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Crop Science 43:101-105 (2003)
© 2003 Crop Science Society of America

CROP BREEDING, GENETICS & CYTOLOGY

Rps8, A New Locus in Soybean for Resistance to Phytophthora sojae

K. D. Burnham, A. E. Dorrance*, D. M. Francis, R. J. Fioritto and S. K. St. Martin

Dep. of Plant Pathology, The Ohio State University, Wooster, OH 44691-4096

* Corresponding author (dorrance.1{at}osu.edu)


   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Phytophthora root and stem rot caused by Phytophthora sojae M.J. Kaufmann & J.W. Gerdemann (=Phytophthora megasperma Drechs. f. sp. glycinea T. Kuan & D.C. Erwin) is the second leading cause of yield loss in soybean [Glycine max (L.) Merr.] in the USA. Currently, seven loci for resistance with 13 alleles have been identified in soybean. Populations of P. sojae exist in many soybean production regions that cause disease on plants with many, if not all, of these genes. Consequently, the need for new resistance loci is great. A number of plant introductions (PIs) from South Korea were identified in an earlier study that may contain novel resistance loci. The objectives of this project were to identify the allele(s) for resistance to P. sojae present in PI399073 and to map these allele(s) to a linkage group. PI399073 was crossed with ‘Williams’ and ‘S 19-90’ to develop populations. These populations were assayed for disease resistance, single sequence repeats (SSR), restriction fragment length polymorphisms (RFLP), and isozyme markers. A new Phytophthora resistance locus, Rps8, was mapped to MLG (major linkage group) A2 in two different crosses with PI399073. This is the first locus for Phytophthora resistance that has been identified on MLG A2.

Abbreviations: SSR, simple sequence repeat • MAS, marker assisted selection • RFLP, restriction fragment length polymorphisms • MLG, major linkage group


   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
PHYTOPHTHORA ROOT AND STEM ROT is a devastating disease of soybean that occurs throughout the USA and the world (Wrather et al., 2001). Yield losses in 1998 due to Phytophthora root and stem rot in top soybean producing countries were 1149 and 92 thousand megagrams in the USA and Argentina, respectively (Wrather et al., 2001). Suhovecky and Schmitthenner (1955) first described this disease of soybeans in Ohio and shortly thereafter it was described in Indiana and North Carolina. The pathogen is now referred to as Phytophthora sojae Kaufmann & Gerdemann (syn. Phytophthora megasperma Drecsh f. sp. glycinea Kuan & Erwin).

Bernard et al. (1957) identified the first soybean gene (Rps or Rps1) for resistance to this pathogen. To date, 13 resistance (Rps) alleles at seven loci have been described: Rps1 (Bernard et al., 1957), Rps2 (Kilen et al., 1974), Rps3 (Mueller et al., 1978), Rps4 (Athow et al., 1980), Rps5 (Buzzell and Anderson, 1981), Rps6 (Athow and Laviolette, 1982), and Rps7 (Anderson and Buzzell, 1992). Single allele resistance has provided adequate disease management; however, each single allele deployed in a soybean cultivar is only effective for 8 to 15 yr (Schmitthenner, 1985). Pathotypes of P. sojae have already been found in fields throughout the Midwest with cultivars containing virulence genes to Rps1k, the most recently deployed Rps allele (Abney et al., 1997; Kaitany et al., 2001; Kurle and ElAraby, 2001; Leitz et al., 2000; Schmitthenner et al., 1994; Yang et al., 1996). Consequently, novel resistance loci or alleles need to be identified and incorporated into soybean cultivars to protect against yield losses.

Soybean PIs from South Korea may serve as potential new sources of resistance loci (Dorrance and Schmitthenner, 2000). Resistant PIs were identified by inoculating seedlings with a series of P. sojae isolates that attacked all of the known Rps alleles as well as combinations of alleles. Germplasm from South Korea has previously been the source of other Rps alleles. One of the many sources of Rps3a, PI86972-1, was from South Korea (Mueller et al., 1978). PI157409, with the gene combination Rps1b and Rps4, was also collected in South Korea (Layton et al., 1984). The objectives of this study were (i) identify the number of Rps genes in PI399073 and (ii) to map the gene(s) to a linkage group on the soybean genome map.


   MATERIALS AND METHODS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
The plant introduction and Williams were obtained from the USDA Soybean Germplasm Collection at Urbana, IL, and S 19-90 was purchased from a Dekalb licensed dealer. This plant material was maintained in the Ohio Agricultural Research Development Center (OARDC) soybean breeding program. The crosses used for mapping the new allele were Williams (rps) x PI399073 and S 19-90 (Rps1c) x PI399073. The F1 plants from these crosses were selfed to produce populations of approximately 40 to 60 F2 plants for each cross. The F2 plants were then selfed and each plant was threshed individually to yield seed for F2:3 families.

Phytophthora Resistance Tests
Isolates of P. sojae pathotypes were maintained at the Department of Plant Pathology, OARDC. All isolates used in this study were collected in Ohio. Three isolates of P. sojae were used in this study with the following pathotypes OH1 (vir 7), OH17 (vir 1b, 1d, 3a, 3b, 3c, 4, 5, 6, 7), and OH25 (vir 1a, 1b, 1c, 1k, 7). Differential checks, Williams (universal suscept); ‘Harlon’ (Rps1a), ‘Harosoy 13XX’ (Rps1b), ‘Williams 79’ (Rps1c); PI103091 (Rps1d); ‘Williams 82’ (Rps1k); L76-1988 (Rps2); L83-570 (Rps3); PRX 146-36 (Rps3b); PRX 145-48 (Rps3c); L85-2352 (Rps4); L85-3059 (Rps5); and ‘Harosoy 62XX’ (Rps6) and ‘Harosoy’ (Rps7), were included in all tests to ensure that the P. sojae isolate used elicited the appropriate reaction.

Ten individual F3 seedlings per F2: 3 family were inoculated in the laboratory by means of a modification of the hypocotyl inoculation technique. Inoculum was prepared by growing the P. sojae isolates for 1 wk on lima bean (Phaseolus lunatus L.) agar (50 g lima beans, 12 g agar per liter). Seeds were placed between germination papers wetted with water, rolled up, and stored in the dark in plastic containers. The plastic containers had wire mesh in the bottom to allow for water to drain from the papers. After 1 wk of growth, papers were unrolled and the seedlings were inoculated with a hypodermic syringe. The syringe was filled with colonized agar from a plate of P. sojae, and then the agar was forced through the syringe to create a slurry. The slurry was placed back into the syringe. Seedlings were inoculated by scratching the hypocotyl with the needle of the hypodermic syringe and placing the agar–mycelium mixture onto the wound. Following inoculation plants were rolled again and placed back into plastic containers as before. Seven days after inoculation the seedlings were scored for resistance reactions. Reactions were recorded as R (resistant; seedlings alive) or S (susceptible, seedlings dead with brown hypocotyls) after 10 d. Each F2:3 family had 10 plants scored, either all R, all S, or a combination of both. The 10 scores were used to develop a single classification, R, S, or H (heterozygous), for each F2 plant from which an F2:3 was derived.

Genetic Analysis
Leaves from 10 individual F3 seedlings were bulked from each F2:3 family, and DNA was extracted according to the protocol previously described (Burnham et al., 2002). The number of seedlings used was determined by

where p = probability of recovering one susceptible plant, and q = probability of occurrence of susceptibility (Sedcole, 1977). The use of 10 seedlings allows between 94 and 95% probability of recovering one susceptible seedling.

Fifty-five SSR primer pairs (Research Genetics Inc., Huntsville, AL) were evaluated for polymorphisms between the parents in the Williams x PI399073. The polymorphic SSR markers were then used to test the F2:3 progeny. PCR reactions were performed as recommended by the manufacturers in a total of 25 µL containing 30 ng of genomic DNA. Amplified PCR products were resolved on 5% (w/v) high-resolution agarose gels (Amresco, Solon, OH) and stained with ethidium bromide for visualization of the DNA products. Reactions were scored as 1 (homozygous for PI parent allele), 2 (homozygous for susceptible parent allele), or 3 (heterozygous).

Fresh leaf tissue was used to detect the presence of the isozymes acid phosphatase (Ap) (E.C. 3.1.3.2) and leucine aminopeptidase (Lap) (E.C. 3.4.11.1) (Hebert and Beaton, 1993, p. 31). Leaves from each F2:3 family were collected, placed on ice, and then placed in grinding buffer [10 mL 0.1M Tris-HCL pH 8.0, 0.5 mL ß-mercaptoethanol, 50 mg PVP (polyvinylpolypyrrolidone)]. Samples were ground immediately before loading on cellulose acetate membrane. Electrophoresis was carried out at 200 V for 20 min in CAAPM running buffer [8.4 g citric acid, 10 mL 4-(3-aminopropyl) morpholine per liter].

The stain for Ap contained 3 mL of acetate ACP acetate buffer (2.43 g sodium acetate trihydrate, 4.7 mL glacial acetic acid, 5.0 mL 1.0 M MgCl2 per liter), 4 mg {alpha} napthyl acid phosphate, 3.2 mg of fast garnet GBC salt, and 2 mL of 2% (w/v) agarose. The stain for Lap contained 2 mL 0.1 M Tris maleate, 1 mg L-leucine ß naphthylamide HCl, 1 mg fast black K salt, and 2 mL of 2% (w/v) agarose. Isozyme bands were scored as described for SSR markers as 1, 2, or 3.

DNA from F2:3 families used in RFLP marker analysis was isolated using the same methods as described for SSR marker analysis. DNA samples were digested with restriction enzymes (EcoRV, HindIII, and HaeII) (Promega, Madison, WI). DNA fragments were separated on 0.8% (w/v)agarose gels and stained with ethidium bromide for visualization of the DNA products. DNA was transferred to nylon membrane (Bio-Rad, Hercules, CA) by the procedure described by Sambrook et al. (1989). DNA was UV cross linked to the nylon membrane at a setting of 1200 J with a Stratalinker (Stratagene, La Jolla, CA).

DNA probes were prepared by amplifying insert DNA from the Bng clones (Vallejos et al., 1992). The inserts were then labeled with 32P with the Ambion Deca-Prime kit following instructions from the manufacturer (Ambion, Inc., Austin, TX). Hybridizations were carried out at 55°C for 2 h in roller tubes and Quik-Hyb solution containing 100 ng/mL of Salmon sperm (Stratagene, La Jolla, CA). Following hybridization the blots were washed twice in 2x SSC/0.1% (w/v) SDS (1x SSC is 0.15 M NaCl plus 0.015 M sodium citrate) for 15 min at room temperature followed by a final wash with 0.1x SSC/0.1% SDS for 30 min at 50°C. Blots were then exposed to phosphoimaging screens for 2 d and visualized on a Molecular Dynamics phosphoimager (Amersham Biosciences, Sunnyvale, CA). F2:3 families were scored as 1, 2, or 3 in a manner similar to the scoring for SSR markers. The same procedures were followed for the S19-90 x PI399073 population with one exception. SSR markers, isozymes, and RFLP probes were evaluated on the F2:3 families that were linked to the resistance loci in the Williams x PI399073 population.

Linkage Analysis
Two approaches were used to map loci affecting resistance relative to molecular markers. First, a qualitative approach was used to determine if the resistance involved multiple resistance loci. Scoring 10 F2:3 individuals would provide sufficient numbers to identify segregating lines with high confidence in the event that resistance was controlled by more than one locus. Second, on the basis of the preliminary identification of a single locus, quantitative models were applied to test the robustness of a single locus model because mapping populations were small (39 and 54 F2:3 families). For this approach, each family was given a phenotypic score that represented the proportion of resistant seedlings out of 10 seedlings inoculated. For example, 0.5 would indicate that five seedlings were resistant and five seedlings were susceptible from that F2:3 family.

Chi-square analyses were performed on the phenotypic data to test if a 3:1 resistant to susceptible ratio was present in the F2 lines. F2 plants were scored as R, S, or H on the basis of the results of the hypocotyl inoculation of the F2:3 families. For this analysis, all R and H scores were grouped together. Chi-square analysis was also used for each DNA marker to test whether the F2:3 families fit the expected 1:2:1 ratio. DNA marker data that fit the expected ratio were then used in an ANOVA to determine if the marker data were significantly associated with resistance. All 10 F3 scores were used in an ANOVA. ANOVAs were conducted by the GLM procedure in SAS (SAS Institute, 1988). Once an SSR marker was found that was significantly associated with resistance, more DNA markers including restriction fragment length polymorphism (RFLPs) and isozymes were tested from that area of the linkage group. Mapmaker EXP (Lander et al., 1987) was then used to determine the order of the marker loci in the region of interest and the distances between them. Linkage group designations were made by means of mapped loci from the composite genetic linkage map (Cregan et al., 1999) and maintained on the Soybase web site (Grant et al., 2002).


   RESULTS AND DISCUSSION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
The cross of Williams x PI399073 resulted in F2:3 families that fit a 3:1 resistant to susceptible phenotypic ratio. Ten individual F3 seedlings from 39 F2:3 families were inoculated with P. sojae pathotype vir 7 (OH-race 1) and after 10 days 31 F2:3 families were scored as resistant and eight were scored as susceptible ({chi}2 = 0.42). To confirm this result, 10 additional F3 seedlings from each F2 plant were inoculated with pathotype vir 1b, 1d, 3a, 3b, 3c, 4, 5, 6, 7 (OH-race 17). A 3:1 ratio was observed again by means of this second pathotype, and the same eight F2:3 families were susceptible in both tests (Table 1).


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  		Table 1. Summary of phenotypic ratios of F2:3 soybean families tested with different pathotypes of P. sojae from both the Williams x PI399073 and S 19-90 x PI399073 crosses.

 
Thirty-one out of 55 SSR markers screened were found to be polymorphic between Williams and PI399073. These 31 markers were then tested on the 39 F2:3 families. The genotypic data from these 31 markers was then tested with the phenotypic data from both pathotype inoculations in a single marker-trait analysis by PROC GLM (SAS Institute, 1988). The results of the ANOVA indicated that only the marker Satt228 was significantly associated with the resistance phenotype (P < 0.05). The other 30 markers did not show a significant association, indicating that the new resistance allele must be near Satt228 (Table 2). The SSR marker Satt228 is located at position 161.8 on MLG A2 and it also results in a 1:2:1 ratio indicating that this marker fit the expected segregating ratio for a codominant marker (Table 3) (Soybase web site; Grant et al., 2002).


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  		Table 2. SSR markers used to identify a marker associated with the resistance to Phytophthora sojae found in soybean PI399073, and the Rps genes linked to various markers are indicated.

 

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  		Table 3. Summary of the molecular marker results from F2:3 soybean families of the crosses Willams x PI399073 and S 19-90 x PI399073 that indicate that the allele for resistance to P. sojae is associated with Satt228 and Sat_040.

 
To position more accurately the new resistance gene on MLG A2, it was necessary to find other markers in this region that were polymorphic for Williams and PI399073. Two nearby SSR markers, Satt538 (position 173.5) and Sat_040 (position 123), were polymorphic between Williams and PI399073, but many others were not polymorphic. Also mapped near Satt228 were other types of markers, both RFLPs and isozymes. The RFLP marker Bng225_1 and the isozymes acid phosphatase (Ap) and leucine aminopeptidase (Lap) are near Satt228 and were all three polymorphic between Williams x PI399073.

Since numerous polymorphic markers were identified on MLG A2, Mapmaker EXP (Lander et al., 1987) was used to determine the order of the resistance phenotype, the marker loci, and the linkage distances between them using LOD = 3.0 (Fig. 1). The resistance phenotype was flanked by Satt228 and Sat_040.



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  		Fig. 1. Linkage Map of MLG A2 of soybean. A. Williams x PI399073. B. S 19-90 x PI399073. Distances between markers were assigned in centimorgans (Kosambi) by means of a LOD = 3.0. The novel locus, Rps8, was placed relative to known markers previously mapped to MLG A2 found on the composite soybean genetic map.

 
To confirm the presence of a new gene, an additional cross with S 19-90 was evaluated with SSR markers, in contrast to earlier techniques that required developing multiple populations to test for allelism. If the new resistance gene could be mapped to the same location in this second cross, this correspondance would confirm the location of the new Rps gene. S 19-90 was chosen to incorporate Sclerotinia stem rot resistance, caused by Sclerotinia sclerotiorum (Lib.) de Bary, from S 19-90 as a step towards cultivar development. S 19-90 contains Rps1c so expectations for segregation ratios would be different.

The same procedures were used to map the new resistance gene in the cross S 19-90 x PI399073. First, 10 F3 seedlings from each of 54 F2:3 families were inoculated with pathotype vir 7 (OH-race 1). The results of this inoculation fit a 15:1 ratio, which was expected because of the presence of both the new gene and Rps1c (Table 1). Second, 10 F3 seedlings were inoculated with vir 1a, 1b, 1c, 1k, 7 (OH-race 25). This inoculation also fit a 3:1 ratio, 48 F2:3 families that were scored as resistant and 9 were scored as susceptible (Table 1).

The SSR markers found to be polymorphic in the first cross were tested on the parents of the second cross S 19-90 x PI399073. Satt228, Satt538, and Sat_040 were also polymorphic for this cross. Other SSR markers from MLG A2 were tested with S 19-90 and PI399073 and Satt378 was found to be polymorphic as well. Additionally, the RFLP markers Bng225_1 and Bng205_1 were polymorphic for S 19-90 x PI399073 cross. However, the Lap isozyme was the only polymorphic locus for this cross.

All of the polymorphic markers for S 19-90 and PI399073 were used to generate linkage distances and loci order by Mapmaker EXP as done previously with an LOD score of 3.0. The new resistance allele mapped to the same location between Satt228 and Sat_040. The order of the markers was similar between the two crosses. The difference between the two maps of Williams x PI39903 and S 19-90 x PI39903 was the distance between markers.

In the past, numerous inoculations with different pathotypes of P. sojae were needed to confirm the presence of a new resistance allele in a number of soybean crosses. Mapping new alleles was also difficult due to the limited number of classical gene markers. SSR DNA marker technology has expedited this process of mapping a new gene with more precision. SSR markers linked to known Rps genes were selected in order to determine if a previously described gene or a new allele of a known gene was involved in the resistance reaction (Table 2) (Demirbas et al., 2001). Rps5 is not included on the table because there are no SSR markers linked to Rps5; however, Diers et al. (1992) reported that Rps5 was linked to Rps4. Rps4 is found on MLG G, so it is expected that Rps5 would also be found on MLG G; however, this has not yet been confirmed (Demirbas et al., 2001).

A new resistance locus to P. sojae has been mapped to MLG A2 of the soybean map. The other Rps resistance alleles are found on MLGs N, J, F, and G. This new locus, hereafter designated Rps8, is the first P. sojae resistance locus to be placed on MLG A2. Another resistance allele has also been mapped to A2. Rhg4, a resistance allele to race 3 of soybean cyst nematode (Heterodera glycines Ichinohe) is found at 42 cM on MLG A2 (Matthews et al., 1998).

Rps8 is linked to the isozyme locus, acid phosphatase (Ap). Interestingly, other resistance alleles are linked to this classical marker. The root knot nematode resistance gene (Mi gene) in tomato (Lycopersicon esculentum L.) is tightly linked to the acid phosphatase-1 (Aps-1) locus (Williamson and Colwell, 1991).

Since the source of Rps8 was a South Korean PI, PI399073, we are continuing to evaluate germplasm from this country to determine if more Rps alleles to P. sojae are present. Although agronomically these PIs are poor, some of the alleles that they carry are valuable and can be moved into more suitable backgrounds for U.S. cultivars. This process can be expedited by molecular markers like Sat_040 and Satt228 in marker assisted selection (MAS).


   ACKNOWLEDGMENTS
 
We wish to thank C.E. Vallejos for providing the RFLPs Bng205_1 and Bng225_1 used in this study.


   NOTES
TOP
 NOTES
ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Salaries and research support provided by State and Federal Funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University. This research project was supported by Ohio's Soybean Producers' check-off dollars through the Ohio Soybean Council.

Received for publication March 25, 2002.


   REFERENCES
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 




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