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Published online 27 October 2005
Published in Crop Sci 45:2503-2509 (2005)
© 2005 Crop Science Society of America
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CROP BREEDING, GENETICS & CYTOLOGY

Characterization of Resistance to Soybean mosaic virus in Diverse Soybean Germplasm

C. Zhenga, P. Chena,* and R. Gergerichb

a Dep. of Crop, Soil, and Environmental Sciences
b Dep. of Plant Pathology, Univ. of Arkansas, Fayetteville, AR 72701

* Corresponding author (pchen{at}uark.edu)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Soybean mosaic virus (SMV) causes one of the most destructive viral diseases in soybean [Glycine max (L.) Merr.] worldwide. Ninety-eight SMV isolates identified in the USA have been classified into seven strain groups (G1–G7). Three independent loci (Rsv1, Rsv3, and Rsv4) have been identified for SMV resistance. Multiple resistance alleles have been reported for the Rsv1 and Rsv3 locus. The objective of this research was to group diverse soybean genotypes on the basis of their differential reactions to SMV strains. SMV strains G1 and G7 were used to characterize the reactions of 212 soybean genotypes to SMV. Fifty-five genotypes were resistant to G1 but susceptible to G7, and virus was detected in G7-inoculated plants. Thirty-one genotypes were resistant to G1 but exhibited stem-tip necrosis following G7 inoculation. These 86 soybean genotypes presumably carry alleles at the Rsv1 locus. Thirty-seven genotypes were resistant to G1 and G7, and SMV was not detected by ELISA, indicating that they probably carry Rsv4, Rsv1-r, or Rsv1-h or a combination of two resistance genes Rsv1Rsv3, Rsv1Rsv4, or Rsv3Rsv4. Seven genotypes were susceptible to G1 but resistant to G7 and may carry alleles at the Rsv3 locus. PI 507389 and PI 61944 developed stem-tip necrosis after inoculation with G1 and a mosaic symptom when inoculated with G7, indicating that PI 61944 may carry the same Rsv1-n gene as PI 507389. Eighty soybean accessions developed mosaic symptoms when inoculated with G1 or G7 because of the lack of SMV resistance genes. The information from this research will be helpful in selecting SMV-resistant parents for crossing in a breeding program.

Abbreviations: ELISA, enzyme-linked immunosorbent assay • N, necrotic • R, resistant • S, susceptible • SMV, Soybean mosaic virus


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
SOYBEAN MOSAIC, caused by SMV, is one of the most common and important diseases in soybean worldwide, resulting in substantial yield losses and significant seed-quality deterioration. SMV is seed-borne and transmitted by aphids in a nonpersistent manner. The use of genetic resistance is the most effective and economical strategy for managing SMV. Pathogenic variability among SMV isolates has been widely observed. Symptoms of infection by SMV in soybean include mosaic (light and dark green areas), chlorosis, leaf rugosity, leaf curl, and necrosis (necrotic lesions, veinal necrosis, stem browning, and stem-tip necrosis). Cho and Goodman (1979) classified 98 SMV isolates from seeds in the USDA soybean germplasm collection into seven strain groups (G1–G7) on the basis of their virulence on inoculating a set of eight differential soybean genotypes including two susceptible soybean cultivars (Clark and Rampage) and six resistant cultivars (Buffalo, Davis, Kwanggyo, Marshall, Ogden, and York). G1, the least virulent strain, did not infect any of the resistant cultivars. However, the most virulent strain, G7, infected all cultivars tested and caused necrosis in Marshall, Ogden, Kwanggyo, and Buffalo and mosaic symptoms in Davis and York.

Various sources of SMV resistance have been identified in soybean. Several gene symbols have been assigned for the SMV-resistance alleles identified in the USA. There are three independent loci reported so far for SMV resistance, Rsv1, Rsv3, and Rsv4. Eight resistance alleles have been identified at the Rsv1 locus, namely, Rsv1 in PI 96983, Rsv1-t in Ogden, Rsv1-y in York, Rsv1-m in Marshall, Rsv1-k in Kwanggyo, Rsv1-r in ‘Raiden’, Rsv1-h in ‘Suweon 97’, Rsv1-s in LR1, and Rsv1-n in PI 507389 (Buss et al., 1997; Buzzell and Tu, 1989; Chen et al., 1991, 1993, 1994, 2001, 2002; Kiihl and Hartwig, 1979; Ma et al., 1995, 2003). Two alleles for SMV resistance have been reported at the Rsv3 locus; one was identified in OX 686 soybean line derived from the cultivar Columbia (Buzzell and Tu, 1989), and the other was found in L29 soybean derived from the cultivar Hardee (Buss et al., 1999). The Rsv4 locus was identified in a breeding line V94–5152 derived from PI 486355 x ‘Essex’ and was shown to confer resistance to SMV strains G1 through G7 (Buss et al., 1997; Chen et al., 1993; Ma et al., 1995).

Although three SMV resistance loci have been identified in many soybean genotypes, most of the modern commercial soybean cultivars are susceptible to SMV, particularly to more virulent strains. Identification of SMV resistance in diverse soybean germplasm is important for soybean breeding and production, and discovery of new resistance genes will continue to provide effective SMV resistance to a broad and ever-changing range of SMV isolates. The objective of this research was to group diverse soybean cultivars and lines into putative SMV resistance allele groups on the basis of their differential reactions to two SMV strains so that the available sources of resistance can be efficiently utilized in breeding programs.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Plant Materials
Two hundred twelve diverse soybean genotypes were chosen on the basis of their reactions to SMV in a field nursery where plant introductions, breeding lines, and released cultivars were evaluated. The selected genotypes had shown some level of resistance on the basis of these field observations. Soybean seeds were provided by Dr. Randy Nelson, curator of the USDA Soybean Germplasm Collection, USDA-ARS, at the University of Illinois and Dr. Glenn Buss of Virginia Polytechnic Institute and State University. Seeds were planted in 15-cm-diam plastic pots in the greenhouse. Plants of each genotype (two pots each with eight plants) were inoculated at the unifoliolate leaf stage with SMV strains G1 or G7. Eight plants in one pot per genotype were left uninoculated as a control. Plants were monitored for symptom expression for 4 wk and tested for virus 3 wk after inoculation. Plants were classified as resistant (R, symptomless), necrotic (N, stem-tip necrosis), or susceptible (S, mosaic) (Fig. 1) .



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  		Fig. 1. Symptom expression and plant classification after inoculation with Soybean mosaic virus (SMV). R = resistant (symptomless), N = necrotic (stem-tip necrosis), and S = susceptible (mosaic).

 
Virus Strains
SMV strains G1 and G7 were provided by Dr. Sue Tolin of Virginia Polytechnic Institute and State University and maintained by mechanical inoculation in soybean cultivar Essex. Virus strain identity was verified by inoculation of a set of differential genotypes consisting of V94–5152, L29, PI 96983, PI 507389, York, Essex, and Suweon 97 (Chen et al., 2002; Gunduz et al., 2001; Ma et al., 2003). The reactions of these differential genotypes to SMV strains are summarized in Table 1.


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  		Table 1. Reaction of differential soybean genotypes to two strains of Soybean mosaic virus (SMV).

 
Mechanical Inoculation
Inoculum was prepared by grinding young symptomatic leaves of infected Essex soybean with a mortar and pestle in 0.05 M potassium phosphate buffer, pH 7.2 (approximately 10 mL buffer per g leaf tissue). The inoculum was applied with cheesecloth pads to both unifoliolate leaves of soybean seedlings previously dusted with carborundum (Zheng et al., 2005b).

Test for Virus Infection
Leaf samples of test plants were assayed for SMV infection by Protein-A enzyme-linked immunosorbent assay (ELISA) (Edwards and Cooper, 1985) using anti-SMV rabbit polyclonal antiserum. The middle leaflet from young, expanded, uppermost trifoliolate leaves was collected from each plant in each pot and mixed as one sample for ELISA. Leaf extracts were prepared with a tissue extractor (Erich Pollahne, Germany). Samples of the leaf extracts were tested at a dilution of 1:10 in phosphate buffered saline, pH 7.0, containing 0.1% (v/v) Tween 20 [polyoxyethylene (20) sorbitan monolaurate]. ELISA values were determined spectrophotometrically 30 min after substrate addition at a wavelength of 405 nm with a microplate reader (Model 7250, Cambridge Technology Inc., Cambridge, MA). Samples were considered positive for SMV if ELISA values were three or more times greater than those of healthy plant extracts.

Pedigree Analysis
The pedigrees of selected soybean genotypes were obtained using the Germplasm Resources Information Network (GRIN) System (http://www.ars-grin.gov/npgs/searchgrin.html; verified 17 July 2005), National Plant Germplasm System, USDA-ARS. Pedigree analysis was used only for the U.S. soybean cultivars in this study since the pedigree information for soybean cultivars and plant introductions (PI) from other countries is not readily available on GRIN. The pedigree information was used to trace the specific source of SMV resistance and determine relationships among different resistance sources.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
A set of differential soybean genotypes were selected and inoculated with G1 and G7 to verify the SMV strain identity throughout this study (Table 1). Suweon 97 and V94–5152, carrying Rsv1-h and Rsv4, respectively, were resistant to both G1 and G7, whereas Essex was susceptible to both strains as expected. PI 96983 carrying Rsv1 was resistant to strain G1 but necrotic to G7. York carries Rsv1-y conferring resistance to G1 and mosaic reaction to G7. PI 507389 carries Rsv1-n and is necrotic to G1 but susceptible to G7. L29 contains Rsv3 giving rise to resistance to G7 but susceptibility to G1. The reaction of these differential genotypes to G1 and G7 used in this study was in agreement with previous reports (Chen et al., 2002; Cho and Goodman, 1979; Gunduz et al., 2001, Ma et al., 2003; Zheng et al., 2005a), which confirmed the identity of the SMV strains used for screening. The combination of reactions to G1 and G7 (resistant or susceptible to both, resistant to one and necrotic or susceptible to the other, and necrotic to one but susceptible to the other) allowed the separation of soybean genotypes on the basis of phenotypic response and prediction of resistance alleles at the specific loci.

Two hundred twelve soybean accessions were tested for their response to inoculation with G1 and G7. Fifty-five of the 212 soybean accessions were resistant to G1 (no virus was detected by ELISA in the inoculated plants) and susceptible (mosaic) to G7 (virus was detected by ELISA; Table 2). Twenty-one of these 55 soybean accessions were from Korea, eight from Japan, seven from China, one from Russia, and 18 from the USA. Resistance to G1 and mosaic reaction to G7 are typical characteristics of the Rsv1-y allele in York. These 55 genotypes presumably carry a resistance allele at the Rsv1 locus, which might be the same as or similar to the Rsv1-y allele found in York or the ancestral parents of York (Table 1; Chen et al., 1991).


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  		Table 2. Soybean genotypes that are resistant or necrotic to SMV-G1 and fit the phenotypes produced by alleles at the Rsv1 locus.

 
York was developed from the cross ‘Dorman’ x ‘Hood’. Dorman was derived from the cross between ‘Dunfield’, a collection from Belgium, and ‘Arksoy’, a collection from North Korea. Both Dorman and Arksoy have the same SMV reactions as York (resistant to G1 and susceptible to G7), therefore, the resistance gene in York (Rsv1-y) presumably came from Arksoy via Dorman (Table 2). Hood was a selection from the cross ‘Roanoke’ x N45–745, and N45–745 was derived from Ogden x ‘CNS’. Roanoke was a plant selection of ‘Nanking’ introduced from Nanjing, China. Roanoke is susceptible to both G1 and G7 whereas CNS is susceptible to G1 and resistant to G7 (Tables 3 and 4). Therefore, the resistance to G1 in Hood was most likely derived from Ogden (Rsv1-t).


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  		Table 3. Soybean genotypes that are resistant to SMV-G1 and/or G7 and fit the phenotypes produced by resistance genes Rsv1-r, Rsv1-h, Rsv3, or Rsv4.

 

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  		Table 4. Soybean genotypes that are susceptible to both SMV-G1 and SMV-G7.

 
Pedigree analysis of the 18 G1-resistant but G7-susceptible (mosaic) soybean accessions from the U.S. showed that thirteen soybean genotypes (‘Brim’, ‘Calhoun’, ‘Cook’, ‘Davis’, ‘Dillon’, ‘Doles’, Dorman, L85–2308, ‘Musen’ ‘Prolina’, ‘Ripley’, York, and ‘Young’) have the same ancestral parent, Arksoy, in the pedigree (Table 5). Therefore their resistance to SMV was likely derived from Arksoy. Ripley, Calhoun, and Musen have the same SMV resistant ancestral parent York in the pedigree and their resistance was likely inherited from York and conditioned by Rsv1-y, which presumably originated from Arksoy. Davis was reported to be resistant to G1 and susceptible (mosaic) to G7 (Cho and Goodman, 1979), which agrees with our observation. Davis has a pedigree having Arksoy as one of the ancestral parents and apparently inherited its SMV resistance from Arksoy. Both Young and Prolina have Davis in their pedigree, and Davis is apparently the source of SMV resistance. Brim, Cook, Dillon, and Doles have the common ancestral parent Young, and they inherited SMV resistance from Davis via Young (Table 5). L85–2308 was derived from the backcross of ‘Williams’ (6) x Dorman. Williams is susceptible to G1 and G7, therefore the resistance gene in L85–2308 was evidently derived from Arksoy via Dorman.


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  		Table 5. SMV resistant soybean accessions from the USA and their ancestors as putative contributors for the resistance genes.

 
Thirty-one of the 212 soybean genotypes were resistant to G1 (no virus was detected by ELISA), but exhibited stem-tip necrosis following G7 inoculation (Table 2). Two of these 31 accessions were collected from Korea, 17 from Japan, two from China, and 10 from the USA. These 31 genotypes presumably carry alleles found in PI 96983 (Rsv1), Ogden (Rsv1-t), Marshall (Rsv1-m), or Kwanggyo (Rsv1-k), which confer resistance to G1 but a necrotic reaction to G7 (Chen et al., 1991).

Pedigree analysis of the 10 U.S. soybean accessions that showed stem-tip necrosis to G7, but resistance to G1 indicated that L78–379, L81–4420, and ‘Pace’ inherited their Rsv1 gene from PI 96983 since PI 96983 is one of the common ancestral parents of these accessions and they all have the same SMV reaction as PI 96983 (Table 5). L84–2112 is an isoline of Williams with Rsv1-m derived from Marshall and has the same SMV reaction as Marshall. Further pedigree analysis indicated that ‘Holladay’, Hood, ‘Johnston’, L93–3327, ‘Mercury’, and ‘Saturn’ have Ogden as a common ancestral parent and the same SMV reaction as Ogden, and likely inherited Rsv1-t from this source (Table 5).

The 86 soybean accessions that are resistant to G1 and susceptible (mosaic) or necrotic to G7 likely carry resistance alleles at the Rsv1 locus (Table 2). This conclusion is supported by the phenotypic characteristics of the accession and the pedigrees through which the SMV resistance was inherited. This pedigree analysis indicated that most of the soybean accessions with SMV resistance in the USA carry alleles at the Rsv1 locus which are traced back to common progenitors Ogden, York, PI 96983, Arksoy, or Marshall (Table 5). G1 is a common strain of SMV that occurs wherever soybean is grown. Therefore, most of the resistance sources were bred for and selected against G1. However, this common resistance gene can be overcome by more virulent SMV strains such as G7, as shown in Tables 1 and 2. Research is underway to screen these resistant germplasm selections with additional SMV strains (G2–G6) to differentiate specific alleles at the Rsv1 locus and to confirm phenotypic differential reactions of the 26 U.S. resistant genotypes to SMV strains on the basis of Cho and Goodman's (1979) classification system.

PI 507389 and PI 61944 developed stem-tip necrosis after inoculation with G1 and a mosaic symptom after inoculation with G7, and virus was detected in both necrotic and mosaic plants (Table 2). Therefore, PI 61944 may carry the same Rsv1-n gene as PI 507389 (Ma et al., 2003). Since PI 61944 originated from China and PI 507389 from Japan, the resistance gene in PI 61944 may be a new gene allelic to Rsv1-n or a gene at a different locus. Further genetic research is needed to test the allelic relationship of the gene in PI 61944 and Rsv1-n in PI 507389.

Thirty-seven of the 212 soybean accessions were resistant to both G1 and G7, and virus was not detected by ELISA in the inoculated plants (Table 3), indicating that these resistant soybean accessions carry the Rsv4, Rsv1-h, or Rsv1-r gene. It is also possible that they carry a combination of two resistance genes Rsv1Rsv3, Rsv1Rsv4, or Rsv3Rsv4. Seven of the 37 resistant accessions were from Korea, 14 from Japan, 11 from China, and five from the USA. L88–8431 carries the Rsv1-r derived from Raiden (Table 5) that is resistant to G1 through G4 and G7 but necrotic to G5 and G6 (Chen et al., 2001). L92–8580 may carry Rsv1-h since Suweon 97 was one of its primary ancestors (Table 4). PI 88788 from China carries a resistance gene allelic to Rsv4 in V94–5152, both of which are resistant to all SMV strains identified in the USA (Gunduz et al., 2004). The reactions of V94–5152 and L88–8431, which carry Rsv4 and Rsv1-r derived from PI 486355 and Raiden, respectively, to G1 and G7 were the same as previously reported (Gunduz et al., 2001; Chen et al., 2001).

‘Tousan140’ and ‘Hourei’, both collected from Japan, were reported to carry two dominant genes, Rsv1 and Rsv3, for SMV resistance (Gunduz et al., 2002). A Chinese soybean cultivar Zao 18 was also shown to carry Rsv1 and Rsv3 conferring resistance to all SMV strains (Liao et al., 2002). Pedigree analysis showed that ‘Beeson’ may carry Rsv1-t and Rsv3, which were derived from Ogden and ‘Harosoy’, respectively (Table 5). ‘Columbia’ was reported to carry both Rsv3 and Rsv4 for resistance to all SMV strains (Ma et al., 2002). ‘Virginia’ was selected from ‘Morse’, and Morse was collected from China. Our results revealed that most of the soybean genotypes that are resistant to both G1 and G7 are from the Asian countries China, Japan, and Korea. Pedigree analysis of the five soybean genotypes from the USA that were resistant to both G1 and G7 also demonstrated that the SMV resistance genes originated from China, Japan and Korea. It appears that the abundance of SMV resistance genes in Asia is attributed to the genetic diversity in that region where soybean originated and coevolved with SMV over time. Therefore it is valuable to identify SMV resistance genes in germplasm from foreign countries and incorporate this resistance into U.S. soybean genotypes. Rsv1-h, Rsv4, and the two resistance gene combinations (Rsv1Rsv3, Rsv1Rsv4, and Rsv3Rsv4) provide complete resistance to all identified SMV strains and therefore are valuable genetic resources for a breeding program.

There may be new resistance genes in the soybean accessions having resistance to both G1 and G7 since these accessions have wide geographic origins. Further genetic study is needed to test the allelism with reported resistance genes. Additional screening with other SMV strains (G2 to G6) is in progress to confirm the proposed alleles and determine if any accessions have new alleles. Although the separation of Rsv1-h, Rsv4, the two gene combinations (Rsv1Rsv3, Rsv1Rsv4, and Rsv3Rsv4), and three gene combinations (Rsv1Rsv3Rsv4) was not possible on the basis of phenotypic reactions, in practice all these gene combinations would provide resistance to all SMV strains. In fact, 28 new soybean accessions that are resistant to both G1 and G7 have been identified in this study (Table 3). These materials are valuable germplasm and will serve as an excellent choice of parents for crossing in a breeding program where SMV resistance is an objective.

Seven of the 212 accessions were susceptible to G1 but resistant to G7. Virus was detected in the G1-inoculated plants but not in the G7-inoculated plants (Table 3). One of these accessions was collected from China, one from Canada, one from Zimbabwe, and four from the USA. These accessions presumably carry alleles at the Rsv3 locus as previously reported in L29. However, the occurrence of Rsv3 is rare in soybean germplasm as the only soybean accessions have been reported to carry Rsv3 alleles are L29, Hardee, and Harosoy (Buss et al., 1999; Gunduz et al., 2001). The additional four of the seven soybean accessions identified as being susceptible to G1 and resistant to G7 in this study may also carry resistance alleles at the Rsv3 locus. Pedigree analysis of the four soybean accessions from the USA showed that ‘Cordell’, ‘Bryan’, and Hardee have the same ancestor, CNS (Table 5). It is, therefore, assumed that the resistance to G7 in these cultivars was originally derived from CNS and probably conferred by Rsv3 alleles. L29 is a Williams isoline with SMV resistance derived from Hardee. The pedigree of ‘Rhosa’ is ‘Lincoln’ x ‘Blyvoor’ (South Africa), and the SMV resistance in Rhosa cannot be easily traced to a common ancestor since the pedigree of Lincoln is unknown. The pedigree of Harosoy is ‘Mandarin’ (Ottawa) (2) x ‘A.K.’ (Harrow). Mandarin (Ottawa) was selected from Mandarin in 1929, and Mandarin was selected from PI 36653 introduced from China. A.K. (Harrow) was also collected from China. Therefore, the SMV resistance in Harosoy must have originated from China. CNS from China, Rhosa from Zimbabwe, and Cordell and Bryan from the USA are newly identified soybean cultivars that likely carry Rsv3 alleles for resistance to more virulent strains of SMV.

Eighty soybean accessions were susceptible to both G1 and G7, and virus was detected in all inoculated plants (Table 4). Eight of those germplasm accessions were from Korea, 17 from Japan, six from China, one from Turkey, one from Canada, and 47 from the USA. Pedigree analysis of the 47 susceptible soybean accessions from the USA showed that the susceptibility in most of these accessions traces back to several common susceptible parents such as Clark, Essex, ‘Hill’, ‘Lee’, ‘S-100’, and Williams. A few cultivars in this group such as Camp, Pearl, Vinton, Vinton 81, and Nattosan have been used for the soyfood market. They may potentially produce mottled seeds if infected with SMV, which will affect the seed quality for marketing. These SMV-susceptible germplasm accessions should be avoided when selecting parental materials for crossing when SMV resistance is a priority.

Many new soybean genotypes with SMV resistance have been identified in this study. This diverse collection of resistant germplasm has been grouped by the SMV resistance alleles, each likely contain and will provide valuable parental material for a breeding program in which SMV resistance is an objective. In addition, the genetic classification of the resistant sources will be helpful for breeders to select specific genes for introgression or pyramiding in a breeding strategy to develop soybean cultivars with durable and multiple resistance genes to combat changing SMV strains. Rsv1 alleles are common in soybean germplasm but do not provide a high level of resistance and can be overcome by virulent strains. Rsv3 alleles only confer resistance to more virulent strains. Rsv1-h and Rsv4 provide resistance to all SMV strains and therefore are an excellent choice for genetic resistance sources. Identification and classification of new sources of resistance can be achieved by observing phenotypic reactions to selected SMV strains; however, differentiation between certain genes requires an allelism test and additional genetic studies. Molecular marker techniques may facilitate this process. Research is underway to differentiate alleles at the identified loci and between Rsv1-h and Rsv4.


   ACKNOWLEDGMENTS
 
We thank Dr. G.R. Buss, Virginia Polytechnic Institute and State University, and Dr. R.L. Nelson, USDA-ARS, Urbana, IL, for providing the Glycine max germplasm used in this study. We also thank Dr. S. Tolin, Virginia Polytechnic Institute and State University, for providing SMV strains used in this study. This work was funded in part by the Arkansas Soybean Promotion Board and the United Soybean Board.

Received for publication February 3, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 




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