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Journal of Heredity Advance Access originally published online on May 19, 2008
Journal of Heredity 2008 99(6):598-603; doi:10.1093/jhered/esn035
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Genetic Confirmation of 2 Independent Genes for Resistance to Soybean Mosaic Virus in J05 Soybean Using SSR Markers

Ainong Shi, Pengyin Chen, Dexiao X. Li, Cuiming Zheng, Anfu Hou, and Bo Zhang

From the Department of Crop, Soil, and Environmental Sciences, University of Arkansas, 115 Plant Science, Fayetteville, AR 72701

Address correspondence to P. Chen at the address above, or e-mail: pchen{at}uark.edu.

J05 soybean was previously identified to carry 2 independent genes, Rsv1 and Rsv3, for "soybean mosaic virus" (SMV) resistance by inheritance and allelism studies. The objective of this research was to confirm the 2 genes in J05 using molecular markers so that a marker-assisted selection can be implemented. The segregation of F2 plants from J05 x Essex exhibited a good fit to a 3:1 ratio when inoculated with SMV G1. Three simple sequence repeat (SSR) markers near Rsv1, Satt114, Satt510, and Sat_154, amplified polymorphic DNA fragments between J05 and Essex and were closely linked to the gene on soybean molecular linkage group (MLG) F, thus verifying the presence of Rsv1 in J05 for resistance to SMV G1. The presence of Rsv3 in J05 was confirmed by 2 closely linked SSR markers on MLG B2, Satt726 and Sat_424, in F2:3 lines that were derived from the SMV G1-susceptible F2 plants and segregated in a 1:2:1 ratio for reaction to SMV G7. Two closely linked markers for Rsv4, Satt296 and Satt542, segregated independently of SMV resistance, indicating the absence of Rsv4 in J05. These SSR markers for Rsv1 and Rsv3 can serve as a useful molecular tool for selection and pyramiding of genes in J05 for SMV resistance.

"Soybean mosaic virus" (SMV) is one of the most destructive viral diseases, causing substantial yield loss and seed quality reduction in soybean (Glycine max [L.] Merr.). Pathotypic variability among SMV isolates has been widely observed worldwide. Symptomology on soybean is often used to classify SMV isolates into strains. Phenotypic reactions of soybean to SMV strains include resistant (R, symptomless), necrotic (N, foliar necrotic lesions, leaf vein and/or stem necrosis), and susceptible (S, mosaic, light and dark green areas or leaf rugosity, leaf curl, and chlorosis). Isolates were grouped into strains on the basis of their virulence and symptoms on differential soybean genotypes (Chen and Choi 2008). Different SMV strain groups were reported in different countries, and the relationships among these groups have not been determined (Takahashi et al. 1980; Choi et al. 2005; Guo et al. 2005). In the United States, Cho and Goodman (1979, 1982) classified 98 isolates collected from soybean germplasm into 7 strain groups (G1 through G7).

The use of genetic resistance is the primary method of controlling this disease. Three independent loci, Rsv1, Rsv3, and Rsv4, have been reported for SMV resistance and 9 alleles have been identified at the Rsv1 locus: Rsv1 (Kiihl and Hartwig 1979), Rsv1–m (Buss et al. 1989; Chen et al. 1991), Rsv1-y (Roane et al. 1983; Chen et al. 1991), Rsv1-r (Chen et al. 2001), Rsv1-k (Buss et al. 1989; Chen et al. 1991), Rsv1-t (Kiihl and Hartwig 1979; Chen et al. 1991), Rsv1-h (Lim 1985; Chen et al. 2002), Rsv1-s (Chen et al. 1993), and Rsv1-n (Ma et al. 2003). Rsv1 alleles confer resistance to some, but not all, of the 7 SMV strains identified in the United States, Some Rsv1 alleles also give rise to a necrotic reaction to some SMV strains. The alleles at Rsv3 condition resistance to SMV G5 through G7, but not G1 through G4, whereas Rsv4 alleles confer resistance to all 7 SMV strains.

Rsv1 was first identified in PI 96983 (Kiihl and Hartwig 1979) and later mapped on molecular linkage group (MLG) F (Yu et al. 1994). Two restriction fragment length polymorphism (RFLP) markers, pA 186 and pK 644a, and 1 simple sequence repeat (SSR) marker, SM176, were found to be tightly linked to Rsv1 with distances of 1.5, 2.1, and 0.5 cM, respectively (Yu et al. 1994). A random amplified polymorphic DNA (RAPD) marker OPN11 closely linked to Rsv1 was first reported by Li et al. (1998), and this linkage relationship was confirmed by single nucleotide polymorphism (SNP) markers designed from an OPN11 clone (Jeong and Saghai Maroof 2004). A similar RAPD marker OPN11980/1070 and its derived sequence-characterized amplified region marker SCN11980/1070 were also identified to be linked to Rsv1 with a distance of 3.03 cM (Zheng et al. 2003). A high-resolution map of the Rsv1 region containing 38 loci was later constructed with 24 markers including 1 RAPD (OPN11), 4 SSR (HSP176, 64-A8C, Satt510, and Satt120), and 19 RFLP markers; Rsv1 was flanked by HSP176 (2.9 cM) and Satt510 (2.4 cM); and the closest SSR marker to Rsv1 was 64-A8C (0.5 cM) (Gore et al. 2002). Subsequently, Rsv1 was postulated to reside near Sat_154 on MLG F based on the soybean SSR linkage map (Cregan 2003). Recently, a polymerase chain reaction (PCR)–based marker has been developed for tagging the Rsv1 alleles and has great potential in marker-assisted selection for SMV resistance (Shi et al. 2008).

Rsv3 originated from "L29" (Buss et al. 1999), a derivative of "Hardee," and was later mapped on MLG B2 by flanking markers A519F/R (designed from RFLP clone A519 at 0.8–0.9 cM) and M3Satt (designed from RFLP clone M3a at 0.8 cM) (Jeong et al. 2002). The linkage relationship between A519 and Rsv3 was confirmed by SNP markers from RFLP clone A519 in L29 (Jeong and Saghai Maroof 2004). The Rsv3 locus was mapped at 3.0–6.0 cM from the SSR marker Satt063 on MLG B2 (Jeong et al. 2002). Rsv4 was identified in V94-5152 (Buss et al. 1997; Ma et al. 1995) and later mapped on MLG D1b by 2 flanking SSR markers, Satt542 at 4.7 cM and Satt558 at 7.8 cM (Hayes et al. 2000). More recently, Hwang et al. (2006) developed a fine map for the region around Rsv4 in V94-5152, adding 2 SSR markers (Satt634 and Satt254) and 5 expressed sequence tag markers closer to the Rsv4 locus. The Rsv4 locus is located at around 1.9 cM near SSR marker AI856415 on MLG D1b based on the soybean linkage map (Cregan 2003).

"J05" is a Chinese soybean cultivar developed by the Institute of Crop Breeding and Cultivation, Chinese Academy of Agricultural Science, in China. J05 was reported to be resistant to the most virulent strains of SMV in Northeastern China and resistant to all 7 SMV strains identified in the United States. J05 was shown to contain 2 SMV resistance genes, Rsv1 and Rsv3, based on classic genetic analysis and allelism tests (Zheng et al. 2006). The objectives of this research were to confirm the 2 genes (Rsv1 and Rsv3) for SMV resistance in J05 using SSR markers and identify molecular markers closely linked to the 2 genes for marker-assisted selection and for gene pyramiding of SMV resistance in soybean breeding programs.


   Materials and Methods
Top
 Materials and Methods
Results and Discussion
 References
 
Plant Materials and SMV Resistance Tests
Shown in Figure 1 are the procedures for genetic population development and phenotypic evaluation of reaction to SMV. In order to obtain phenotypic data for confirmation of the 2 genes in J05, a cross between J05 (Rsv1Rsv3) and a susceptible cultivar "Essex" (rsv) was made. F1 plants were grown without SMV inoculation to generate an F2 plant population. The reactions of F2 plants to SMV G1 (referred to as G1 hereafter) were used to confirm the presence of Rsv1 in J05 because Rsv1 confers resistance to G1 and Rsv3 gives rise to susceptibility to G1. The susceptible plants from the F2 population were harvested separately to develop F2:3 lines. The reactions to SMV G7 (referred to as G7 hereafter) of those F2:3 lines derived from the G1-susceptible F2 plants were used to confirm the presence of Rsv3 in J05 because these F2:3 lines did not contain Rsv1 and G7 inoculation would reveal the presence or absence of Rsv3.


Figure 1
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  		Figure 1. The scheme of population development and phenotypic evaluation for reactions to SMV strains G1 and G7 used for confirmation of the 2 genes (Rsv1 and Rsv3) in J05 soybean.

 
All plants were grown in 15-cm–diameter plastic pots under greenhouse conditions with 24 °C temperature and 14-h photoperiod at Harry R. Rosen Alternative Pest Control Center of University of Arkansas, Fayetteville, AR. Single plant from the F2 population was grown in each pot for DNA samples and SMV inoculation. Reactions to SMV strains G1 to G7 were evaluated in separate greenhouses. Virus inoculum was prepared by grinding systemically infected leaves from strain-maintaining plants with a mortar and pestle in 0.05 M potassium phosphate buffer pH 7.2 at an approximate dilution of 1:10 (w/v). Inoculations were performed by rubbing the inoculum onto both unifoliolate leaves that had been previously dusted with carborundum (Chen et al. 1991; Zheng et al. 2005). SMV strains G1 and G7 were provided by Dr Sue Tolin of Virginia Polytechnic Institute and State University. 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" (Gunduz et al. 2001; Chen et al. 2002; Ma et al. 2003). Plants were classified as resistant (R, symptomless), necrotic (N, stem-tip necrosis), or susceptible (S, mosaic). F2:3 lines were classified as homozygous resistant, segregating, or homozygous susceptible based on individual plant reactions.

DNA Extraction and PCR-Based Assay
Genomic DNA was extracted from fresh leaves of greenhouse-grown plants using the hexadecyltrimethyl ammonium bromide method (Kisha et al. 1997). Thirty-two PCR-based markers including 11 SSR markers around the Rsv1 locus, 7 around Rsv3, and 14 around Rsv4, were used to screen for polymorphism between J05 and Essex (Table 1). Those that showed polymorphism between the 2 parents were further used to detect SMV resistance genes in each plant of the F2 population or individual F2:3 lines.


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  		Table 1. PCR-based markers around 3 independent loci for SMV resistance and their position from the telomeric end on the soybean linkage map

 
Among the 11 selected markers around the Rsv1 locus on MLG F, HSP176L, which was later renamed as SOYHSP176 on the soybean composite genetic map (Cregan 2003), was selected as it was first found to be tightly linked to Rsv1 (Yu et al. 1996). The closest SSR marker to Rsv1 was 64-A8C (0.5 cM), but it was not available. Therefore, Satt510 and Sat_120 with a genetic distance of 2.4 and 3.8 cM to the Rsv1 locus, respectively, were selected according to Gore et al. (2002). Another marker used for Rsv1 screening was Satt114, which is linked to the PCR-based marker Rsv1-f/r with a distance of 5.42 cM (Shi et al. 2008). In addition, 7 SSR markers on MLG F were selected from the region of 18.5 cM spanning both sides of the Rsv1 locus according to soybean genetic composite map to ensure polymorphism (Cregan 2003).

Among the 7 markers surrounding the Rsv3 locus on MLG B2, Satt063, A519, and M3Satt were selected based on their close linkage (3.2–6.3 cM, 0.8–0.9 cM, and 0.8 cM, respectively) to Rsv3 (Jeong et al. 2002). Additional 4 SSR markers on MLG B2 near the Rsv3 locus within a region of 15.7 cM were also selected from the soybean composite genetic map to ensure polymorphism (Cregan 2003). Among the 14 selected markers for Rsv4 on MLG D1b, 2 flanking markers, Satt542 (4.7 cM) and Satt558 (7.8 cM), were selected according to Hayes et al. (2000). Ten additional markers linked to Rsv4 on MLG D1b including Sat_254, BF070293 [GenBank] -S, AI856415-g, AI856415-S, BI470504 [GenBank] , Satt634, BF070293 [GenBank] , AW417852R, AW307114A, and Satt266 were selected based on a recent report by Hwang et al. (2006). Also included in the maker selection for Rsv4 were AI856415 and Satt296 selected from the soybean composite genetic map to ensure polymorphism (Cregan 2003).

PCR amplification was performed in an iCycler Thermal Cycler (Bio-Rad Laboratories, Inc., Hercules, CA) following standard PCR procedures with minor modifications. Briefly, each 50 µl PCR reaction mixture consisted of 36 µl sterilized ddH2O, 5 µl 10X PCR buffer (Promega, Madison, WI), 3 µl MgCl2 (25 mM), 1.5 µl deoxynucleoside triphosphate (10 mM total, 2.5 mM each), 1.5 µl each primer (20 ng/µl), 0.2 µl Taq polymerase (Promega) (5 U/µl), and 1.3 µl template DNA (20 ng/µl). PCR cycles consisted of an initial denaturation step at 94 °C for 5 min followed by 38 cycles of 45 s at 94 °C, 45 s at 45–55 °C depending on the primer Tm, and 1 min at 72 °C followed by an extension step at 72 °C for 5 min and a 4 °C soak. The PCR products were separated on 6% nondenaturing polyacrylamide gel or 1.0–1.5% agarose gel in 0.5x TBE and visualized by staining with ethidium bromide.

Data Analysis
Phenotypic segregation ratios for SMV reactions and the molecular data of the F2 population and F2:3 lines derived from J05 x Essex were tested for goodness of fit and independence using a chi-square test (Liu 1998). Linkage analysis was performed based on the maximum likelihood estimator (Allard 1956). The recombination fraction was calculated using an SAS program kindly provided by Dr Ben-Hui Liu, Department of Forestry in North Carolina State University, NC (Liu BH, unpublished data). The recombination fraction between loci was transformed according to the Kosambi function as described by Weir (1996).


   Results and Discussion
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 Materials and Methods
 Results and Discussion
References
 
The phenotypic segregation of G1 reaction in the F2 population derived from J05 x Essex showed an excellent fit to the 3:1 ratio as expected for a single dominant gene for resistance (Table 2). Three out of 11 SSR makers around the Rsv1 locus, Satt114, Satt510, and Sat_154, amplified polymorphic DNA fragments between J05 and Essex, and the Figure 2 shows an example for the differential amplifications from the SSR marker Satt114 in 34 F2 plants derived from J05 x Essex and 2 parents (J05 and Essex) on 6% nondenaturing polyacrylamide gel. The phenotyping and genotyping data further demonstrated that these 3 markers are closely linked to Rsv1 on soybean MLG F, thus verifying the presence of Rsv1 in J05 for resistance to G1. The gene Rsv1 in J05 was mapped on MLG F and flanked by Sat_154 and Satt510 with 0.5 and 2.3 cM, respectively (Figure 3). Satt114 is 4.3 cM upstream from Rsv1 along the same side of Sat_154. The mapping result for the Rsv1 region in the present study is in good agreement with reports by Yu et al. (1994) and Gore et al. (2002) and the soybean SSR linkage map by Cregan (2003) and Cregan et al. (1999). Therefore, the gene for resistance to G1 in J05 is confirmed to be Rsv1.


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  		Table 2. Segregation of the F2 population and F2:3 lines derived from J05 x Essex when inoculated with SMV G1 and G7, respectively

 


Figure 2
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  		Figure 2. DNA fragments amplified from Satt114 in 34 F2 plants from J05 x Essex and the 2 parents (J05 and Essex) on 6% nondenaturing polyacrylamide gel. P1 = J05, P2 = Essex, R = the F2 plants resistant to SMV G1, and S = the F2 plants susceptible to SMV G1. Lane M is a 100-bp DNA molecular ladder.

 


Figure 3
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  		Figure 3. Genetic map for the Rsv1 region on MLG F with closely linked SSR markers identified in this study.

 
The segregation among resistant, segregating, and susceptible F2:3 lines derived from the selected G1-susceptible F2 plant from J05 x Essex showed a good fit to a ratio of 1:2:1 as expected for a single dominant gene for reaction to G7 (Table 2). Two SSR makers around the Rsv3 locus, Sat_424 and Satt726, amplified polymorphic DNA fragments between J05 and Essex, and the Figure 4 represents an example for the differential pattern of amplification from the SSR marker Satt726 in 36 G1-susceptible F2 plants derived from J05 x Essex on 1.5% agarose gel. Using the phenotyping and genotyping data, Sat_424 and Satt726 were shown to be closely linked to the resistance gene on soybean MLG B2, thus confirming the presence of Rsv3 in J05 for resistance to G7. Rsv3 in J05 was mapped on MLG B2 with a distance of 1.5 cM from Sat_424 and 2.0 cM from Satt726 (Figure 5). These results are in agreement with the report by Jeong et al. (2002) and the soybean SSR linkage map by Cregan (2003) and Cregan et al. (1999). Therefore, the gene for resistance to G7 in J05 is confirmed to be Rsv3.


Figure 4
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  		Figure 4. DNA fragments amplified from Satt726 in 36 G1-susceptible F2 plants derived from J05 x Essex on 1.5% agarose gel. R = the F2 plant producing resistant or segregating F2:3 lines to SMV G7 and S = the F2 plant producing F2:3 lines susceptible to SMV G7. Lane M is a 100-bp DNA molecular ladder.

 


Figure 5
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  		Figure 5. Genetic map for the Rsv3 region on MLG B2 with closely linked SSR markers identified in this study.

 
Two SSR markers around Rsv4, Satt296 and Satt542, amplified polymorphic DNA fragments between J05 and Essex and were shown to be independent for resistance to G1 in the F2 population derived from J05 x Essex, thus confirming that J05 does not contain the gene Rsv4 for SMV resistance.

This research confirmed the presence of 2 genes, Rsv1 and Rsv3, for SMV resistance in J05 and 5 SSR markers were confirmed to be closely linked to the 2 resistance genes. The study demonstrates an efficient strategy for identifying the 2 genes for SMV resistance in a given cultivar using molecular markers and phenotypic reactions. When 2 resistance genes segregate in a population, selection for each individual gene can be achieved by inoculation with differential SMV strains. However, selection for individuals with both resistance genes is solely dependent on the use of molecular markers. The identified SSR markers that are closely linked to Rsv1 (Satt114 and Sat_154) and Rsv3 (Sat_424 and Satt726) in J05 should be useful in marker-assisted selection for the 2 independent genes in breeding for SMV resistance.


   Footnotes
 
Corresponding Editor: Reid Palmer

Received January 9, 2008
Accepted April 14, 2008


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