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CELL BIOLOGY & MOLECULAR GENETICS

Molecular Marker Mapping of RSV4, a Gene Conferring Resistance to all Known Strains of Soybean Mosaic Virus

^a Crop and Soil Environmental Sciences, Virginia Tech, Blacksburg, VA 24061-0404 USA
^b Medtronic Sofamor Danek, 1800 Pyramid Place, Memphis, TN 38132 USA

smaroof{at}vt.edu

	ABSTRACT

TOP ABSTRACT INTRODUCTION Materials and methods Results Discussion REFERENCES

 
Soybean mosaic virus (SMV) is a prevalent viral pathogen of soybean [Glycine max (L.) Merr.] wherever it is grown. Several genes that confer resistance in soybean to soybean mosaic virus have been identified. One of these resistance loci, Rsv4, confers resistance to all the known strain groups of SMV. This study was conducted to determine the map position of the Rsv4 locus in the soybean genome. A population of 255 F₂ individuals from the cross of the SMV resistant line LR2 (Rsv4) by the susceptible line Lee68 (rsv4) was evaluated in a mapping study. DNA from 12 to 15 F₂ individuals being either homozygous resistant or susceptible were pooled to produce bulk resistant and bulk susceptible DNA samples. Parents and bulks were screened with 101 AFLP primer pairs and two linked polymorphisms were identified. A putative linked marker, amplified by the primers Mse-AAA and Eco-AAG, was converted to a restriction fragment length polymorphism (RFLP) clone and a single polymorphic band was mapped 4.8 cM away from Rsv4. The same band was mapped in a second population containing 400 mapped loci and it was determined that this marker was located on the soybean D1b linkage group. Subsequent mapping in the original Rsv4 mapping population showed that the Rsv4 locus is flanked by the microsatellite markers, Satt542 at 4.7 cM and Satt558 at 7.8 cM.

Abbreviations: AFLP, amplified fragment length polymorphism • bp, base pair • BSA, bulk segregant analysis • cM, centimorgan • LL, population LR2 x Lee68 • VP, population V71-370 x PI407162 • R, resistant • RFLP, restriction fragment length polymorphism • S, susceptible • SMV, soybean mosaic virus

	INTRODUCTION

TOP ABSTRACT INTRODUCTION Materials and methods Results Discussion REFERENCES

 
THE MOST IMPORTANT viral disease of soybean worldwide is caused by the soybean mosaic virus (SMV). The occurrence of this disease has been reported wherever soybean is grown (Thottapilly and Rossel, 1987). Outbreaks of the disease, particularly in some regions of Asia, have been blamed for severe yield losses (Irwin and Goodman, 1981). The disease has been reported throughout the U.S. soybean production area (Pacumbaba et al., 1997; Ross, 1970). Incidence in the upper South has been blamed for significant yield reduction (Ren et al., 1997). Efforts to control the occurrence and spread of SMV revolve mainly around the development and utilization of cultivars possessing SMV resistance.

To date, SMV resistance has been reported from three distinct genetic loci, Rsv1, Rsv3, and an unnamed locus (here referred to as Rsv4). Rsv1 (Kiihl and Hartwig, 1979) is the resistance gene most commonly found in commercially available cultivars (Chen et al., 1994). Of the reported resistance alleles at this locus, none are effective against all SMV strains. Buzzell and Tu (1984) reported that the cultivar Raiden contained a resistance gene at a separate locus, Rsv2. Subsequent research (Wang et al., 1998; Buss et al., 1995) has shown that Raiden actually contains an Rsv1 allele. Another gene, Rsv3, from the cultivar Columbia produces a necrotic reaction to SMV (Buzzell and Tu, 1989). Finally, an SMV resistance locus was reported by Ma et al. (1995). This gene, referred to in this paper as Rsv4, confers resistance to all known strains of SMV. The Rsv4 allele reported by Ma et al. (1995) is derived from the line PI486355, which was shown to contain two resistance loci, one which is allelic to Rsv1 and another (Rsv4) which is not allelic at either the Rsv1 or Rsv3 locus. It is of interest to note that this resistance gene is completely dominant, in contrast to Rsv1 alleles which show systemic necrosis in the heterozygous state (Chen et al., 1994). The Rsv4 locus from PI486355 shows resistance without necrosis in both the heterozygous and homozygous states.

To date, only the Rsv1 locus has been mapped in the soybean genome. Yu et al. (1994) mapped the Rsv1 locus on the soybean molecular linkage group F, to a cluster of resistance genes flanked by the RFLP markers K644H and B212V. In order to map the Rsv4 locus, we used amplified fragment length polymorphism (AFLP) (Vos et al., 1995) and bulk segregant analysis (BSA) (Michelmore et al., 1991). AFLP is a PCR-based molecular marker that allows researchers to screen large numbers of loci in a short period of time. By combining AFLP with BSA, one can quickly identify markers closely linked to a gene of interest. In an F₂ population segregating for a known major gene of interest, bulk segregant analysis is the most effective way to identify a closely linked marker.

Numerous studies have been conducted using BSA and AFLP to map a gene of interest. Jong et al. (1997) mapped the Nb gene that confers resistance in potato (Solanum tuberosum L.) to potato virus X. They screened parents and bulks with 96 AFLP primer combinations to identify eight putatively linked markers. In a similar study, Bendahmane et al. (1997) used AFLPs to develop a high resolution map around the Rx1 locus for extreme resistance in potato to potato virus X. They screened a total of 728 primer pairs using BSA to identify 57 potentially linked markers.

In soybean, AFLP has proven to be a valuable marker for both mapping and population studies (Rector et al., 1999; Jin et al., 1998; Maughan et al., 1996b). Keim et al. (1997) have recently published an AFLP-based linkage map in soybean using 650 AFLP markers. The map consists of 28 linkage groups covering 3441 cM with a marker density of 1 per 4 cM.

In this study, we employed AFLP and BSA to determine the chromosomal location of the Rsv4 locus in the soybean linkage map.

	Materials and methods

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Plant Genetic Materials
Susceptible soybean cultivar Lee68 was crossed with the breeding line LR2 to produce an F₂ population of 255 individuals (hereafter referred to as the LL population). LR2 is a line containing the Rsv4 allele from PI486355. SMV data were collected on 15 to 20 F₃ plants from each of 255 F_2:3 lines (for details see Ma, 1995). This population was used for the fine mapping of the Rsv4 locus. A second mapping population of 149 F₂ individuals of the cross V71-370 x PI407162 [hereafter referred to as the VP population (Maughan et al., 1996a)] that contains over 400 mapped loci, was used as a reference population to assign Rsv4 to a previously defined linkage group. The VP population does not segregate for Rsv4.

Young trifoliolate leaves of 15 to 20 healthy, greenhouse-grown, F_2:3 plants were collected 2 to 3 wk after planting. DNA was isolated by freeze-drying followed by CTAB extraction as described (Saghai Maroof et al., 1984). On the basis of the F_2:3 disease data, DNA from 12 lines which are homozygous resistant (R) and 12 lines which are homozygous susceptible (S) was pooled to form bulk R and bulk S samples.

Marker Analysis
AFLP analysis was conducted according to Vos et al. (1995) and Maughan et al. (1996b). Bulk and parental DNA was digested with restriction enzymes EcoRI and MseI and ligated with specific adaptors. AFLP products were visualized either by means of a ³²P end-labeled Eco primer and running on a 7 M urea, 6% (w/v) polyacrylamide gel for 3 h at 45 W or by means of a fluorescently-labeled Eco primer which was then run on a 6 M urea, 4.5% polyacrylamide gel for 5 h at 1680 V. Fluorescently labeled products were visualized by the ABI 377 GeneScan system (Applied Biosystems, Foster City, CA).

AFLP bands of interest were converted to RFLP clones by excision of the polymorphic band from the polyacrylamide gel. Bands cut from the gel were eluted in 100 µL of water incubated in a boiling bath for 15 min (Upender et al., 1995). After elution, a small aliquot was used for PCR amplification of the excised DNA fragment. This PCR product was then cloned into the pCNTR shuttle vector using the General Contractor cloning kit from 5prime-3prime (Boulder, CO). Subsequent AFLP reactions were conducted on plasmid DNA, as described above, of putative positive clones. In this case, 50 ng of plasmid DNA template were used instead of genomic template. The fragments were then run alongside products resulting from an AFLP reaction of parental DNA on a 7 M urea, 6% polyacrylamide gel for 3 h at 45 W to tentatively confirm that the proper band was cloned.

The cloned PCR product was used as a probe for RFLP analysis essentially as previously described (Yu et al., 1994). Briefly, 8 µg of parental DNA was digested individually with enzymes DraI, EcoRI, EcoRV, HindIII, XbaI, and TaqI, according to the manufacturers protocols. Digested DNA was then separated on a 1% (w/v) agarose gel at 70 to 90 mA for 14 to 16 h. The DNA was transferred to Hybond nylon membrane (Amersham, Piscataway, NJ) by Southern blotting with 0.4 M NaOH buffer. Screening blots were hybridized with [³²P]dCTP, random primer labeled probe (Ambion, Austin, TX). Hybridizing bands were visualized by autoradiography on Kodak (New Haven, CT) Xomat film. Additional probes for RFLP screening and mapping were kindly provided by Randy Shoemaker (ISU/USDA/ARS).

In addition, SSR analysis was conducted essentially as described by Yu et al. (1994). Briefly, 50 ng of parental and F₂ DNA was used as template in a 20 µL of reaction containing 1x reaction buffer (10 mM Tris-HCL, 50 mM KCL, pH 8.3); 2.5 mM MgCl2; 2 µM of each primer; 50 µM each of dATP, dGTP, and dTTP; 1 µM of dCTP; 1 µM of ³²P-dCTP; and 1.0 unit of Taq polymerase. Thirty cycles of a standard PCR reaction were run with denaturation at 94°C for 30 s, primer annealing at 50°C for 30 s, and primer extension at 72°C for 60 s. Primers for SSR analysis were obtained from Research Genetics Inc. (Huntsville, AL) or custom made by Gibco-BRL Life Technologies (Rockville, MD). Primer sequences for SSR analysis were kindly provided by Perry Cregan (USDA/ARS).

Genetic map distances were calculated by the MAPMAKER 3.0 computer program (Lander et al., 1987). A LOD threshold of 3.0 was used to establish marker linkage.

	Results

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AFLP analysis of the parents of the LL population showed a very low level of polymorphism. A total of 101 primer combinations were screened with DNA from parents and bulks. A mean of 50 clearly distinguishable AFLP bands were detected per combination. Of these, only 141 total polymorphisms were detected between the parents among all primer combinations tested. This is equivalent to approximately 1.4 polymorphisms per AFLP reaction. Assuming a random distribution of AFLP markers, this equates to a genome coverage of roughly one polymorphic marker every 22 cM, as determined on the basis of an average predicted soybean genome size of approximately 3100 cM (Cregan et al., 1999; Keim et al., 1997). Of these 141 polymorphisms, two were determined to be linked to the Rsv4 gene by bulk segregant analysis. These linked polymorphisms, R4-1 and R4-2, were detected with the primer combinations Eco+AAA/Mse+AAT and Eco+AAA/Mse+AGG, respectively.

R4-1 is an easily distinguishable dominant band of 250 bp, that is absent in Lee68 and bulk S and present in LR2 and bulk R. R4-1 was excised by elution and cloned into the pCNTR shuttle vector by means of the General Contractor 5prime-3prime cloning kit. When used as a probe, the R4-1 clone hybridized to a single polymorphic band on a Southern blot containing parental and bulk DNA digested with the enzymes EcoRI and DraI. Both the LR2 parent and resistant bulk showed one size band while Lee68 and the susceptible bulk showed a different sized band. The clone was mapped in the LL population by means of the enzyme EcoRI and was found to be located 4.8 cM from the Rsv4 locus. Similarly the probe was mapped in the VP population with the enzyme DraI which showed an equivalent sized single-copy polymorphic band. Linkage analysis showed that the R4-1 probe maps to the soybean linkage group D1b [USDA/ARS/ISU map (Cregan et al., 1999)], 25.8 cM from the RFLP marker A605-1. Linkage of A605-1 to Rsv4 was then confirmed by mapping the probe in the LL population in order to verify that Rsv4 is located on the D1b linkage group. A605-1 was shown to be linked to Rsv4 at a distance of 26.3 cM in the LL population (Fig. 1) .

View larger version (7K): [in this window] [in a new window]   Fig. 1 Genetic map of the soybean D1b linkage group surrounding the soybean mosaic virus resistance gene, Rsv4. Markers were mapped in a 255 individual F2:3 population of the cross LR2 (Rsv4) x Lee68 (rsv4)

On the basis of the D1b linkage group information, several published RFLP and SSR markers (Cregan et al., 1999) were identified as likely candidates to be linked to Rsv4. Markers were screened and polymorphic loci including RFLP marker K19, B122, and A808 and SSRs Satt095, Satt157, Satt558, Satt542, and Satt266 were mapped in the LL population. Rsv4 was mapped to a region of D1b which is flanked by SSR markers Satt542 at 4.7 cM and Satt558 at 7.8 cM.

	Discussion

TOP ABSTRACT INTRODUCTION Materials and methods Results Discussion REFERENCES

 
Mapping of the Rsv4 locus was significantly expedited by the use of AFLP and bulk segregant analysis. This was particularly useful because of the low level of polymorphism observed in this particular population. Earlier studies have estimated the level of polymorphism detected by AFLP. Maughan et al. (1996b) observed 127 polymorphisms out of 759 bands detected in at least one of 12 G. max lines evaluated. In this particular study, we obtained 141 clear polymorphisms from approximately 5050 amplified fragments. This works out to an extremely low level of polymorphism of 2.7%. This low level of polymorphism is likely due to the fact that both LR2 and Lee68 are closely related to cv. Essex, such that their genomes are likely to be very homologous.

In this study, we were able to show that Rsv4 maps to the molecular linkage group D1b. Previous work has indicated that numerous disease resistance loci are clustered in various regions of the soybean genome. Rsv1, for instance, is located on the F linkage group, in a small genomic region where numerous genes for resistance to the pathogens including Phytophthora sojae (Rps3) (Diers et al., 1992), Pseudomonas syringae pv. glycinea (Rpg1) (Ashfield et al., 1998), and peanut mottle virus (Rpv1) (Roane et al., 1983) have been identified. Rsv4, by contrast, is located in a portion of the genome where few disease resistance loci have been reported. Recently, Rector et al. (1999) reported a QTL for resistance to corn earworm in a region near Rsv4 on the D1b linkage group. Interestingly, they also reported a similar QTL on the F linkage group near Rsv1.

Rsv4 is an important resistance gene both because it confers broad resistance to SMV and also because its mode of action, though not entirely understood, appears to be distinct from the hypersensitive-response type of disease resistance exhibited by Rsv1 alleles (Ma et al., 1995). Because of its unique resistance nature, there is interest in pyramiding this gene with other resistance loci such as Rsv1 and Rsv3 to incorporate multiple lines of defense against SMV infection. The ability to pyramid resistance genes into a single cultivar is greatly expedited by the use of closely linked molecular markers. Since genes such as Rsv4 and Rsv1 can mask one another's presence, selecting lines that contain both genes is not always possible by simple phenotypic methods. By using marker-assisted selection, gene pyramiding becomes a valuable alternative for introducing multiple disease resistance genes. The close linkage of flanking microsatellite Satt542 and AFLP R4-1 make these markers excellent candidates for this type of pyramiding approach. These markers are linked at 4.7 and 4.8 cM, respectively, with corresponding recombination frequencies of 3.5 and 3.0%.

In addition, there is tremendous interest in understanding how resistance genes are involved in defense response against invading pathogens. Numerous disease resistance genes have been cloned in the last 5 yr, and a large number of these genes share common nucleotide binding site (NBS) and leucine rich repeat (LRR) motifs (Baker et al., 1997). All of these NBS-LRR genes confer resistance by means of a hypersensitive response where-by localized cell death is triggered in response to pathogen ingress, in order to deter the spread of the pathogen. Rsv4 appears phenotypically to be distinct from this large class of resistance genes because it produces no necrotic or hypersensitive type reactions. Because of the unique nature of this gene, it would be of interest to clone it in order to better understand the mechanism controlling resistance. The first step toward cloning any gene of interest such as Rsv4 is to map its location within the genome.

The mapping of the Rsv4 locus has resulted in the identification of closely linked markers that will be useful in the marker-assisted selection of lines containing this gene. In addition, we have laid the groundwork leading toward the eventual cloning of this important gene. Future efforts will involve identifying more closely linked markers in order that physical mapping of the Rsv4 region can be conducted.

	ACKNOWLEDGMENTS

 
This study was supported in part by the U.S. Dept. of Agric., Natl. Research Initiative, Competitive Grants Program, Grant no. 96-35300-3648 and by the United Soybean Board. The authors wish to thank Randy Shoemaker and Perry Cregan for providing RFLP and SSR markers and for sharing the soybean integrated linkage map prior to publication.

Received for publication September 14, 1999.

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