Bean Pod Mottle Virus (BPMV) Is Wide- Ies Each of a Large (L) and Small (S) Coat Reported (13,49)

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 plants may be discolored. C-terminus (47). BPMV in 1948 on Phaseolus vulgaris L. Furthermore, BPMV predisposes soybeans 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 comoviruses, 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- <HDU coln, NE 68583-07222; E-mail: [email protected]. Fig. 1. Number of F2 bean leaf beetles per 50 sweeps from 1989 to 2001 in central Iowa. Means determined by pooling data from a weekly sampling program conducted Publication no. D-2002-0925-01F on three fields at the Iowa State University Johnson Farm, Ames. Courtesy of Larry P. © 2002 The American Phytopathological Society Pedigo, Wai-Ki F. Lam, and Rayda K. Krell, Entomology Department, ISU. 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 bean leaf beetle (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.

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