The Journal of Heredity 2002:93(6)
© 2002 The American Genetic Association 93:447-452
Brief Communication |
Inheritance and Allelism of Resistance to Soybean Mosaic Virus in Zao18 Soybean From China
From the Department of Crop and Soil Environmental Sciences (Liao and Buss), and the Department of Plant Pathology, Physiology, and Weed Science (Tolin), Virginia Polytechnic Institute and State University, Blacksburg, VA 24061; Department of Crop, Soil, and Environmental Sciences, University of Arkansas, Fayetteville (Chen); and the Institute for Genomic Research (Yang).
Address correspondence to Dr. G. R. Buss at the address above, or e-mail: gbuss{at}vt.edu.
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Soybean mosaic disease caused by soybean mosaic virus (SMV) occurs wherever soybean [Glycine max (L.) Merr.] is grown and is considered one of the most important soybean diseases in many areas of the world. Use of soybean cultivars with resistance to SMV is a very effective way of controlling the disease. China has rich soybean germplasm, but there is very limited information on genetics of SMV resistance in Chinese soybean germplasm and reaction of the resistance genes to SMV strains G1–G7. There also is no report on allelic relationships of resistance genes in Chinese soybeans with other named genes at the three identified loci Rsv1, Rsv3, and Rsv4. The objectives of this study were to examine reactions of Chinese soybean cultivar Zao18 to SMV strains G1–G3 and G5–G7, to reveal the inheritance of SMV resistance in Zao18 and to determine the allelic relationship of resistance genes in Zao18 with previously reported resistance genes. Zao18 was crossed with the SMV-susceptible cultivar Lee 68 to study the inheritance of resistance. Zao18 was also crossed with the resistant lines PI96983, L29, and V94-5152, which possess Rsv1, Rsv3, and Rsv4, respectively, to examine the allelic relationship between the genes in Zao18 and genes at these three loci. Our research results indicated that Zao18 possesses two independent dominant genes for SMV resistance, one of which is allelic to the Rsv3 locus; the other is allelic with Rsv1. The presence of both genes (Rsv1 and Rsv3) in Zao18 confers resistance to SMV strains G1–G7.
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Introduction |
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Soybean mosaic virus (SMV) is the most frequently isolated virus of soybean [Glycine max (L.) Merr.] (Thottappilly and Rossel 1987). Soybean mosaic disease caused by SMV occurs worldwide wherever soybean is grown and is regarded as one of the most important soybean diseases in many areas of the world (Hill 1999). It can reduce soybean yield by 10%–30% generally, and up to 50%–100% in severe outbreaks (Buss et al. 1985; Ross 1983; Suteri et al. 1979, 1983). Growing resistant soybean cultivars is a very effective way of controlling the disease.
Many investigators have studied the inheritance of soybean resistance to SMV. Resistance to SMV in soybean is generally conditioned by single dominant genes (Bowers et al. 1992; Buss et al. 1989; Buzzell and Tu 1984; Kiihl and Hartwig 1979; Lim 1985; Roane et al. 1983). However, Kwon and Oh (1980) reported that resistance to a necrosis-inducing strain in Korea is conferred by a single recessive gene. In addition, Koshimizu and Iizuka (1963) reported that the F1 plants were susceptible, and the segregation ratio of the F2 population from the cross Kitaminagaha x Lincoln was roughly 7 resistant:9 susceptible. They concluded that the resistance is controlled by two complementary genes.
Three independent gene loci have been identified for SMV resistance. Kiihl and Hartwig (1979) first identified a single dominant gene for SMV resistance in PI96983 and designated it as rsv1-t. Later Chen et al. (1991) renamed it as Rsv1-t. Buzzell and Tu (1989) found Rsv3 in a line derived from Columbia that conditions systemic necrosis to SMV G1, as defined by Cho and Goodman (1979). Buss et al. (1999) reported a new resistance allele at the Rsv3 locus derived from Hardee and indicated that it confers susceptibility to SMV strains G1–G4, but resistance to SMV strains G5–G7. A gene at a separate locus, tentatively identified as Rsv4, was reported in V94-5152, a line derived from PI486355, that offers resistance to SMV strains G1–G7 (Buss et al. 1997; Hayes et al. 2000). In addition, seven single resistance genes for SMV were also found to be alleles at the Rsv1 locus. They were named Rsv1-t in Ogden, Rsv1-y in York, Rsv1-k in Kwanggyo, Rsv1-m in Marshall, Rsv1-r in Raiden, Rsv1-h in Suweon97, and Rsv1-s in LR2 (derived from PI486355) (Chen et al. 1991, 1993, 2002; Ma et al. 1995).
Soybean originated in China, and there are rich resources of soybean germplasm in China. Inheritance of resistance to SMV has been studied in some Chinese cultivars. In an investigation of the inheritance of resistance to four local strains (Sa, Sc, Sg, and Sh) of SMV in Southern China, Gai et al. (1989) found that the resistance to each of these SMV strains was conferred by the dominant genes A, C, G, and H, respectively. All four loci were shown to be in the same linkage group, with the order of G–H–A–C. In addition, inheritance of resistance to three SMV strains in northeastern China has been investigated. Results demonstrated that resistance to strain SMV-I in Ha88-2501 was controlled by a single dominant gene, while two dominant complementary genes (Chen et al. 1999) conditioned the resistance in Ha88-7704. The resistance to strain SMV-II in Jilin No. 21 and GJ8107-12 was controlled by a single dominant gene, and resistance of both cultivars to strain SMV-III was conditioned by a recessive gene (Sun et al. 1990). Additionally, resistance to strain SMV-II in Ludou No. 4 and Xudou No. 2 was controlled by two complementary genes (Liao et al. 1993, 1994). Direct comparisons among SMV resistance genes from northeastern and southern China cannot be made, because there is no uniform classification of SMV strains in China and allelism tests have not been conducted.
Wang et al. (1998) studied the inheritance of resistance to SMV G1 in four soybean cultivars from China. They have demonstrated that each of these four cultivars has a single dominant gene for resistance to SMV-G1 and that the resistance genes in Kefeng No.1, Dabaima, and Xudou No.1 are not at the Rsv1 locus. The gene in Fengshouhuang is an Rsv1 allele. However, Wang et al. did not study the allelism of these four Chinese cultivars with resistance genes at other loci.
Soybean Zao18 serves as a major resistance source in China and is also used as a differential host in the SMV classification system in northeastern and southern China. Not only is it resistant to all strains in the SMV classification system in the northeast of China, but it is also resistant to the majority of strains identified in southern China. The objectives of this study were (1) to clarify reactions of soybean Zao18 to SMV strains G1–G3 and G5–G7, (2) to determine inheritance of SMV resistance, (3) to determine the allelic relationship of resistance genes in Zao18 with previously described resistance genes, and (4) to reveal the interactions between the genes in Zao18 and two SMV strains G1 and G7.
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Materials and Methods |
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Soybean variety Zao18, developed at the Institute of Genomic Research, China Academy of Sciences, was crossed with SMV-susceptible cultivars Lee 68 and Hefeng No. 25 to study the inheritance of resistance. Zao18 was also crossed with resistant lines PI96983, L29, and V94-5152, which possess Rsv1, Rsv3, and putative Rsv4 (Buss et al. 1997, 1999; Hayes et al. 2000; Kiihl and Hartwig 1979), respectively, to determine genetic allelism. The crosses were made in the field at Blacksburg, Virginia, and F1 plants were grown in the greenhouse or in the field, free of SMV, and harvested individually. The F1 plants were verified as true crosses by using genetic markers such as leaf shape, flower color, pubescence color, and maturity. F2 populations were planted in the field without SMV inoculation, and the plants were harvested individually to obtain F2:3 progenies.
F2 populations were inoculated with SMV strains G1 and G7 in the greenhouse. F2:3 progenies were inoculated with SMV G1 strain in the greenhouse or in the field nursery and with SMV G7 strain in the greenhouse. One hundred or more F2 plants from each cross were screened for SMV reactions, depending on availability of seeds. At least 30 plants from each of 40 to 60 F2:3 progenies derived from a cross were inoculated with SMV G1 or G7 and observed four times for disease reactions at 8-day intervals after inoculation.
Zao18 and other parents were inoculated with SMV strains G1–G3 and G5–G7 to examine disease reaction in the greenhouse. In addition, differential cultivars Lee 68, Essex, York, PI96983, PI507389, V94-5152, and L29 were also included in each set of inoculations to confirm the identity and purity of the SMV strains used.
In the greenhouse, SMV strains G1–G3 were propagated in Lee 68, and SMV strains G5–G7 were propagated in York. Inoculations were performed 7 to 10 days after planting at the unifoliolate leaf stage. Infected leaves were ground in 0.01 M sodium phosphate buffer solution, pH 7.0, at an approximate rate of 1 g infected leaf tissue per 10 ml buffer, with a blender. Before inoculating, 600-mesh carborundum was dusted on the leaves. Both unifoliolate leaves of each plant were rubbed with a pestle dipped in the inoculum. Inoculated leaves then were rinsed with tap water. The temperature was maintained at 20–30°C.
SMV G1 was propagated in cultivar Lee 68 in the greenhouse for use in field inoculations. Inoculum preparation was the same as in the greenhouse and also the same as described by Roane et al. (1983). About 0.2 ml of inoculum was applied to the underside of a single leaflet per plant (V1–V3 stages) by using an artist's airbrush for one second from a distance of 1–2 cm. Air pressure was maintained at 4.2–5.6 kg/cm2 (60–80 psi) by a gasoline-powered portable compressor.
Individual plant reactions were classified into three distinct phenotypes: resistant (R), symptomless or with only local necrotic lesions on inoculated leaves; necrotic (N), systemic local necrosis or stem tip necrosis; or susceptible (S), typical mosaic. All plants with symptoms that did not appear typical of SMV were tested to confirm the presence or absence of SMV by dot blot enzyme-linked immunoabsorbent assays (ELISA) (Srinivasan and Tolin 1992). Plants that tested negative for SMV were assumed to be resistant. Chi-square tests were used to determine the goodness-of-fit of observed segregations to expected genetic ratios and the homogeneity of different populations from the same type of crosses.
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Inheritance of Resistance to SMV Strains G1 and G7 in Zao18
Zao18 exhibits resistant reactions to SMV strains G1–G3 and G5–G7 (Table 1). Hefeng No. 25 is considered a susceptible cultivar in China. However, its reaction to our SMV strains was similar to PI507389 except that the initial necrotic reaction later changed to mosaic when inoculated with SMV strains G1, G2, G5, and G6 (Table 1). Lee 68, a universal susceptible line, showed mosaic reaction to all strains used in this study. The reactions of other parents carrying resistance genes Rsv1, Rsv3, and Rsv4 were in agreement with those reported previously (Buss et al. 1997, 1999; Chen et al. 1991) (Table 1).
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The segregation of F2 populations from Zao18 (R) x Lee 68 (S) showed acceptable fit to a 3R:1S ratio when inoculated with SMV G7, while the F2 populations from Zao18 (R) x Lee 68 (S) and Hefeng No. 25 (S) x Zao18 (R) segregated in a ratio of 3(R+N):1S when inoculated with SMV strains G1 and G7, respectively (Table 2). All three crosses appeared to show segregation for a single gene, and when all three populations were combined for a heterogeneity test, a good fit to 3(R+N):1S was obtained and the populations were segregating homogeneously.
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When the F2:3 progenies derived from Zao18 (R) x Lee 68 (S) were inoculated with SMV G7, an excellent fit to a ratio of 1 (all R):2 (3R:1S):1 (all S) was observed (Table 3). When the F2:3 progenies from this cross were inoculated with SMV G1, and the F2:3 progenies derived from Hefeng No 25 (S) x Zao18 (R) were inoculated with SMV G7, a ratio of 1 (all R):2 [3(R+N):1S]:1 (all S) was observed (Table 3). The heterogeneity test showed that all three crosses were segregating similarly. These data also appear to support the presence of a single gene in Zao18 that is resistant to both SMV strains.
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Some necrotic plants were found in the F2 populations and F2:3 progenies from Zao18 (R) x susceptible crosses, but no homogeneous necrotic F2:3 progenies were observed. All of the necrotic plants (1.2%) were observed in rows that were segregating for SMV reaction. These observations suggest that the necrotic phenotype is associated with genotypic heterozygosity. Similar observations have been reported previously (Bowers et al. 1992; Chen et al. 1991; Kiihl and Hartwig 1979; Ma et al. 1995). For this reason, we combined necrotic plants with resistant plants in testing goodness-of-fit to expected genetic ratios as other researchers have done. If the necrotic plants were treated as a separate class, the data would not fit 1R:2N:1S, due to a deficiency of necrotic plants. This suggests that the phenotypic expression of necrosis is affected by environmental conditions.
Allelic Relationship of the Resistance Gene(s) in Zao18 With Rsv1
No susceptible plants were observed in the F2 population and F2:3 progenies of the cross between PI96983 (R, Rsv1) and Zao18 (R) when inoculated with SMV G1 strain (Tables 2 and 3). Although one necrotic plant in the F2 and four necrotic plants from 3 of 40 F2:3 progenies were found, they did not seem to represent genetic segregation, due to their low frequency and irregular distribution. Similar observations have been reported previously by Chen et al. (1991) and Ma et al. (1995). The complete absence of susceptible plants in the F2 population and F2:3 progenies from PI96983 (R, Rsv1) x Zao18 (R) indicated that Zao18 has a resistance gene at the Rsv1 locus.
However, when SMV G7 was used for inoculation, the F2 population from PI96983 (N, Rsv1) x Zao18(R) exhibited some segregation and provided a good fit to a 12 (R):3 (N):1 (S) digenic ratio (Table 2). When the 60 F2:3 progenies from this cross were inoculated with SMV G7, 7/16 of them exhibited homozygous resistance, homozygous necrosis, or a mixture of resistance and necrosis, 8/16 segregated for resistance or necrosis versus susceptible, and 1/16 showed homogeneous susceptible reactions (Table 4). The 1/16 susceptible plants in the F2 and 1/16 homozygous susceptible progenies in the F2:3 indicated that two independent genes were segregating, one of which is probably an allele at the Rsv1 locus, while the other is at a different locus. When the 8/16 segregating progenies from F2:3 were further analyzed, we found that 50% of them segregated 15 (R+N):1S, 25% segregated 3R:1S and 25% segregated 3N:1S. The overall segregation of the F2:3 progenies from PI96983 (N, Rsv1) x Zao18 (R) thus fits a digenic ratio of 4 (all R):1 (all N):2 (3R:1N):4 [15(R+N):1S]:2 (3R:1S):2 (3N:1S):1 (all S). The appearance of homozygous N families as well as homozygous R families indicates that the Rsv1 gene in Zao18 is different from the Rsv1 gene in PI96983. Additionally, a second gene appears to be segregating that provides complete resistance to SMV G7.
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Allelic Relationship of the Resistance Genes in Zao18 With Rsv3
When the F2 population from the cross between L29 (R, Rsv3) and Zao18(R) was inoculated with SMV G7, no susceptible plants were found (Table 2). The F2:3 progenies from the same cross also did not segregate for reaction to SMV G7 (Table 3). These results indicate that the non-Rsv1 gene in Zao18 is an allele at the Rsv3 locus. When the F2 population from the cross L29 (S, Rsv3) x Zao18 (R) was tested with SMV G1, the segregation provided a good fit to 3 (R+N):1S ratio (Table 2). The F2:3 progenies from the same cross segregated in a ratio of 1(all R):2 [3(R+N):1S]:1(all S) to SMV G1 (Table 3). These data indicate that there is only one gene segregating in the cross of L29 (S, Rsv3) x Zao18 (R) for the reaction to SMV G1. Because the Rsv3 gene in L29 is susceptible to SMV strains G1–G3 but resistant to SMV strains G5–G7 (Table 1), it is apparent that the Rsv3 gene in both L29 and Zao18 is defeated with SMV G1 inoculation. Therefore, segregation of only one gene (Rsv1) was observed in the progenies of the cross of L29 (S, Rsv3) x Zao18 (R) when inoculated with SMV G1.
From all the allelism test data, we conclude that Zao18 has two independent genes for SMV resistance. One of the resistance genes is at the Rsv1 locus and conditions resistance to SMV G1 but susceptibility to SMV G7. The other gene is an allele at the Rsv3 locus, which governs resistance to SMV G7 but is susceptible to SMV G1.
Allelic Relationship of the Resistance Genes in Zao18 With Rsv4
V94-5152 carries the Rsv4 gene, which confers resistance to SMV strains G1 and G7 (Table 1). When the F2 population from the cross of Zao18 (R) and V94-5152 (R, Rsv4) were inoculated with SMV G1 or G7, the digenic segregation ratio of 15 (R+N):1S was obtained (Table 2). The F2:3 progenies from the same cross inoculated with SMV G1 and G7 showed a good fit to 7 (all R):4 [15 (R+N):1S]:4 [3 (R+N):1S]:1 (all S) (Table 3), which would be expected for two genes. These results indicate that neither of the two genes in Zao18 is allelic to the Rsv4 locus. Apparently, when SMV G1 is used for inoculation, the Rsv3 gene in Zao18 is nondetectable, and the Rsv1 gene in Zao18 is defeated when SMV G7 is used. Therefore, the progenies from the cross of V94-5152 (R, Rsv4) x Zao18 (R) exhibited digenic segregation with either SMV G1 or G7 inoculation.
Proposed Genetic Models Explaining the Co-Segregation of the Two Genes (Rsv1, Rsv3) in Zao18 Crossed With Lee 68 (rsv), PI96983 (Rsv1), and L29 (Rsv3)
From the inheritance and allelism test data, we have concluded that Zao18 carries two independent dominant genes. One of the genes is at the Rsv1 locus and is responsible for resistant reaction to SMV G1 but susceptible to SMV G7. The other gene resides at the Rsv3 locus, which confers resistance to SMV G7 but susceptibility to SMV G1. A resistant reaction to both SMV G1 and G7 is expected if both genes are present. In demonstrating the interactions of the two genes and two SMV strains G1 and G7, we propose four theoretical genotypes: Rsv1zRsv1zRsv3zRsv3z (R1zR1zR3zR3z) for Zao18, Rsv1Rsv1rsv3rsv3 (R1R1 r3r3) for PI96983, rsv1rsv1Rsv3Rsv3 (r1r1R3R3) for L29, and rsv1rsv1rsv3rsv3 (r1r1r3r3) for Lee 68, and three genetic models (Tables 5, 6, and 7).
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In the cross of Zao18 (R1zR1zR3zR3z) x Lee 68 (r1r1r3r3), the F2 population exhibits a 3 (R+N):1S segregation to SMV G1 and a 3R:1S segregation to SMV G7. The F2:3 progenies of this cross should segregate in a ratio of 1 (all R):2 [3 (R+N):1S]:1 (all S) to SMV G1 and a ratio of 1 (all R):2 (3R:1S):1 (all S) to SMV G7. Our observations of the F2 population and F2:3 progenies are in a good agreement to the genotypic segregation ratios from the proposed genetic model (Tables 2, 3, and 5). Obviously, only the Rsv1 gene in Zao18 has shown an incomplete dominance nature, resulting in the necrotic phenotype of some heterozygous individuals instead of complete resistance. However, the Rsv3 gene in Zao18 exhibits complete dominance. These research results were comparable to those reported previously. Chen et al. (1991) and Ma et al. (1995) reported that a low frequency of necrotic plants also had been observed in F2 populations from resistant x resistant crosses between parents with alleles at the Rsv1 locus. Also, Rsv3 previously was shown to provide good resistance to SMV G7, even in heterozygotes, whereas most of the alleles at the Rsv1 locus do not (Buss et al. 1999).
In the cross of PI96983 (R1R1r3r3) x Zao18 (R1zR1zR3zR3z), no segregation with SMV G1 can be anticipated, because both parents have a gene at the common Rsv1 locus (Table 6). Therefore, the F2 population and F2:3 progenies would not segregate at all for reactions to SMV G1. However, with SMV G7, the F2 population would segregate in a ratio of 12R:3N:1S, where the necrotic phenotype results from the absence of Rsv3 and the presence of Rsv1. Therefore, the individuals with the genotypes of R1zR1r3r3 and R1R1r3r3 in the F2 population would exhibit necrosis rather than mosaic reaction. These observations are supported by the fact that PI96983 (Rsv1) is necrotic to SMV G7 (Table 1) and Rsv1zfrom Zao18 is susceptible to SMV G7 (Table 4).
With SMV G7 inoculation, the F2:3 progenies derived from F2 individuals with homozygous Rsv3 genotypes should all be resistant regardless of the status of Rsv1 (R1zR1zR3zR3z, R1zR1R3zR3z, and R1R1R3zR3z), whereas progenies from R1zR1zr3r3 plants would be all susceptible and R1R1r3r3 all necrotic. F2:3 progenies from R1zR1zR3zr3, R1zR1r3r3, and R1R1R3zr3 F2 plants would segregate in the ratios of 3R:1S, 3N:1S, and 3R:1N, respectively, whereas the progenies from double heterozygous F2 genotypes would show the same segregation (12R:3N:1S) as in the F2 population. Our allelism test data from the F2 population and F2:3 progenies with SMV G1 and G7 inoculation fit well with the proposed model (Tables 2, 3, 4, and 6).
In the cross of Zao18 (R1zR1zR3zR3z) x L29 (r1r1R3R3), we would expect no segregation at all for SMV G7 inoculation because of the presence of the Rsv3 gene in both parents. However, when inoculated with SMV G1, the F2 population would show a segregation of 3 (R+N):1S, and F2:3 progenies would segregate in a ratio of 1 (all R):2 [3(R+N):1S]:1 (all R) (Table 7). The heterozygous genotypes for the Rsv1 gene would exhibit either resistant or necrotic response, due to the incomplete dominance nature of the Rsv1 gene. It should also be pointed out that the Rsv3 gene is not detectable upon inoculation with SMV G1 strain. Therefore, genotypes with no Rsv1 gene would produce the susceptible response to SMV G1. This observation is in agreement with other previous reports (Bowers et al. 1992; Chen et al. 1991; and Ma et al. 1995). The results from our allelism tests (Tables 2 and 3) are in agreement with the proposed genetic model (Table 7).
Separation of the Two Resistance Genes from Zao18 and Comparison of Their Reactions to SMV Strains
We know that genotypes R1zR1zr3r3 are resistant to SMV G1 but susceptible to SMV G7, and that r1r1R3zR3zis resistant to SMV G7 but susceptible to SMV G1 (Table 5). Therefore, we selected four F2:3 progenies, V00-LR1-1, V00-LR1-2, V00LR3-1, and V00LR3-2, from Zao18 (R) x Lee 68 (S), based on their reactions to SMV G1 in the field. The four progenies were tested in the greenhouse for reaction to SMV G7. Observations that we obtained in the greenhouse and the field showed that V00-LR1-1 and V00-LR1-2 are resistant to SMV G1 in the field but susceptible to SMV G7 in the greenhouse, and V00LR3-1 and V00LR3-2 are susceptible to SMV G1 in the field but resistant to SMV G7 in the greenhouse. It can be assumed that the genotype of V00-LR1-1 and V00-LR1-2 is R1zR1zr3r3 and that of V00LR3-1 and V00LR3-2 is r1r1R3zR3z (Table 5). We tested the four lines in the greenhouse for reactions to SMV strains G1–G3 and G5–G7. The results indicated that the lines V00-LR3-1 and V00-LR3-2 were resistant to SMV strains G5–G7 but susceptible to SMV strains G1–G3; V00-LR1-1 and V00-LR1-2 were resistant to SMV strains G1–G3 but susceptible to SMV strains G5–G7.
These observations further support our conclusion that Zao18 possesses two independent dominant genes, Rsv1 and Rsv3, for SMV resistance. The Rsv1 gene in Zao18 confers resistance to SMV strains G1–G3, and the Rsv3 gene conditions resistance to SMV strains G5–G7. The combination of both genes in Zao18 results in resistance to all SMV strains and provides support for the pyramiding of SMV resistance genes to achieve broader resistance.
Received October 10, 2001
Accepted October 29, 2002
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References |
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Bowers GR, Jr, Paschal EH, II, Bernard RL, Goodman RM, 1992. Inheritance of resistance to soybean mosaic virus in "Buffalo" and HLS soybean. Crop Sci. 32:67-72.
Buss GR, Ma G, Chen P, Tolin SA, 1997. Registration of V94-5152 soybean germplasm resistant to soybean mosaic potyvirus. Crop Sci. 37:1987-1988.
Buss GR, Ma G, Kristipati S, Chen P, Tolin SA, 1999. A new allele at the Rsv3 locus for resistance to soybean mosaic virus. In: Proceedings of World Soybean Research Conference VI. Chicago, IL, August 4–7, 1999 (Kauffman HE, ed). Champaign, IL: Superior Printing; 490.
Buss GR, Roane CW, Tolin SA, 1985. Breeding for resistance to virus in soybeans. In: Proceedings of World Soybean Research Conference III. Ames, IA, August 12–17, 1984 (Shibles R, ed). Boulder, CO: Westview Press; 433–438.
Buss GR, Roane CW, Tolin SA, Chen P, 1989. Inheritance of resistance to soybean mosaic virus in two soybean cultivars. Crop Sci. 29:1439-1441.
Buzzell RI, Tu JC, 1984. Inheritance of soybean resistance to soybean mosaic virus. J Hered. 75:82.
Buzzell RI, Tu JC, 1989. Inheritance of a soybean stem-tip necrosis reaction to soybean mosaic virus. J Hered. 80:400-401.
Chen P, Buss GR, Roane CW, Tolin SA, 1991. Allelism among genes for resistance to soybean mosaic virus in strain differential soybean cultivars. Crop Sci. 31:305-309.
Chen P, Buss GR, Tolin SA, 1993. Resistance to soybean mosaic virus conferred by two independent genes in PI486355. J Hered. 84:25-28.
Chen P, Buss GR, Tolin SA, Gunduz I, Cicek M, 2002. A valuable gene in Suweon 97 soybean for resistance to soybean mosaic virus. Crop Sci. 42:333-337.
Chen Y, Du W, Man W, Zhang G, 1999. An evaluation and screening of soybean germplasms resistant to mosaic virus. Soybean Sci. 18:32-36.
Cho EK, Goodman RM, 1979. Strains of soybean mosaic virus: classification based on virulence in resistant soybean cultivars. Phytopathology. 69:467-470.[Web of Science]
Gai J, Hu YZ, Zhang YD, Xiang YD, Ma RH, 1989. Inheritance of resistance of soybeans to four local strains of soybean mosaic virus. In: Proceedings of World Soybean Research Conference IV. Buenos Aires, Argentina, March 5–9, 1989 (Pascale AJ, ed). Argentina: Orientacion Grafica Editora SRL; 1182–1187.
Hayes AJ, Ma G, Buss GR, Saghai-Maroof MA, 2000. Molecular marker mapping of Rsv4, a gene conferring resistance to all known strains of soybean mosaic virus. Crop Sci. 40:1434-1437.
Hill J, 1999. Soybean Mosaic. In: Compendium of soybean diseases, 4th ed (Hartman GL, Sinclair JB, and Rupe JC, eds). St. Paul, MN: American Phytopathological Society Press.
Kiihl RAS, Hartwig EE, 1979. Inheritance of reaction to soybean mosaic virus in soybeans. Crop Sci. 19:372-375.
Koshimizu S, Iizuka T, 1963. Studies on soybean virus diseases in Japan. Tohoku Nat Agric Exp Stn Bull. 27:1-104.
Kwon SH, Oh JH, 1980. Resistance to a necrotic strain of soybean mosaic virus in soybeans. Crop Sci. 20:403-404.
Liao L, Liu Y, Sun D, Zhao Y, Tian P, 1993. Inheritance of soybean resistance to soybean mosaic virus: II. Inheritance of soybean adult plant resistant to SMV No. 2. Acta Agric Sin. 1:167-170.
Liao L, Liu Y, Sun D, Zhao Y, Tian P, 1994. Inheritance of soybean resistance to soybean mosaic virus: I. Inheritance of several resistance varieties introduced resistance to SMV No. 2. Acta Genet Sin. 21:403-408.
Lim SM, 1985. Resistance to soybean mosaic virus in soybeans. Phytopathology. 75:199-201.[Web of Science]
Ma G, Chen P, Buss GR, Tolin SA, 1995. Genetic characteristics of two genes for resistance to soybean mosaic virus in PI486355 soybean. Theor Appl Genet. 91:907-914.[Web of Science]
Roane CW, Tolin SA, Buss GR, 1983. Inheritance of reaction to two virus in the soybean cross "York" x "Lee 68.". J Hered. 74:289-291.
Ross JP, 1983. Effect of soybean mosaic on component yields from blends of mosaic resistant and susceptible soybeans. Crop Sci. 23:343-346.
Srinivasan I, Tolin SA, 1992. Detection of three viruses of clovers by direct tissue immunoblotting. Phytopathology. 82:721.
Sun Zh, Liu Y, Sun D, Liao L, 1990. Inheritance of resistance to SMV No. 1, No. 2, and No. 3 in soybeans. Oil Crops China. 2:20-24.
Suteri BD, 1979. Effect of soybean yellow mosaic on growth and yield of soybean (Glycine max). Plant Dis Rep. 63:151-153.
Suteri BD, 1983. Effect of soybean mosaic virus on growth of soybean. Indian Phytopathol. 36:719-721.
Thottappilly G, Rossel HW, 1987. Viruses affecting soybean. In: Soybean for the tropics: research, production, and utilization. (Singh SR, Rachie KO, and Dashiell KE, eds). Chichester, U.K.: John Wiley & Sons; 53–68.
Wang Y, Nelson RL, Hu Y, 1998. Genetic analysis of resistance to soybean mosaic virus in four soybean cultivars from China. Crop Sci. 38:922-925.
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