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Crop Science 42:333-337 (2002)
© 2002 Crop Science Society of America

CROP BREEDING, GENETICS & CYTOLOGY

A Valuable Gene in Suweon 97 Soybean for Resistance to Soybean Mosaic Virus

Pengyin Chena, Glenn R. Buss*,b, Sue A. Tolinc, Irfan Gunduzb and Mine Cicekb

a Dep. of Crop, Soil, and Environmental Sciences, Univ. of Arkansas, Fayetteville, AR 72701
b Dep. of Crop and Soil Environmental Sciences, Virginia Polytechnic Institute and State Univ., Blacksburg, VA 24061
c Dep. of Plant Pathology, Physiology, and Weed Science, Virginia Polytechnic Institute and State Univ., Blacksburg, VA 24061

* Corresponding author (gbuss{at}vt.edu)


   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
‘Suweon 97’ (PI 483084) soybean [Glycine max (L.) Merr.] from Korea is resistant (R) to all strain groups (G1–G7 and G7A) of soybean mosaic virus (SMV) identified in the USA. The objectives of this study were to determine the number of loci conditioning SMV resistance and the relationships between the Suweon 97 gene and other genes for SMV resistance. Suweon 97 was crossed to susceptible (S) cultivars Essex and Lee 68 for the inheritance study. For the allelism test, Suweon 97 was crossed with SMV resistant cultivars possessing the Rsv1, Rsv3, and Rsv4 genes. The F2 data from R x S crosses showed a good fit to the monogenic ratio of 3[R+Necrotic(N)]:1S. The F2:3 progenies from the R x S crosses exhibited a ratio of 1R: 2 segregating: 1S, indicating that Suweon 97 has a single dominant gene for SMV resistance. The presence of N plants in R x S crosses suggests the Suweon 97 gene for SMV resistance is incompletely dominant. None of the F2 populations and F2:3 progenies from crosses of Suweon 97 with other resistant cultivars having Rsv1 alleles segregated for susceptibility to five SMV strains, suggesting that the Suweon 97 gene is an allele at the Rsv1 locus. Data from crosses with Rsv3 and Rsv4 cultivars exhibited good fit to dihybrid ratios. This digenic segregation verifies that the Suweon 97 gene resides at a locus other than Rsv3 and Rsv4. In contrast to other previously identified SMV resistance genes, none of which are resistant to all SMV strains, Suweon 97 is immune to all SMV strains in the USA, thus a valuable source of genetic resistance. The gene symbol Rsv1-h is proposed for the resistance gene in Suweon 97.

Abbreviations: SMV, soybean mosaic virus • R, resistant • N, necrotic • S, susceptible


   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
CHO AND GOODMAN (1979)(1982) described a set of seven strain groups (G1–G7) of soybean mosaic virus (SMV) that could be differentiated by resistant, mosaic, or necrotic reactions on five cultivars having resistance to the common strain (G1) of SMV. The differential cultivars included ‘Buffalo’, ‘Kwanggyo’, ‘Ogden’, ‘Marshall’, and ‘Davis’. Most of these SMV-resistance sources were found to be resistant to some, but not all seven strains.

Inheritance of SMV resistance has been studied by a number of investigators using various SMV strains or isolates and different soybean types. Resistance to some mosaic-inducing strains is conditioned by single dominant genes (Bowers et al., 1992; Buss et al., 1985, 1989a, b; Buzzell and Tu, 1984; Kiihl and Hartwig, 1979; Koshimizu and Iizuka, 1963; Lim, 1985; Roane et al., 1983), whereas resistance to a necrosis-inducing strain has been reported to be controlled by a single recessive gene (Kwon and Oh, 1980). In addition, two complementary genes (Koshimizu and Iizuka, 1963) and four linked genes (Gai et al., 1989) for SMV resistance have been reported. Tu and Buzzell (1987) also showed that stem-tip necrosis on soybean was a hypersensitive and temperature-dependent reaction, and was conferred by a single dominant gene.

Three independent loci have been identified for SMV resistance and several gene symbols have been assigned to previously recognized genes. The Rsv1 locus was first identified in PI 96983 for resistance to SMV-G2 and G3 and was shown to provide a high level of resistance to SMV (Kiihl and Hartwig, 1979). Ogden was demonstrated to carry a gene designated rsv1-t at the Rsv1 locus. The rsv1-t gene gave protection against SMV only in the homozygous condition and was recessive to Rsv1. Both of these genes were dominant to rsv in susceptible cultivars (Kiihl and Hartwig, 1979). Three additional genes were later reported at the Rsv1 locus for SMV resistance, Rsv1-y in York, Rsv1-k in Kwanggyo, and Rsv1-m in Marshall (Chen et al., 1991). These three allelic genes are partially dominant and confer differential reactions to the seven SMV strain groups.

Rsv2 was found in a breeding line ‘OX670’, a derivative of resistant cultivar Raiden, for resistance to SMV-G7 and G7A, and was shown to be independent of Rsv1 (Buzzell and Tu, 1984). However, this gene was later proven to be allelic to the Rvs1 locus and assigned a new gene symbol Rsv1-r (Chen et al., 2001). Tu and Buzzell (1987) reported a stem-tip necrosis symptom in the cultivar Columbia and some of its progenies in response to SMV-G1 and G4. Later in a genetic study, they found that the necrotic reaction was controlled by a single gene which was dominant to the gene conferring mosaic reaction. This gene was shown to be at a locus independent of both Rsv1 and Rsv2, therefore, was assigned the gene symbol Rsv3 (Buzzell and Tu, 1989). Buss et al. (1999) reported a new resistance allele at the Rsv3 locus in L29 which is an isoline of ‘Williams’ and contains a gene derived from ‘Hardee’. This gene in L29 provides resistance to more virulent SMV strains (G5 to7) but is susceptible to SMV-G1 to G4. Rsv4 (Hayes et al., 2000) was identified in a breeding line, V94-5152 (Buss et al., 1997) derived from PI 486355 which was demonstrated to possess two independent genes for SMV resistance (Chen et al., 1993). The other gene from PI 486355 was shown to be an allele at the Rsv1 locus and was designated as Rsv1-s (Ma et al., 1995).

Suweon 97 (PI483084) is resistant to all seven identified SMV strains (Cho and Goodman, 1982; Lim, 1985) and can serve as a desirable source of SMV resistance in a breeding program. However, the inheritance of resistance in Suweon 97 has not been completed and no allellism tests have been done against other named genes. This study was conducted to characterize further the inheritance of SMV resistance in Suweon 97 and to determine the allelomorphic relationships between the resistance gene in Suweon 97 and those previously reported.


   MATERIALS AND METHODS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Suweon 97 was crossed with SMV-susceptible cultivars Essex and Lee 68. Advanced progenies from these crosses were tested with different SMV strains to determine the inheritance of resistance. Suweon 97 was also crossed with SMV resistant soybean lines PI 96983(Rsv1), Ogden(Rsv1-t), York(Rsv1-y), Marshall(Rsv1-m), Kwanggyo(Rsv1-k), Raiden(Rsv1-r), L29 (Rsv3), and V94-5152(Rsv4) to determine allelic relationships of the Suweon 97 gene with other genes for resistance at three separate loci, Rsv1, Rsv3, and Rsv4. The methods used in this study have been described previously (Chen et al., 1991, 1994) except that several F2 populations from different crosses were screened with SMV-G1 in the field nursery (Groseclose loam soil) at Blacksburg, Virginia. In the field tests, each F2 population from a cross was planted in three rows (approximately 40–45 seeds/row) 0.9 m long with 0.9 m between rows. Also included in the field tests were single rows of parental and susceptible check cultivars.

Strains SMV-G1, G5, G6, G7, or G7A were used, as appropriate, to observe genetic segregations and were maintained in greenhouse-grown susceptible plants. SMV-G2, G3, and G4 were not used for inoculation because of greenhouse space limitations for strain maintenance and propagation. In addition, inoculations with those strains would not be likely to provide additional genetic information. Greenhouse inoculation was done with a mortar and pestle while field inoculations were performed by an air-brush technique (Chen et al., 1991). Individual plant reactions were classified as R, N, or S (Chen et al., 1991, 1994). Chi-square tests were used to examine the goodness-of-fit of observed segregations to expected genetic ratios and to determine whether comparable populations from the same type of cross were homogeneous.

In presenting results of inoculations of segregating progenies, the original cross is classified as resistant x resistant (R x R) if both parents are resistant to the SMV strain used for inoculation, while the same cross is referred to as resistant x susceptible (R x S) or as resistant x necrotic (R x N) if one of the parents is susceptible or necrotic to the virus strain used for inoculation. Necrotic plants were combined with R plants in R x S crosses for use in Chi-square tests.


   RESULTS AND DISCUSSION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
The reactions of five F2 populations from Suweon 97 x susceptible crosses and the parents indicated monogenic inheritance (Table 1). The F2 plants from Suweon 97 x Lee 68 segregated with an acceptable fit to a ratio of 3(R+N):1S when inoculated with SMV-G1 in the greenhouse and in the field. The Suweon 97 x Essex cross exhibited a good fit to 3(R+N):1S segregation with SMV-G6 inoculation in the greenhouse but a poor 3:1 fit in the field test because of a deficiency of susceptible plants. However, the reciprocal cross Essex x Suweon 97 showed an excellent fit to the 3(R+ N):1S segregation when inoculated with G7A in the greenhouse. These observations suggest that Suweon 97 carries a single gene with partial dominance for resistance to SMV strains G1, G6, and G7A. When data for all five F2 populations were combined, a poor fit to the 3(R+N):1S was obtained because of the overall deficiency of susceptible plants. However, all five R x S populations were homogeneous for the 3:1 segregation of reactions to the three strains tested.


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  		Table 1. Segregation and {chi}2 tests for SMV reactions in F2 populations from Suweon 97 (R) x susceptible (S) soybean crosses in the greenhouse and field.

 
Both crosses showed satisfactory fit to a ratio of 1(all R), 2 segregating for 3(R+N):1S, and 1(all S) in F2:3 lines, which would be expected from the segregation of a single gene (Table 2). The pooled data from the two R x S crosses provided a good fit to the monogenic 1:2:1 segregation and the two populations were homogeneous. These F2:3 results provide further evidence that Suweon 97 has a single gene for SMV resistance.


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  		Table 2. Reactions of F2:3 lines from Suweon 97 (R) x susceptible (S) soybean crosses following inoculation with SMV-G1 in the field.

 
With G7A inoculation of crosses with lines having Rsv1 alleles, both Suweon 97 x Marshall and Suweon 97 x York segregated satisfactorily into a ratio of 3(R+N):1S as expected from a monogenic segregation (Table 3). The York x Suweon 97 cross exhibited a rather poor fit to the 3:1 segregation when inoculated with G6 because of a deficiency of susceptible plants, thus resulting in an unsatisfactory overall fit to the expected ratio. However, the three populations were homogeneous for monohybrid segregation.


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  		Table 3. Genetic segregation of SMV reactions in F2 populations from Suweon 97 (R) x susceptible (S) soybean crosses in the greenhouse when inoculated with virulent strains.

 
Six F2 populations of Suweon 97 x necrotic crosses when screened with four SMV strains in the greenhouse showed a good fit to 3R:1N ratio, indicating the presence of a single gene in Suweon 97 for SMV resistance (Table 4). Since there were no susceptible plants observed in all six R x N populations, it shows that the Suweon 97 gene is allelic to the other genes at the Rsv1 locus. Also if the gene for resistance were independent of the gene for necrosis, one would expect 1/16 susceptible segregants in a R x N cross. Even if the two genes were closely linked, a few susceptible plants would be observed in the R x N F2 populations. The complete lack of susceptible segregants in nearly 1000 plants from six populations makes the existence of separate genes controlling the R and N reactions highly unlikely.


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  		Table 4. Reactions of F2 populations from Suweon 97 (R) x necrotic (N) soybean crosses to selected SMV strains in the greenhouse.

 
F2 populations of R x R crosses of Suweon 97 with the other five resistant lines carrying Rsv1 alleles showed no susceptible segregants, providing strong evidence that the single gene in Suweon 97 is an allele at the Rsv1 locus (Table 5). Although the possibility of close linkage between the Suweon 97 gene and other Rsv1 alleles cannot be ruled out, the complete absence of susceptible plants in more than 1500 plants from seven populations and three SMV-strain combinations appears to support allelism rather than linkage. The occasional necrotic plants observed in some of the R x R crosses did not actually represent any genetic segregation since some of the parents also occasionally give a necrotic reaction.


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  		Table 5. Reactions of F2 soybean populations from R x R crosses of Suweon 97 and other resistant cultivars carrying Rsv1 alleles when inoculated with SMV strains in the greenhouse and field.

 
Data of 414 F2:3 lines from Suweon 97 x other resistant cultivars carrying Rsv1 alleles with field inoculations indicated homogeneous resistant reaction (Table 6). No susceptible plants were observed in 7865 plants screened. These results provide additional evidence that the resistance gene in Suweon 97 is allelic to Rsv1.


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  		Table 6. Reactions of F2:3 soybean lines from R x R crosses of Suweon 97 and other resistant genotypes possessing Rsv1 alleles when inoculated with SMV-G1 in the field.

 
The F2 population of Suweon 97 x V94-5152 (Rsv4) showed an excellent fit to a 15R:1S ratio as expected from the segregation of two independent dominant genes (Table 7). The F2:3 lines from the same cross also exhibited a good fit to a digenic segregation of 7(all R):4(15R:1S):4(3R:1S):1(all S). When inoculated with SMV-G1 strain, the F2 population from L29 x Suweon 97 segregated into a ratio of 3R:1S and the F2:3 lines from the same cross showed a good fit to 1(all R):2(3R:1S):1(all S). These monogenic segregation ratios were expected because L29 is susceptible to G1 and the Rsv3 gene in L29 is non-functional for resistance. However, when this cross was inoculated with G7, the F2 population exhibited an excellent fit to a 15R:1S as anticipated from a digenic segregation. This is because both the Suweon 97 gene and Rsv3 in L29 confer resistance to G7 and the two genes are at different loci.


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  		Table 7. Segregation and {chi}2 tests for SMV reactions of F2 soybean populations and F2:3 lines from allelism test crosses of Suweon 97 with Rsv3 and Rsv4 genotypes.

 
In our experiment, the F2 populations from R x S crosses involving Suweon 97 produced some necrotic plants. These necrotic plants were considered heterozygotes and were combined with the resistant class, as others have done (Kiihl and Hartwig, 1979; Bowers et al., 1992). Any other classification would not provide a good fit to either monohybrid or dihybrid genetic ratios. The presence of a number of necrotic plants in the R x S F2 populations indicates incomplete dominance of the Suweon 97 gene.

The results of this study clearly indicate that Suweon 97 has a single dominant gene at the Rsv1 locus for SMV resistance. Although this gene shows partial dominance as other Rsv1 alleles do, it provides genetic protection to a wider range of SMV strains than any of the other genes at the Rsv1 locus (Table 8). Thus, Suweon 97 is a valuable source of genetic resistance to SMV because it is immune to all the SMV strains identified in the USA. Other Rsv1 alleles can be defeated by at least one of the seven strains, thus giving rise to necrotic or susceptible reactions. Suweon 97 is an experimental line derived from the cross of Shirome Nagaha (a Japanese cultivar) with a F2 plant from (Kwanggyo x Clark 63) and released as the cultivar, Hwang-Kum-Kong, in Korea (S.D. Kim, personal communication, June 30, 1999). This cultivar has served as a primary source of SMV resistance in Korea. The gene in Suweon 97 appears to have been inherited from Shirome Nagaha since the Kwanggyo gene (Rsv1-k) confers resistance to only four SMV strains (G1 to G4), but is necrotic to others (G5–G7, G7A) (Table 8). Clark 63 is susceptible to all SMV strains (Cho and Goodman, 1979). We propose that the gene symbol Rsv1-h be assigned to the SMV resistance gene in Suweon 97.


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  		Table 8. Comparison of differential reactions of soybean genotypes with Rsv1 genes to identified SMV strains.

 

   NOTES
TOP
 NOTES
ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
This research was supported in part by a grant from the Virginia Soybean Board.

Received for publication January 24, 2001.


   REFERENCES
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 




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