Journal of Heredity 2004:95(4):322-326
© 2004 The American Genetic Association
Genetics of Resistance to Two Strains of Soybean Mosaic Virus in Differential Soybean Genotypes
From Medtronic Sofamor Danek, 1800 Pyramid Place, Memphis, TN 38132 (Ma); Department of Crop, Soil, and Environmental Sciences, University of Arkansas, Fayetteville, AR 72701 (Chen); Departments of Crop and Soil Environmental Sciences (Buss) and Plant Pathology, Physiology, and Weed Science (Tolin), Virginia Tech, Blacksburg, VA 24061-0404.
Address correspondence to Pengyin Chen at the address above, or e-mail: pchen{at}uark.edu.
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Abstract |
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There are seven pathotypes of soybean mosaic virus (SMV) representing seven strain groups (G1–G7) in the United States. Soybean genotypes [Glycine max (L.) Merr.] may exhibit resistant (R), susceptible (S), or necrotic (N) reactions upon interacting with different SMV strains. This research was conducted to investigate whether reactions to two SMV strains are controlled by the same gene or by separate genes. Two SMV-resistant soybean lines, LR1 and LR2, were crossed with the susceptible cultivar Lee 68. LR1 contains a resistance gene Rsv1-s and is resistant to strains G1–G4 and G7. LR2 contains the Rsv4 gene and is resistant to strains G1–G7. Two hundred F2:3 lines from LR1 x Lee 68 and 262 F2:3 lines from LR2 x Lee 68 were screened for SMV reaction. Seeds from each F2 plant were randomly divided into two subsamples. A minimum of 20 seeds from each subsample were planted in the greenhouse and plants were inoculated with either G1 or G7. G1 is the least virulent, whereas G7 is the most virulent strain of SMV. The results showed that all the F2:3 lines from both crosses exhibited the same reaction to G1 and G7. No recombinants were found in all the progenies for reactions to G1 and G7 in either cross. The results indicate that reactions to both G1 and G7 are controlled by either the same gene or very closely linked genes. This research finding is valuable for studying the resistance mechanism and interactions of soybean genotypes and SMV strains and for breeding SMV resistance to multiple strains.
Soybean mosaic virus (SMV) occurs wherever soybean is grown and causes yield loss and seed quality deterioration in many soybean production areas worldwide (Hartman et al. 1999; Hunst and Tolin 1982; Ross 1987). Cho and Goodman (1979, 1982) classified 98 SMV isolates found in the United States into seven strain groups, G1 through G7, based on the symptoms induced on a set of soybean differential cultivars. There are five SMV strains (A to E) identified in Japan (Takahashi et al. 1980) and eight strains (Sa through Sh) reported in China (Chen et al. 1986; Pu et al. 1982), but their pathotypic relationships to G1 through G7 are not known.
Various sources of resistance have been identified in soybean, most of which are resistant to some, but not all of the SMV strains (Cho and Goodman 1979, 1982; Gai et al. 1989a; Koshimizu and Lizuka 1963; Kwon and Oh 1980; Lim 1985). In most cases, resistance is controlled by single dominant genes (Buzzell and Tu 1984, 1989; Chen et al. 1991, 1994, 2001, 2002; Kiihl and Hartwig 1979; Zhang et al. 1989). There are three independent loci for SMV resistance: Rsv1, Rsv3, and Rsv4. Nine resistance alleles at the Rsv1 locus have been reported (Chen et al. 1991, 1994, 2001, 2002; Kiihl and Hartwig 1979; Ma et al. 1995, 2003), and two alleles have been identified at the Rsv3 locus (Buss et al. 1999; Buzzell and Tu 1989). The Rsv4 locus (Hayes et al. 2000) was identified in a breeding line, LR2, which was released as V94-5152 (Buss et al. 1997). Several molecular markers have been identified for Rsv1, Rsv3, and Rsv4 (Hayes et al. 2000; Jeong et al. 2002; Yu et al. 1994). Rsv2 was assigned to the resistance gene derived from the cultivar Raiden (Buzzell and Tu 1984), but this gene was later changed to Rsv1-r due to its allelism with the Rsv1 locus (Chen et al. 2001).
The interaction of SMV with its soybean host is complex, involving a number of different strains and several loci with multiple alleles. To cope with multiple strains occurring naturally in the field, it is very important for breeders to know the genetic relationship of soybean resistance to different strains of the virus. When resistance to different strains is controlled by genes at separate loci, it is possible to incorporate as many genes as needed into one cultivar for multiple resistance. If genes for resistance to different strains are alleles at a single locus, a given homozygous cultivar can only contain a resistance gene from one source, making gene pyramiding for multiple resistance virtually impossible through traditional breeding methods. The objective of the present study was to determine whether soybean reactions to two strains are governed by the same gene or by separate genes.
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Materials and Methods |
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Two SMV-resistant lines, LR1 and LR2, were crossed with the susceptible cultivar Lee 68. LR1 and LR2 were two sister lines derived from Essex x PI 486355 and carry single genes at independent loci for SMV resistance (Chen et al. 1993; Ma et al. 1995). LR1 contains Rsv1-s and is resistant to strains G1–G4 and G7, but gives necrotic reaction to G5 and G6. LR2 carries a gene at the Rsv4 locus and is resistant to all strains G1–G7 (Hayes et al. 2000; Ma et al. 1995). A single representative plant from each of LR1 and LR2 was used as the female parent for crossing to maintain genetic purity. Precautions were also taken to prevent outcrossing and to avoid seed mixtures during seed production and generation advancement. F1 plants were grown in the greenhouse and threshed by hand. F2 seeds from a single F1 plant of each cross were planted by hand in an isolated field where SMV is seldom observed. Individual F2 plants were harvested and threshed separately.
To determine the genotype of each F2 plant for reactions to G1 and G7, a minimum of 20 seeds (F2:3) from each F2 plant were planted in the greenhouse in each of two 15 cm pots containing 40% topsoil and 60% commercial soil mix. Plants in one pot were inoculated with G1 and plants in the other pot were inoculated with G7. Two hundred F2:3 lines from LR1 x Lee 68 and 262 F2:3 lines from LR2 x Lee 68 were tested. Individual plant reactions were classified as resistant (R, no symptoms), necrotic (N, systemic necrosis), or susceptible (S, systemic mosaic). Based on individual plant reactions, F2:3 lines were classified into homogeneous resistant (all R), segregating, and homogeneous susceptible (all S). In the cross of LR1 x Lee 68, necrotic plants were observed in segregating F2:3 lines and combined with resistant plants for the chi-square test for goodness-of-fit to expected genetic ratios since the resistance gene in LR1 is partially dominant and some of the heterozygotes express systemic necrosis (Ma et al. 1995).
The two SMV strains used, G1 and G7, are the least virulent and the most virulent strains, respectively, in Cho and Goodman's (1979, 1982) classification system. The inoculation procedure, virus cultures, and greenhouse conditions were as described previously (Chen et al. 1991, 1994; Ma et al. 1995).
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Results and Discussion |
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When inoculated with SMV-G1, the F2:3 lines from LR1 x Lee 68 showed a good fit to a 1 (all R):2 segregating:1 (all S) ratio and the overall segregation of all plants in the segregating F2:3 lines exhibited a good fit to a ratio of 3 (R + N):1 S (Table 1). The same result was obtained for the same set of F2:3 lines following inoculation with SMV-G7. Occasional necrotic plants were observed in both the resistant parent, LR1, and some otherwise totally resistant F2:3 lines, especially with SMV-G7 inoculation. Perfect agreement in reaction to the two strains was observed in all the progenies. Any disagreements would be the result of recombination between the gene for resistance to G1 and the gene for resistance to G7. The lack of any recombination indicates that either the same gene in LR1 confers resistance to both strains or, if separate genes exist, they are tightly linked. The results of Gore et al. (2002) support the latter hypothesis. They found a very low percentage of F2 plants from PI 96983 x Lee 68 that produced a necrotic reaction to G1 which was very similar to the reactions of other Rsv1 alleles. Molecular mapping indicated that these plants contained a crossover within the Rsv1 locus, suggesting that the Rsv1 locus actually consists of a group of tightly linked resistance genes. While the populations in our study were reasonably large, they probably were not large enough to detect crossovers of the frequency observed by Gore et al. (2002).
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We have reported previously that the resistance gene Rsv1-s in LR1 is allele dosage dependent, with the dominant homozygotes conferring resistance while the heterozygotes exhibit necrosis to G7. When inoculated with G1, only a portion of heterozygotes expressed necrosis (Ma et al. 1995). We obtained similar results in the present study. However, when inoculated with G7, the necrotic plants were more than the expected 50% in the segregating F2:3 lines from LR1 x Lee 68, and thus resulted in a rather poor fit to the 1 R:2 N:1 S ratio. Since the surplus of necrotic plants closely matches the deficiency of resistant plants, it appears likely that some homozygous dominant plants expressed systemic necrosis as observed in the resistant parent LR1 (Table 1).
In the cross of LR2 x Lee 68 inoculated with G1, the F2:3 lines segregated with a good fit to a ratio of 1 (all R):2 segregating:1 (all S), and the segregating F2:3 lines provided an excellent overall fit to a 3 R:1 S ratio (Table 2). When inoculated with G7, F2:3 lines showed the same pattern of segregation. No necrotic plants were observed in any of the progenies. The results revealed that the gene for resistance to G1 and the gene for resistance to G7 in LR2 were either the same gene or very closely linked genes, since no recombinants were observed for reactions to the two strains.
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This conclusion is supported by the fact that an SMV-resistant isoline of the susceptible cultivar Essex showed the same reactions to strains G1 through G6 (resistant) and G7 (necrotic) as did the resistant donor parent, PI 96983, which carries a single dominant gene Rsv1. Selections were made for resistance to only one SMV isolate (G1) during 11 generations of crossing and backcrossing (Buss et al. 1989a). Similarly L78-379, a resistant isoline of the susceptible cultivar Williams, developed by six generations of backcrossing with PI 96983 as the resistant donor parent, shows the same reactions to strains G1–G7 as PI 96983 (Bernard et al. 1991; Cho and Goodman 1982). These observations suggest that a single gene or very closely linked genes, rather than distantly linked or independent genes, conferred resistance to different SMV strains in PI 96983.
Our results conflict with those of Gai et al. (1989b), who reported that resistance to each of four local strains in China was conditioned by a single gene and the four resistance genes were located at separate, but loosely linked loci with recombination frequencies ranging from 13% to 28%. Although their sources of resistance and SMV strains were different from those used in this study, the discrepancy is perhaps the result of their using a different system of symptom classification for genetic analysis. They combined necrotic plants with susceptible plants in the susceptible class. In most other reports on the inheritance of SMV resistance, necrotic plants observed in segregating populations from R x N and R x S crosses have been interpreted as being the expression of heterozygotes of resistance genes. Thus necrotic plants were combined with resistant ones as a resistant class for the purpose of genetic analysis (Bowers et al. 1992; Buss et al. 1989b; Chen et al. 1991, 1994; Kiihl and Hartwig 1979; Ma et al. 1995; Shigemori 1988).
The necrosis expression in heterozygotes may also be strain dependent. A heterozygote that shows complete resistance to less virulent strains may give necrosis to more virulent strains of SMV (Chen et al. 1991, 1994; Ma et al. 1995). In such cases, some segregating progenies that contained necrotic and susceptible plants, but no resistant plants, as the result of testing only a small number of plants for each F2:3 progeny, could be classified as homogeneous susceptible to one strain, as was probably done according to the classification of Gai et al. (1989b). However, the same progeny could be classified as segregating (for resistance and susceptibility) to other strains which do not induce necrosis on homozygotes and/or heterozygotes. The result would give a false conclusion that recombinations had occurred. Gai et al. (1989b) did not specify the number of plants tested for each F2:3 progeny or distinguish homozygous resistant F2 genotypes from heterozygous F2 genotypes in their analysis.
A desirable goal of breeding for SMV resistance is to incorporate resistance to as many strains as possible to reduce the likelihood that strains occurring in the field would overcome resistance in new cultivars. When resistance to different strains is conditioned by independent genes, a breeder can simply make crosses between cultivars with resistance to different strains and select for resistance to multiple strains. Unfortunately this is not the case as revealed in the present study. In fact, resistance to different strains in a given soybean line can be controlled by a single gene or very closely linked genes, as demonstrated in this study. Although the possibility that resistance to two SMV strains is conditioned by very closely linked genes cannot be ruled out, it is not important to make such a distinction between a single gene and very closely linked genes from the practical breeding point of view. In either case, the gene(s) would behave as a single genetic unit. The majority of SMV resistance sources studied to date contain a single gene at the Rsv1 locus (Chen et al. 1991, 1994, 2001, 2002; Kiihl and Hartwig 1979; Zhang et al. 1989). Most of these alleles confer resistance to some, but not all, of strains G1 through G7, and furthermore, one or more virulent SMV strains may induce systemic necrosis on soybean lines with these resistance alleles (Chen et al. 1991, 1994; Ma et al. 1995). This will impose a risk when those resistance genes are utilized. The necrotic reaction can be much more deleterious to the plant than the mosaic symptom since necrotic plants produce virtually no seeds (Buss et al. 1989a). An outbreak of the disease with necrosis, caused by a severe strain called SMV-N, was reported in Korea on cultivars that were resistant to the common SMV strains (Cho et al. 1977). Obviously, in a breeding strategy for SMV resistance, high priority should be given to searching for resistance genes at different loci, particularly at loci other than Rsv1.
We have shown that the Rsv4 gene in LR2 is completely dominant and confers resistance to all strains G1–G7 (Hayes et al. 2000; Ma et al. 1995). This gene appears to be very desirable in a breeding program, but reliance on a single source of resistance would result in genetic uniformity and potential vulnerability. Gene pyramiding to incorporate resistance genes at different loci into a single soybean line might be desirable for developing cultivars with durable resistance to multiple strains of SMV. Through gene pyramiding, two or more resistance genes functioning against different SMV strains can be combined in a homozygous cultivar. If one of the resistance genes is defeated by one strain, other genes may still work against that strain, thus preventing a breakdown of resistance. However, it would be difficult to pyramid the two genes studied here since the presence of Rsv1-s could not be detected in a line that also contains the Rsv4 gene from LR2, which is resistant to strains G1–G7. Gene pyramiding would be greatly facilitated by using molecular markers closely linked with the resistance genes. Several molecular markers closely linked to Rsv1 (Yu et al. 1994), Rsv3 (Jeong et al. 2002), and Rsv4 (Hayes et al. 2000) have been identified and characterized, and they can be utilized in marker-assisted selection.
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Footnotes |
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Corresponding Editor: Irwin Goldman
Received May 1, 2003
Accepted April 5, 2004
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References |
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