The Journal of Heredity 2002:93(3)
© 2002 The American Genetic Association 93:179-184
Complementary Action of Two Independent Dominant Genes in Columbia Soybean for Resistance to Soybean Mosaic Virus
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 Polytechnic Institute and State University, Blacksburg, VA 24061.
Address correspondence to G. R. Buss at the address above or e-mail: gbuss{at}vt.edu.
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A stem-tip necrosis disease was observed in the soybean [Glycine max (L.) Merr.] cultivar Columbia and its derivative OX686 when infected with a necrosis-causing strain of Soybean mosaic virus (SMV) in Canada. A dominant gene named Rsv3 was found in OX686 for the necrotic reaction. In the present research we have found that Columbia is resistant to all known SMV strains G1–G7, except G4. Genetic studies were conducted to investigate the inheritance of resistance in Columbia and interactions of resistance gene(s) with SMV strains. Columbia was crossed with a susceptible cultivar, Lee 68, and with resistant lines PI96983, Ogden, and LR1, each possessing a resistance gene at the Rsv1 locus. F1 individuals, F2 populations, and F2:3 lines from these crosses were inoculated with G7 or G1 in the greenhouse. Our inheritance data confirmed the presence of two independent dominant genes for SMV resistance in Columbia. Results from allelism tests further demonstrate that the two genes (referred to as R3 and R4 in this article) in Columbia were independent of the Rsv1 locus. R3 appears to be the same gene previously reported as Rsv3 in OX686, which was derived from Columbia. The R3 gene confers resistance to G7, but necrosis to G1. The other gene, R4, conditions resistance to G1 and G7 at the early seedling stage and then a delayed mild mosaic reaction (late susceptible) 3 weeks later. Plants carrying both the R3 and R4 genes were completely resistant to both G1 and G7, indicating that the two genes interact in a complementary fashion. Plants heterozygous for R3 or R4 exhibited systemic necrosis or late susceptibility, suggesting that the resistance is allele dosage dependent. The R4 gene appeared epistatic to R3 since it masked expression of necrosis associated with the response of R3. The complementary interaction of two resistance genes, as exhibited in Columbia, can be useful in development of soybean cultivars with multiple and durable resistance to SMV.
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The mosaic disease of soybean, caused by Soybean mosaic virus (SMV), occurs wherever soybeans are grown, since the virus is often seed-borne and soybean germplasms are frequently exchanged worldwide. It is regarded as one of the most important crop diseases in many areas of the world (Bowers and Goodman 1979; Ross 1987; Sinclair and Backman 1989). The virus, which was once thought to be quite stable and uniform, has emerged as rather variable based on the differential responses of soybean cultivars to infection.
Cho and Goodman (1979, 1982) established a classification system for grouping various SMV isolates then available in the United States into seven strain groups (G1–G7), based on the differential reactions of a group of soybean cultivars having resistance to a common strain. In their classification scheme, G1 was the least virulent strain, since it infected the fewest cultivars, and G7 was the most virulent, infecting all the cultivars tested. Differentiation of SMV isolates using soybean cultivar reactions has also been reported in other countries, including Japan (Takahashi et al. 1980), China (Chen et al. 1986; Pu et al. 1982; Xu et al. 1986), Korea (Cho et al. 1977; Lee et al. 1992), and Brazil (Almeida 1981; Anjos et al. 1985), but seldom have either the same virus isolates or host genotypes been used in these studies.
The differential cultivars used in the United States have formed a foundation for genetic studies of SMV resistance in soybean. Resistance from most sources available in the United States has been shown to be controlled by single dominant genes (Chen et al. 1991, 1994; Kiihl and Hartwig 1979). Eight allelic dominant genes for SMV resistance have been identified at the most common locus, Rsv1: Rsv1 (PI96983), Rsv1-y (York), Rsv1-m (Marshall), Rsv1-t (Ogden), Rsv1-k (Kwanggyo), Rsv1-s (PI486355), Rsv1-r (Raiden), and Rsv1-h (Suweon 97) (Chen et al. 1991, 1994, 2002; Ma et al. 1995b).
There are several reports of different genes for SMV resistance at loci other than Rsv1. The breeding line OX670 was reported by Buzzell and Tu (1984) to contain a resistance gene, Rsv2, which was assumed to be derived from the Raiden cultivar, one of the ancestors of OX670. However, the Raiden gene was later proven to be allelic to the Rsv1 locus and assigned a new gene symbol, Rsv1-r (Chen et al. 2001). The breeding line OX686, derived from Columbia, was described as having a single dominant gene that conferred stem-tip necrosis to G1 and G4 (Buzzell and Tu 1989; Tu and Buzzell 1987). Since this gene was shown to be independent of Rsv1 and Rsv2, it was assigned the gene symbol Rsv3 (Buzzell and Tu 1989). Shigemori (1988) found that soybean cultivars Tousan 140, Hourei, and Suzuyataka each carry a single gene for resistance to the C strain of SMV in Japan. The resistance gene in Tousan 140 was shown to be independent of the resistance genes (allelic) in Hourei and Suzuyataka. Bowers et al. (1992) reported that Buffalo and HLS carry single dominant genes for SMV resistance at different loci, but no allelism tests were conducted with other reported loci.
Two independent dominant genes were identified in PI486355, one of which is at the Rsv1 locus and has been isolated in LR1 soybean (Chen et al. 1993; Ma et al. 1995a,b). The other resistance gene from PI486355 was isolated in the soybean line LR2 (later named V94-5152; Buss et al. 1997) and found to be independent of Rsv1 (Ma and Buss 1995). This gene was also proven to be independent of a gene in L29 (a soybean line with a resistance gene derived from Hardee), which also is not at the Rsv1 locus (Ma and Buss 1995). The L29 gene was later demonstrated to be an allele at the Rsv3 locus (Buss et al. 1999). This gene provides resistance to more virulent strains (G5–G7) but is susceptible to G1–G4.
Most of the Rsv1 genes studied to date confer resistance to lower-numbered strains of SMV and susceptible or necrotic reaction to higher-numbered strains. On the other hand, genes at the Rsv3 locus condition resistance to higher-numbered strains, but necrotic or susceptible response to lower-numbered strains. Although some of the genes identified so far confer relatively broad resistance, reliance on a single locus will result in genetic uniformity and potential vulnerability. Columbia soybean is resistant to all known SMV strains except G4 and therefore may serve as valuable source of SMV resistance. The objectives of this study were to investigate the inheritance of SMV resistance in Columbia, to test the allelism of resistance genes in Columbia with other known genes, and to examine the interactions of resistance genes in Columbia with SMV strains.
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Seeds of Columbia soybean were provided by Dr. R. I. Buzzell (Agriculture and Agri-Food Canada). The soybean line LR1 was derived from the cross between Essex and PI 486355 in our breeding program (Ma et al. 1995b). Other differential cultivars used in the study were also from our germplasm collections for SMV research.
The sources of SMV strains, maintenance of virus cultures, inoculation procedures, and greenhouse conditions were as described previously (Chen et al. 1991, 1994; Ma et al. 1995b). Columbia was tested with G1–G7 to confirm its reaction to differential SMV strains. Progenies from all crosses were inoculated with G1 or G7, as appropriate, to examine genetic segregations. The differential cultivars York, Marshall, Ogden, Kwanggyo, and PI96983 were also included in each set of inoculations to confirm the identity and purity of the virus strains.
For genetic studies, Columbia was crossed with susceptible cultivar Lee 68 to determine the number of gene loci conditioning SMV resistance. For allelism tests, Columbia was crossed with resistant lines PI 96983, Ogden, and LR1, which possess the resistance genes Rsv1, Rsv1-t, and Rsv1-s, respectively (Chen et al. 1991; Ma et al. 1995b). Rsv1 and Rsv1-t each confer resistance to G1 but systemic necrosis to G7 (Chen et al. 1991, 1994). Rsv1-s conditions resistance to both G1 and G7 (Ma et al. 1995b).
F1 individuals and F2 populations were screened for SMV reactions in the greenhouse. To confirm the genetic segregation in the F2 generation, a minimum of 20 plants from each F2:3 progeny were tested with each virus strain. Individual plant reactions were examined visually and classified as described below until at least 4 weeks after inoculation.
Responses were initially classified into three categories: resistant (R), systemic necrosis (N), and susceptible (S). Plants classed as resistant showed no localized symptoms on inoculated leaves or systemic symptoms on subsequent leaves. Plants classed as systemic necrotic initially developed necrotic lesions 3–5 mm in diameter on inoculated leaves 4–6 days after inoculation, with necrosis spreading into the veins. The virus then moved rapidly into the vascular system, causing chlorotic vein clearing and spotting on the first trifoliolate leaves within 6–8 days. Necrosis of small veins in the leaf lamina of noninoculated trifoliolate leaves followed within 2–3 days, together with extensive midrib, petiole, and stem necrosis. No more than two to three trifoliolate leaves developed prior to stem-tip necrosis, followed by subsequent plant death. Susceptible plants exhibited typical mosaic symptoms on the first trifoliolate leaves as they emerged and expanded 7–10 days after inoculation. Then the virus and mosaic symptoms move and spread to new leaves as they develop.
In addition to the above three distinctive reaction classes, two other phenotypes were recognized in the progenies of crosses with Columbia: resistant with local necrotic lesions and late susceptible. The resistant plants with necrotic lesions (RNL) developed localized necrotic spots, 4–6 mm in diameter, on inoculated leaves within 1 week or so after inoculation, with no systemic symptoms nor detection of virus in noninoculated leaves. Some RNL plants showed yellow spots on mature, noninoculated lower leaves, but not on newly developed leaves on the upper parts of plants. Some RNL plants also had slightly distorted leaves. The late susceptible (LS) plants developed delayed mild mosaic symptoms, which differ from typical early susceptible symptoms both in appearance and timing. Late susceptible plants were symptomless until 3 or more weeks after inoculation, when large sectors of chlorotic mosaic began to appear on upper developing leaflets of the third or later trifoliolate leaves. In contrast, typical early susceptible plants developed local chlorotic lesions on inoculated leaves and transient vein clearing in the first trifoliolate leaves within 5–7 days of inoculation, followed by development of a fine light green/dark green mosaic, often with rugosity and leaf curling, on second trifoliolate and later-developing leaves.
The presence or absence of SMV in plants with questionable symptoms, including many of the late susceptible plants, was confirmed by leaf tissue immunoblot assays (Gera 1994; Srinivasan and Tolin 1992). Leaf samples were taken from plants with atypical SMV symptoms or suspicious infections and pressed onto a nitrocellulose paper. Antigens in tissue blots were detected by enzyme-labeled immunologic probes. Purple color of tissue blots on the nitrocellulose paper indicates the presence of SMV in the leaf tissue and SMV-negative blots remain colorless. Multiple healthy and susceptible samples were also included as negative and positive checks, respectively, on the same blotted nitrocellulose membrane for the immunoblot assay. S and LS plants always showed a strong positive reaction and R plants were negative. N and RNL plants typically produced a weak positive result. This, as well as our previous experience (Chen et al. 1991), provides confidence that visual symptoms are accurate indicators of the presence of SMV. Virus recovered from S and LS plants retained the characteristics of the pathotype inoculated when inoculated back to the differential cultivars. The F2:3 lines were classified as all R, all N, all S, all RNL, all LS, or segregating. The segregating families were further classified as 3:1 or 15:1 segregations based on chi-square tests. In the chi-square tests for goodness-of-fit to expected genetic ratios, two or more of the non-S classes of plants in the F2 populations and segregating F3 rows were combined, as appropriate, depending on the assumed gene combinations in the individual genotypes and the population size. S plants were always treated as a separate class.
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After inoculation with G1, G2, G3, G5, G6, and G7 in the greenhouse, Columbia showed complete resistance. No localized necrotic spots were observed on the inoculated leaves, nor were systemic symptoms seen on upper leaves of the inoculated plants. However, G4 inoculation induced localized necrotic spots on inoculated leaves and on trifoliolate leaves 2–3 weeks after inoculation, and eventual stem-tip necrosis.
When inoculated with G7, the F1 plants from Columbia (R) x Lee 68 (S) were all resistant and the F2 population showed a two-gene segregation that fit a 15 (R + LS + N):1 S ratio (Table 1). Evidently the segregants with necrotic and late susceptible phenotypes resulted from the interactions of the two genes, which will be further discussed in the hypothetical genetic model later in the text. The F2:3 progenies from the same cross also showed a two-gene segregation pattern (Table 2), which includes 4 (all R):2 (R + RNL):1 (all RNL):4 [15 (R + LS + N):1 S]:2 [3 (R + LS):1 S]:2 [3(RNL + N):1 S]:1 (all S). If we focus on the segregation of susceptible plants in the F3 progenies, we find that the observed overall segregation would well fit the ratio of 7 (all R):8 segregating:1 (all S) (
2 = 1.796, P = .25–.5), which confirms the presence of two genes in Columbia.
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Three different types of resistant F2:3 families were observed in the Columbia x Lee 68 cross with G7 inoculation: all plants resistant (all R), all plants with localized necrotic lesions (all RNL), or a mixture of resistant and necrotic-lesion plants (R + RNL) in the same progeny (Table 2). No F2:3 progeny were homogeneously systemic necrotic or late susceptible, suggesting that the responses of systemic necrosis and late susceptibility are the expression of heterozygous genotypes in this cross. In the progenies that appeared to segregate for single genes, some (2/16) had late susceptible plants but no necrotic plants [3 (R + LS):1 S] and others (2/16) had necrotic plants but no late susceptible plants [3 (RNL + N):1 S]. In the former type of 3:1 segregating progenies, resistant plants were all symptomless (R), while in the latter type of 3:1 segregating progenies, resistant plants all had local necrotic lesions (RNL). The presence or absence and the ratio of the necrotic or late susceptible phenotypes apparently depend on the combination and the state of the two genes in Columbia, which will be further analyzed in the proposed genetic model.
When inoculated with G1, the F2:3 progenies from Columbia x Lee 68 also showed a two-gene segregation, but with different patterns from those observed with G7 (Table 2). The overall segregation exhibited a good fit to a ratio of 1 (all R):1 [all LS or (R + LS)]:1 (all N):2 {3 [LS or (R + LS)]:1 S}:2 (3 N:1 S):1 (all S):8 two-gene segregating classes. The two-gene segregating progenies containing predominantly R and LS plants with no or 1/16 S plants could not be distinguished readily with accuracy because of the complexity of segregation and relatively small sample size. The fact that 1/16 of the F3 lines were homogeneous susceptible (all S) and 4/16 of the F3 lines were segregating 3:1 (3 LS:1 S or 3 N:1 S) provided convincing evidence for the presence of two genes in Columbia. The presence of F2:3 progenies that were homogeneously late susceptible (all LS) or homogeneously systemic necrotic (all N) indicated that the late susceptibility and systemic necrosis to G1 could be conferred by homozygous genotypes. Late susceptible symptoms may not show up uniformly, even within the same F2:3 progeny. Some plants developed LS symptoms 3 weeks after inoculation and others did not show symptoms even 4–5 weeks after inoculation when the final visual score was made in the greenhouse. Thus a few progenies showing LS + R (majority of plants with LS and a few R plants mixed in the same progeny) were classified as all LS for genetic analysis. F2:3 progenies with 3 [LS or (R + LS)]:1 S and 3 N:1 S phenotypes were apparently segregating for single genes which appeared to be different from each other.
It is also interesting to compare the reactions of the F2:3 progenies from Columbia x Lee 68 to G1 and G7. Of 131 progenies tested, 8 were late susceptible [all LS or (R + LS)] to G1, but resistant (all R) to G7 (Table 2). All eight progenies that were systemic necrotic (all N) to G1 were resistant with localized necrotic lesions on the inoculated leaves (all RNL) to G7. Similarly 20 F2:3 progenies that showed a 3 N:1 S segregation to G1 all segregated 3 (RNL + N):1 S to G7; 16 F2:3 progenies segregating for 3 [LS or (R + LS)]:1 S to G1 all showed a 3 (R + LS):1 S segregation to G7; and the same five F2:3 progenies that were susceptible (all S) to G1 were also susceptible to G7. Progenies with a 15 (R + LS + N):1 S segregation ratio to G7 all segregated in a two-gene fashion to G1. A portion of the progenies (11) that were resistant (all R) to G7 had some late susceptible and late systemic necrotic plants with G1 inoculation. Of 29 F2:3 progenies that were resistant (all R) to G7, only 10 were resistant (all R) to G1. All these observed discrepancies in response to G1 and G7 are due to interactions of the two genes in Columbia and the two SMV strains, which can be interpreted with a genetic model.
The genetic model explaining segregation patterns and the two gene interactions in the Columbia x Lee 68 cross is given in Table 3. The two resistance genes in Columbia are temporarily referred to as R3 and R4. The presence of both R3 and R4 genes would give rise to resistance to both G1 and G7, while plants lacking both genes (r3r3 r4r4) would be susceptible to both strains. The R3 gene alone (R3R3 r4r4) confers resistance to G7 with localized necrotic spots on the inoculated leaves (RNL) but systemic necrosis to G1. Plants with this gene combination (R3R3 r4r4) would produce homozygous and homogeneous progenies that are all RNL to G7 and all N to G1. Individuals with the homozygous R3 gene and heterozygous R4 gene (R3R3 R4r4) would be resistant to G7 and G1, but would produce progenies segregating for resistance and necrosis (R + RNL for G7 and R + N for G1) due to the segregation of the R4 gene. The heterozygotes of the R3 gene in the absence of the R4 gene (R3r3 r4r4) usually express the necrotic phenotype (RNL or N) and would produce progenies segregating for susceptibility (3 RNL/N:1 S) in response to G7 and G1. Such an association of genotypic heterozygosity and phenotypic necrosis has been previously observed with Rsv1 genes (Buss et al. 1989; Chen et al. 1991; Ma et al. 1995b).
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The R4 gene confers symptomless resistance (R) to G1 in its homozygous state (r3r3 R4R4) for about 3 weeks after inoculation with G1. Then the inoculated plants start to show susceptible symptoms, which differ from typical mosaic symptoms in timing and appearance, as described earlier. In contrast, the same genotype (r3r3 R4R4) and all of its progenies would be completely resistant when inoculated with G7. Although the R4 gene provides complete resistance to G7 in its homozygous state, some of the presumed heterozygotes (r3r3 R4r4) were late susceptible rather than resistant. It appears that there is an association between heterozygosity and late susceptibility to G7 and that the expression of the late susceptibility of such heterozygotes seems to be incomplete, even when the final scoring was done 4–5 weeks after inoculation. Plants with the r3r3 R4r4 genotype would produce progenies exhibiting a 3 (R + LS):1 S segregation to G7 and 3 [LS or (R + LS)]:1 S to G1. Double heterozygotes (R3r3 R4r4), such as the F1 plants and F2 plants from Columbia x Lee 68, exhibited resistant reactions (Tables 1 and 3) to G7. However, the F1 plants showed an atypical, systemic necrosis at a late stage and did not survive after inoculation with G1. The double heterozygotes tended to segregate in a rather complicated fashion with the presence of an assortment of phenotypes including resistant, local necrosis, systemic necrosis, late susceptible, and regular susceptible. However, the overall ratio appears to fit two-gene segregation, with 1/16 of the population being susceptible.
It is worth noting that the F2:3 progenies presumed to be homozygous for both R3 and R4 genes (R3R3 R4R4) were completely resistant to G1, whereas R3 alone confers necrotic reaction and R4 alone conditions late susceptible reaction to G1. These observations suggest that a complementary interaction between the R3 gene for systemic necrosis and the R4 gene for late susceptibility (early resistance) results in total resistance. For G7, the R4 gene confers symptomless resistance (R) and is epistatic to the R3 gene, masking its expression of necrosis (expected in individuals with R3_ r4r4 genotypes). Therefore R3_ R4_ genotypes, including the double heterozygote, always show symptomless resistance rather than necrosis to G7 (Tables 2 and 3). The LS reaction of some plants presumed to have the r3r3 R4r4 genotype and the N reaction of plants that were assumed to be the R3r3 r4r4 genotype provide further indications that the complementary effect between the two genes enhances total resistance.
Table 4 contains data for allelism tests of the two resistance genes in Columbia with Rsv1. When inoculated with G7, the F1 plants from the N x R cross of Ogden x Columbia were resistant and the F2 population showed a three-gene segregation with a good fit to a ratio of 63 (R + LS + N):1 S. Similar results were obtained from the F2 populations from the N x R cross of PI96983 x Columbia and the R x R cross of LR1 x Columbia. No late susceptible plants were scored in these two populations, perhaps because the populations were not large enough or the final scoring was done before the late susceptible symptoms appeared. The presence of typical susceptible segregants in the progenies of these N x R and R x R crosses indicates that neither of the two resistance genes in Columbia is allelic to the Rsv1 alleles in Ogden, PI96983, and LR1. If one of the genes in Columbia were an allele at the Rsv1 locus, then the N x R cross would segregate for N and R only (not S) and the R x R cross would not segregate at all. The susceptible plants were assumed to be the segregants with triple recessive genotypes (rsv1rsv1 r3r3 r4r4). The F1 plants from Ogden x Columbia were resistant rather than necrotic, which suggests that one of the genes in Columbia, logically the R4 gene, is epistatic to the Rsv1-t gene in Ogden and thus masks the expression of systemic necrosis associated with Rsv1-t.
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The F2:3 progenies from PI96983 x Columbia and Ogden x Columbia also showed a three-gene segregation pattern in response to G7 (Table 5). Of a total of 211 F2:3 progenies from the two crosses, only four were homogeneously susceptible, which fits very well to the expected frequency of 1/64. Five F2:3 progenies were homogeneously systemic necrotic, which are expected to be derived from the Rsv1Rsv1 r3r3 r4r4 F2 plants with a frequency of 1/64. Three different types of F2:3 progenies that appeared to segregate for single genes (Rsv1, R3, and R4) were each observed with the expected frequency of 2/64. In analyzing the progenies segregating for single genes using the proposed genetic model, we assumed that the 3 N:1 S progenies are derived from the heterozygote of the Rsv1 gene (Rsv1rsv1 r3r3 r4r4), the 3 (R + LS):1 S progenies result from the segregation of the R4 gene (rsv1rsv1 r3r3 R4r4), and the 3 (RNL + N):1 S progenies are from the rsv1rsv1 R3r3 r4r4 genotype. All three types of 3:1 segregating progenies occurred in a frequency of 2/64, as anticipated. The homogeneous N progenies were expected to be the Ogden genotype in the absence of the R3 and R4 gene in Columbia (Rsv1-tRsv1-t r3r3 r4r4) with a frequency of 1/64. For chi-square tests, progenies with two-gene or three-gene segregations were combined with all resistant progenies because they could not be statistically distinguished from each other due to the limited population size for each F2:3 progeny. The overall segregation of F2:3 progenies from the two N x R crosses fit the expected ratio of 1 (all S):1 (all N):2 (3 N:1 S):2 [3 (R + LS):1 S]:2 [3 (RNL + N):1 S]:56 (all R, two-gene or three-gene segregations). The presence of 1/64 all S progenies convincingly demonstrated that there are three genes segregating in the N (Rsv1) x Columbia (R3 R4) crosses. These results confirm that neither of the two resistance genes in Columbia is allelic to Rsv1.
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The late susceptible reaction to SMV in soybean has not been reported previously. It is a unique reaction associated with resistance genes in response to certain SMV strains. Plants of this kind display early resistance and then develop delayed mild mosaic symptoms. In addition to the three established types of soybean reactions (R, N, and S) to SMV strains (Cho and Goodman 1979, 1982), the late susceptible reaction can be used in the classification system to differentiate SMV strains and soybean genotypes with specific resistance genes. In future genetic studies, caution needs to be exercised to maintain plants in the greenhouse long enough after inoculation so that this reaction can be distinguished from total resistance. Field scoring of SMV reactions should be done more than once to confirm the phenotypes in the late season. The genes conferring late susceptibility may have practical value: (1) they may provide more durable resistance in combination with resistance genes at other loci; (2) deployment of cultivars carrying such genes may delay epidemics of the virus and at the same time not exert high selection pressure on the virus, thus limiting the buildup of new, more virulent strains; and (3) yield losses and seed transmission of the virus associated with delayed SMV infection are significantly less than those caused by early infection (Bowers and Goodman 1979; Ross 1987).
The R4 gene identified in Columbia will provide new genetic material for studying the mechanisms of SMV resistance. Late susceptibility to G1 appears to result from either delaying the long-distance movement of the virus or inhibiting overall virus replication even after the virus has moved systemically. It also is interesting to see that the heterozygotes of the R4 gene (in absence of other genes) are late susceptible but homozygotes are resistant to G7 (Table 3), indicating a gene-dosage effect. Allele-dosage effects of virus resistance genes have been well documented (Fraser 1990, 1994). The observation that heterozygotes of allele-dosage-dependent genes usually show systemic necrosis (Fraser 1990) has been reported previously with the Rsv1 alleles in soybean (Chen et al. 1991, 1994; Ma et al. 1995b).
G1 induces systemic necrosis in lines with the R3 gene and late susceptibility in those with the R4 gene. It appears to be more virulent against these two genes than G7, to which both genes confer a level of resistance. The necrotic reaction of the R3 gene from Columbia to G1 in this study appears to be similar to the stem-tip necrosis to G1 conferred by Rsv3 in OX686 (Buzzell and Tu 1989; Tu and Buzzell 1987). OX686 is a breeding line derived from the soybean cross of Columbia and Harosoy, which is susceptible to SMV (Buzzell and Tu 1989). Apparently OX686 inherited only one of the two genes from Columbia. Based on the necrotic reaction to G1, it is logical to assume that the R3 gene described here in Columbia is the same gene as Rsv3 reported in OX686. The R4 gene in Columbia confers resistance to G7 and late susceptibility (early resistance) to G1. This gene resides at a locus independent of Rsv1 and Rsv3. Research is under way to separate the R3 and R4 genes into breeding lines for further allelism tests.
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Acknowledgments |
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This research was supported in part by a grant from the Virginia Soybean Board.
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Corresponding Editor: Prem Jauhar
Received September 14, 2001
Accepted March 29, 2002
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