M. T., and Ross, J. P. 1985. Lane, L. C. 2001. Effect of bean pod mottle S. 1992. Noncirculative transmission of Transmission of bean pod mottle virus in virus on soybean seed quality. (Abstr.) Phy- plant viruses by leaf-feeding beetles. Phyto- soybeans and effects of irregular distribution topathology 91:S100. pathology 82:946-950. of infected plants on plant yield. Phytopa- 101. Ziems, A. D., Giesler, L. J., and Lane, L. C. 93. Wellink, J., LeGall, O., Sanfacon, H., Ike- thology 75:310-313. 2001. Incidence of Bean pod mottle virus gami, M., and Jones, A. T. 2000. Comoviri- 97. Witkowski, J. F., and Echtenkamp, G. W. and Soybean mosaic virus in Nebraska. dae. Pages 691-701 in: Virus Taxonomy: 1996. Influence of planting date and insecti- North Central Division of the American Seventh Report of the International Com- cide on the bean leaf beetle (Coleoptera: Phytopathological Society. On-line, publica- mittee on Taxonomy of Viruses. M. H. V. Chrysomelidae) abundance and damage in tion P-2002-0030-NCA.

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