Crop Science 42:90-95 (2002)
© 2002 Crop Science Society of America
CROP BREEDING, GENETICS & CYTOLOGY
Characterization of SMV Resistance Genes in Tousan 140 and Hourei Soybean
I. Gunduza,
G. R. Buss*,a,
P. Chena and
S. A. Tolinb
a Dep. of Crop and Soil Environmental Sciences, Virginia Tech, Blacksburg, Virginia 24061-0404
b Dep. of Plant Pathology, Physiology, and Weed Sciences, Virginia Tech, Blacksburg, Virginia 24061-0404
* Corresponding author (gbuss{at}vt.edu)
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ABSTRACT
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‘Tousan 140’ and ‘Hourei’, two soybean [Glycine max (L) Merr.] accessions from Japan, each possess a single gene at different loci for resistance to Japanese Soybean mosaic virus (SMV) strain SMV C. However, more genetic information is needed to utilize these lines in a breeding program. The objectives of this study were to determine (i) the reaction of Tousan 140 and Hourei to SMV-G1 through G7 strains, (ii) the inheritance of SMV resistance in Tousan 140 and Hourei to strains SMV-G1 and G7, and (iii) the allelomorphic relationship of resistance genes in these accessions with previously known resistance genes. Tousan 140 and Hourei were crossed with SMV susceptible cultivar Lee 68 to study the inheritance of resistance. They were also crossed with lines possessing Rsv1, Rsv3, and putative Rsv4, and to each other, to elucidate the allelomorphic relationships among the genes in Tousan 140, Hourei, and previously reported genes. Inheritance and allelism studies indicated that Tousan 140 possesses two SMV resistance genes. These two genes were separated in two F2:3 lines. One of the genes, an allele of Rsv1, expresses resistance to SMV-G1 through G3 and susceptibility to SMV-G5 through G7 while the other one, an allele of Rsv3, expresses resistance to SMV-G5 through G7 and susceptibility to SMV-G1 through G3. Their presence in Tousan 140 makes it resistant to strains SMV-G1 through G7. Hourei also is resistant to SMV-G1 through G7 and possesses two SMV resistance genes, which are also alleles of Rsv1 and Rsv3. One, probably the Rsv1 allele, expresses resistance to SMV-G1 and G7 and the other, probably the Rsv3 allele, expresses resistance to SMV-G7, but is susceptible to G1.
Abbreviations: SMV, Soybean mosaic virus • R, resistant • N, systemic necrosis • LN, local necrosis • S, susceptible • ELISA, enzyme-linked immunosorbent assay
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INTRODUCTION
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CONOVER (1948) first recognized that soybean mosaic disease is caused by more than one strain of Soybean mosaic virus (SMV). Since then, different isolates of SMV strains have been reported. These SMV isolates have been classified into different groups in Japan (Takahashi et al., 1963, 1980), the United States (Cho and Goodman, 1979, 1982), Taiwan (Han and Murayama, 1970), Korea (Cho et al., 1977), Brazil (Almeida, 1981), and China (Pu et al., 1982; Xu et al., 1983; Chen et al., 1986). In the USA, Cho and Goodman (1979) classified 98 SMV isolates into seven strain groups, G1 through G7, on the basis of symptoms induced on a set of soybean differential cultivars. In Japan, 102 SMV isolates were classified into five strains, A, B, C, D and E, on the basis of symptoms induced on soybean cultivars Harosoy, Shiromame, Ou 13, and Tokachinagaha (Takahashi et al., 1980). Eight isolates from China were designated Sa through Sh (Pu et al., 1982; Chen et al., 1986).
Many investigators have studied the inheritance of SMV resistance in soybean to determine the nature and relationship of resistance genes. Three independent gene symbols, Rsv1, Rsv2, and Rsv3 conferring resistance to SMV have been assigned. A single dominant gene for SMV resistance in PI96983 was identified and designated as Rsv (later renamed Rsv1) (Kiihl and Hartwig, 1979; Chen et al., 1991). The single resistance genes in ‘Ogden’, ‘York’, ‘Marshall’, and ‘Kwangyo’ were also found to be alleles at the Rsv1 locus and were assigned the gene symbols, Rsv1-t, Rsv1-y, Rsv1-m, and Rsv1-k, respectively (Chen et al., 1991). PI486355 was found to contain two genes for SMV resistance, one of which is at the Rsv1 locus and was designated Rsv1-s (Chen et al., 1993; Ma et al., 1995). These six Rsv1 alleles confer differential reaction to SMV strains G1 through G7 as defined by Cho and Goodman (1979)(1982). The Rsv1 locus maps to linkage group F and has been associated with closely linked flanking markers (Yu et al., 1994).
The gene symbol Rsv2 was assigned to a gene in OX670, which was presumably derived from Raiden and exhibits resistance to SMV-G1 through G7 (Buzzell and Tu, 1984). However, it has been shown that OX670 carries two genes. One is derived from Raiden and is allelic to the Rsv1 locus, while the other is derived from Harosoy and is allelic to the Rsv3 locus (Gunduz, 2001). A unique Rsv2 locus does not appear to be in OX670 or its ancestors.
The Rsv3 gene derived from ‘Columbia’ conditions systemic necrosis to SMV G1 (Buzzell and Tu, 1989). Another Rsv3 allele from ‘Hardee’ is susceptible to SMV strains G1 through G4 but is resistant to G5 through G7 (Buss et al., 1999).
Chen et al. (1993) and Ma et al. (1995) reported that PI486355 possesses two independent resistance genes, one of which is at the Rsv1 locus. The other resistance gene (non-Rsv1) was isolated in the soybean line LR2 and found to be independent of Rsv1 and Rsv3 (Ma et al., 1995). LR2 was a selection from PI486355 x Essex. V94-5152 is a reselection from LR2 that was registered as germplasm (Buss et al., 1997). Because of the lack of an allelism test with an Rsv2 source, which has since been shown to be nonexistent, a gene symbol was not assigned to the non-Rsv1 gene in V94-5152. However, it will be referred as putative Rsv4 for reference purposes in this paper.
Shigemori (1988) found that the cultivars Tousan 140, Hourei, and Suzuyataka each possess a single gene conferring resistance to the C strain of SMV in Japan. The resistance gene in Tousan 140 was shown to be independent of the resistance gene in Hourei and Suzuyataka, which appeared to be allelic. Segregation of the F2 populations from resistant x resistant crosses of Tousan 140 and Hourei fit a ratio of 15 (resistant+necrotic): 1 mosaic. An allelism test was not conducted to determine relationships between these genes and previously reported loci. The objectives of this study were to determine (i) the reaction of Tousan 140 and Hourei to SMV-G1 through G7 strains, (ii) the inheritance of SMV resistance in Tousan 140 and Hourei, and (iii) the allelomorphic relationship of resistance genes in these accessions with previously known resistance genes.
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MATERIALS AND METHODS
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Tousan 140 and Hourei were crossed to the SMV susceptible cv Lee 68 for determining the number of resistance genes in these accessions. To investigate the allelomorphic relationship between resistance genes in Tousan 140 and Hourei and previously identified genes, these accessions were crossed to resistant lines PI96983, L29, and V94-5152 possessing known genes Rsv1, Rsv3, and putative Rsv4, respectively. Both parents were also crossed to Harosoy. Crosses were made and F1 plants were grown in the greenhouse or in the field at Blacksburg, VA. F2 plants were grown in the field without virus inoculation either at Blacksburg or Warsaw, and individual plants were harvested to obtain F2:3 families. Crosses were distinguished from selfs in F1 and F2 generations by leaf shape, flower color, pubescence color, and maturity as morphological markers.
The F2 populations and F2:3 families were tested with SMV-G1 in the greenhouse and field and with G7 in the greenhouse at Blacksburg, VA. An average of 200 F2 plants per population and 20 F2:3 plants from each of 50 F2:3 families were inoculated. Individual plant reactions in F2 populations and F2:3 families were examined about 10, 20, 30, and 40 d after inoculation and classified into three distinct groups: resistant (R) (symptomless or local necrotic lesions only on inoculated leaves), necrotic (N) (necrosis develops as systemic necrosis and may kill plants 10 to 15 d after inoculation), and susceptible (S) (mosaic). Necrotic plants were observed in F2 populations, and F2:3 families and were combined with resistant plants for genetic analysis because necrosis has been observed to be the expression of some heterozygotes of resistance genes (Kiihl and Hartwig, 1979; Chen et al., 1991)
All parents used in this study were tested with SMV-G1 through G3, and G5 through G7 in the greenhouse to compare their differential reactions. Two strains, SMV-G1 and SMV-G7, were used to screen F1 plants, F2 populations, and F2:3 families. Strain G1 is a Virginia SMV isolate previously designated SMV-VA and classified in Cho and Goodman's (1979) strain group G1 (Hunst and Tolin, 1982). Strains SMV-G2 through G7 were originally obtained in 1984 from Dr. R.M. Goodman, at the University of Illinois.
The SMV-G1 through G3 cultures were maintained by continuous passage in Lee 68, while SMV-G5 through G7 were maintained in York. For the greenhouse tests, inocula were prepared from infected trifoliolate leaf tissue homogenized in 0.01 M sodium phosphate buffer solution, pH 7.0, at an approximate rate of 1 g infected tissue 10 mL-1 buffer. Unifoliolate leaves were inoculated before trifoliolate leaves emerged, approximately 10 d after planting. A small amount of 600 mesh carborundum was dusted on the leaves to be inoculated. Inoculum was applied by rubbing both unifoliolate leaves of each plant with a pestle dipped in the inoculum. Inoculated leaves were rinsed with tap water. The differential cultivars were also included in each test to confirm the identity and purity of the strain used. A daylength of approximately 14 h was maintained using both fluorescent and incandescent supplemental lighting during winter months. Greenhouse temperatures were maintained at 24 to 30°C during daylight hours and 15 to 20°C at night.
Only strain SMV-G1 was used for field inoculation. The procedure used for the field inoculation has been described previously by Roane et al. (1983). Susceptible and necrotic plants in the segregating populations were tested by dot blot enzyme-linked immunosorbent assays (ELISA) (Srinivasan and Tolin, 1992) for confirming infection of SMV in the field. Chi-square tests were performed to determine the goodness-of-fit of observed segregations to expected genetic ratios.
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RESULTS AND DISCUSSION
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Reaction of Tousan 140 to SMV-G1 through G7 and Inheritance of Resistance
Tousan 140 was resistant to all six SMV strains that were used in this experiment (Table 1). However, small necrotic spots were observed on the inoculated leaves of Tousan 140 when inoculated with SMV-G1 and G2 strains. Virus replication and movement is inhibited by rapid tissue death around the virus-invaded area. This hypersensitive response is referred to as localized necrosis. Occasional systemic necrotic plants (5 to 10%) also were observed when Tousan 140 was inoculated with SMV-G1. F1 plants from Tousan 140 x Lee 68 exhibited systemic necrosis when inoculated with SMV-G1 (Table 2), indicating partial dominance of the resistance gene. On the other hand, F1 plants from the same cross were completely resistant to the SMV-G7 strain (Table 2). Segregation in F2 populations from the crosses between Tousan 140 and the SMV-G1 susceptible cultivars Lee 68, L29, and Harosoy was consistent with a 3(R+N): 1S ratio and was homogeneous among populations when inoculated with SMV-G1 (Table 2). Likewise, monogenic 3(R+N):1S inheritance of resistance was observed for the F2 population of Tousan 140 x Lee 68 inoculated with the SMV-G7 strain (Table 2). F2:3 families of Tousan 140 x Lee 68 segregated to fit a 1 (all R): 2 [3(R+N):1S]:1 (all S) ratio when inoculated with either SMV-G1 or G7 (Table 3). Interestingly, no F2:3 families had all systemic necrotic plants, indicating that systemic necrosis was not the expression of any homozygous genotypes in this cross. Necrosis was associated with heterozygosity, as evidenced by the reaction of F1 plants of Tousan 140 x Lee 68 to SMV-G1 (Table 2). Therefore, necrotic plants in the F2 and F2:3 populations were combined with resistant plants for genetic analysis, as done in many previous studies (Kiihl and Hartwig, 1979; Shigemori, 1988; Buss et al., 1989; Chen et al., 1991, 1994; Bowers et al., 1992; Ma et al., 1995).
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Table 2. Reactions of F1 plants and F2 populations from crosses of Tousan 140 with SMV susceptible and resistant soybean genotypes.
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Table 3. Segregation of F2:3 soybean families from crosses of Tousan 140 x Lee 68, Tousan 140 x L29 (Rsv3), and Tousan 140 x PI 96983 (Rsv1) inoculated with SMV-G1 and G7 strains in the greenhouse.
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When the joint segregation of the reactions of the same F2:3 families of Tousan 140 x Lee 68 to SMV-G1 and G7 were examined, the data were consistent with a 1:2:1:2:4:2:1:2:1 genotypic ratio (Table 4). These results strongly suggest that two independent genes control resistance in Tousan 140. One of the genes expresses the resistant reaction to SMV-G1 and is susceptible to SMV-G7, while the other gene is susceptible to SMV-G1 and resistant to SMV-G7. Three F2:3 lines derived from Tousan 140 x Lee 68 were postulated to possess only one of the two resistance genes identified in Tousan 140 because they were homogeneously resistant to SMV-G1 but susceptible to SMV-G7 and were temporarily designated R1. Two other F2:3 lines of Tousan 140 x Lee 68 were homogeneously susceptible to G1 and resistant to SMV-G7, indicating that these lines possess the other resistance gene, temporarily called R2. Seeds of these F2:3 lines were planted and inoculated separately with SMV-G1, G2, G3, G5, G6, and G7 to detect their differential reactions to SMV strains. No segregation for reaction to any of the SMV strains was observed in these F2:3 lines. R1 lines exhibited susceptible reactions to SMV-G5, G6, and G7, but were resistant to SMV-G1, G2, and G3 (Table 1). In contrast, R2 lines exhibited a resistant reaction to SMV-G5, G6, G7 but were susceptible to SMV-G1, G2, and G3. Thus, the SMV resistance gene in the R1 lines shows a resistance pattern similar to Rsv1 alleles (Kiihl and Hartwig, 1979; Chen et al., 1991, 1994), while the SMV resistance gene in the R2 lines exhibits a reaction pattern similar to Rsv3 (Ma, 1995; Buss et al., 1999). Regardless of their identity, it is clear that the two genes combine to make Tousan 140 resistant to each of the strains SMV-G1, G2, G3, G5, G6, and G7.
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Table 4. Segregation of F2:3 soybean families from Tousan 140 x Lee 68 inoculated with SMV-G1 and G7 in the greenhouse.
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A few necrotic plants were observed in the F2 and F2:3 populations of Tousan 140 (R) x PI96983 (R, Rsv1), but no susceptible plants were observed when they were inoculated with SMV-G1 (Tables 2 and 3). The lack of susceptible plants indicated that one of the resistance genes in Tousan 140 is at the Rsv1 locus. Ten percent of the Tousan 140 parental plants included in the test developed systemic necrosis with SMV-G1, which could explain the source of necrotic plants in this segregating population. Necrotic plants have been observed among progeny of R (Rsv1) x R (Rsv1) crosses and were classified as resistant for genetic analysis by other researchers (Chen et al., 1994; Ma, 1995).
No susceptible plants occurred in the F2 and F2:3 populations from Tousan 140 x L29 when inoculated with SMV-G7, indicating that the other resistance gene in Tousan 140 is allelic to Rsv3 (Tables 2 and 3). The F2 population from Tousan 140 (R) x V94-5152 (R, Rsv4) segregated to give a satisfactory fit to a digenic ratio of 15(R+N):1(S) when inoculated with SMV-G1 (Table 2). F2:3 populations of the same cross conformed to a 7 (all R):4[15(R+N):1S]:4[3(R+N):1S]:1 (all S) genotypic ratio (Table 5) when inoculated with G1, indicating that the gene (Rsv1) conferring resistance to SMV-G1 in Tousan 140 is independent of Rsv4.
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Table 5. Segregation of F2:3 soybean families from Tousan 140 x V94-5152 (putative Rsv4) inoculated with SMV-G1 in the greenhouse.
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Reaction of Hourei to SMV-G1 through G7 and Inheritance of Resistance
Hourei is resistant to SMV-G1, G2, G3, G5, G6, and G7 (Table 1). However, when inoculated with the SMV-G1 strain, local necrotic lesions on inoculated leaves and occasional systemic necrotic plants were observed. Ma (1995) reported that the Rsv1-s allele derived from PI486355 also confers local necrosis on inoculated leaves and occasionally develops systemic necrosis.
F1 plants from Hourei x Lee 68 expressed systemic necrosis when inoculated with SMV-G1 (Table 6), which suggests that the resistance gene in Hourei is incompletely dominant and necrosis is associated with heterozygosity. On the other hand, when SMV-G7 was used, F1 plants of Hourei x Lee 68 produced necrotic lesions only on the inoculated leaves, but new leaves remained symptomless and resistant.
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Table 6. Reactions of F1 plants and F2 populations derived from crosses of Hourei with SMV susceptible and resistant soybean genotypes.
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When inoculated with SMV-G1, F2 populations from crosses between Hourei and the SMV-G1-susceptible cultivars Lee 68, L29, and Harosoy segregated to fit a 3(R+N):1S ratio and were homogeneous (Table 6). When SMV-G7 was used, segregation in the Hourei x Lee 68 F2 conformed to the digenic ratio of 15(R+N):1S (Table 6). These results indicated that Hourei possesses two resistance genes. One gene expresses resistant reactions to G1 and G7, while the other gene expresses susceptibility to SMV-G1 and resistance to SMV-G7.
The overall segregation of the F2:3 families from Hourei (R) x Lee 68 (S) fit a genotypic ratio of 1 (all R): 2[3(R+N):1S]:1 (all S) when the population was inoculated with SMV-G1 (Table 7). However, the same F2:3 families segregated with a 7(all R):4[15(R+N):1S]: 4[(3R+N):1S]:1 (all S) genotypic ratio, when SMV-G7 was used as inoculum (Table 8). These results verified the F2 population data and confirmed that Hourei has two genes. The two genes in Hourei act in a complimentary manner to confer resistance to SMV-G1, G2, G3, G5, G6, and G7.
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Table 7. Segregation of F2:3 soybean families from the crosses of Hourei x Lee 68, L29 x Hourei, L78-379 x Hourei, and Hourei x Tousan 140 inoculated with SMV-G1 and G7 in the greenhouse.
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Table 8. Segregation of F2:3 soybean families from Hourei x Lee 68 when inoculated with SMV-G7 in the greenhouse.
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Systemic necrotic plants observed in the segregating populations of Hourei x Lee 68 were associated with heterozygosity, as the F1 plants exhibited a necrotic reaction when SMV-G1 was used (Table 6). Therefore, necrotic plants in F2 and F2:3 populations were combined with resistant plants for chi-square analysis. When SMV-G7 was used, Hourei x Lee 68 F1 plants produced local necrotic lesions on inoculated leaves but no systemic necrosis was observed (Table 6). However, systemic necrotic plants were observed in the F2 population and F2:3 families. No F2:3 families were completely necrotic.
No susceptible plants occurred in the F2 populations or F2:3 families derived from L78-379 x Hourei inoculated with G1 or in L29 x Hourei populations inoculated with SMV-G7 (Tables 6 and 7). This indicated that one of the genes in Hourei is allelic to Rsv1, and the other is an allele at the Rsv3 locus. The F2 population from V94-5152 x Hourei segregated to fit a digenic segregation ratio of 15 (R+N):1(S) when inoculated with SMV-G1 (Table 6). Segregation among F2:3 families of V94-5152 x Hourei conformed to a 7 (all R): 4[15(R+N):1S]:4[3(R+N):1S]:1 (all S) genotypic ratio and were homogeneous in the field and greenhouse tests (Table 9).
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Table 9. Segregation of F2:3 soybean families from V94-5152 (putative Rsv4) x Hourei inoculated with SMV-G1 in the greenhouse and field.
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When SMV-G1 was used, no susceptible plants were observed in F2 populations of Hourei x Tousan 140, Tousan 140 x Hourei (Table 6), or in F2:3 families of Tousan 140 x Hourei (Table 7). This result corroborates the individual allelism studies of Hourei and Tousan 140 which indicated that both cultivars possess alleles at the Rsv1 and Rsv3 loci. However, 25% of the Hourei x Tousan 140 F2 population expressed a systemic necrotic reaction (Table 6), and there were some necrotic plants in 42 of the 50 F2:3 families (Table 7). None of the F2:3 families had all systemic necrotic plants, which indicated that systemic necrosis was not the expression of any homozygous genotype. Hourei and Tousan 140 both exhibited local necrotic lesions on the inoculated leaves and occasional systemic necrotic plants were observed on each in response to SMV-G1 in greenhouse and field tests. The frequency of necrotic plants observed in the F2 and F2:3 populations of Tousan 140 x Hourei was approximately equal to the frequency of necrotic plants observed in both parents. Ma (1995) also observed that a line, possessing a gene at Rsv1 typically exhibited local necrosis on inoculated leaves, but occasionally developed systemic necrosis in the greenhouse at a high temperature when inoculated with SMV-G7. Similarly, Ali (1950) reported that bean (Phaseolus vulgaris L.) usually exhibited local necrosis on inoculated leaves when inoculated with Common bean mosaic virus in the field, but developed top necrosis (systemic necrosis) in the greenhouse at high temperatures.
When SMV-G7 was used, a few F2 plants of Tousan 140 x Hourei and the reciprocal cross exhibited local necrotic lesions on inoculated leaves but no susceptible plants were observed (Table 6). This confirms that genes conferring resistance to G7 in Tousan 140 and Hourei are allelic. However, Shigemori (1988) reported that Tousan 140 and Hourei each possess a single dominant gene conferring resistance to Japanese C strain, but at different loci. Our classification and analysis of disease data are identical with Shigemori (1988). A difference in SMV strains used in the two studies could explain the contradictory results obtained. Possibly the Tousan 140 and Hourei alleles at each locus exhibit reciprocal resistances to Japanese C strain. Thus each cultivar has a single gene for resistance to strain C, but both genes are seen to segregate in the F2 derived from crossing the cultivars. If this is true, then Hourei and Tousan 140 must possess different alleles at both Rsv1 and Rsv3, since the opposite loci conferred resistance to the Japanese C strain in the two parents. In fact, results of our study indicate that the Rsv1 allele in Tousan 140 expresses resistance to SMV-G1 and susceptibility to SMV-G7 (Tables 1, 2 and 3), while the Rsv1 allele in Hourei confers a resistant reaction to both SMV-G1 and G7 (Tables 6, 7, and 8). The Rsv1 allele in Tousan 140 appears to be different from other alleles at the Rsv1 locus. It exhibits local necrotic lesions on inoculated leaves to SMV-G2 strain, while none of the other alleles at Rsv1 exhibit such a reaction (Chen et al., 1991). The Rsv3 alleles in Tousan 140 and Hourei exhibit a reaction similar to other alleles at the Rsv3 locus (Table 1; Buzzell and Tu, 1989).
Results of this study clearly show that Tousan 140 and Hourei each possess two SMV resistance genes and that each cultivar has a gene at the Rsv1 and Rsv3 loci. The presence of both genes in each of these accessions makes them resistant to more strains than is provided by either of the single genes. This would appear to justify the strategy of pyramiding to provide more effective and durable resistance to SMV.
Received for publication March 7, 2001.
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Crop Sci.,
March 19, 2008;
48(2):
517 - 526.
[Abstract]
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A. Shi, P. Chen, C. Zheng, A. Hou, and B. Zhang
A PCR-based Marker for the Rsv1 Locus Conferring Resistance to Soybean Mosaic Virus
Crop Sci.,
January 16, 2008;
48(1):
262 - 268.
[Abstract]
[Full Text]
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C. Zheng, P. Chen, and R. Gergerich
Genetic Analysis of Resistance to Soybean Mosaic Virus in J05 Soybean
J. Hered.,
September 1, 2006;
97(5):
429 - 437.
[Abstract]
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C. Zheng, P. Chen, and R. Gergerich
Characterization of Resistance to Soybean mosaic virus in Diverse Soybean Germplasm
Crop Sci.,
October 27, 2005;
45(6):
2503 - 2509.
[Abstract]
[Full Text]
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TOP
ABSTRACT
INTRODUCTION
