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CROP BREEDING, GENETICS & CYTOLOGY

Identification, Mapping, and Confirmation of a Soybean Gene for Bud Blight Resistance

^a Univ. of Georgia, Center for Applied Genetic Technologies, 111 Riverbend Road, Athens, GA 30602-6810
^b Pioneer Hi-Bred Int., Crop Genetics Res. and Dev., 19456 St. Hwy 22, Mankato, MN 56001
^c Pioneer Hi-Bred Int., 7300 NW 62nd Avenue, P.O. Box 1004, Johnston, IA 50131
^d Dep. of Plant Pathology, Univ. of Georgia, Georgia Exp. Stn., 1109 Experiment Street, Griffin, GA 30223

^* Corresponding author (rboerma{at}uga.edu).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
Bud blight, caused by Tobacco ringspot virus (TRSV; Genus: Nepovirus; Family: Comoviridae), can significantly reduce the seed yield and seed quality of soybean [Glycine max (L.) Merr.]. The identification of resistance genes and the development of resistant cultivars constitute an effective strategy for preventing yield loss. The objectives of this study were to identify and map quantitative trait loci (QTLs) conditioning resistance to bud blight and validate their genomic location with two populations derived from the cross of ‘Young’ (resistant) x PI 416937 (susceptible). One population consisted of 116 F_4:7 lines and was used to map restriction fragment length polymorphism (RFLP) markers associated with resistance to bud blight. The lines were grown in one-row plots in a randomized complete block design with two replications. The plots were naturally infected with TRSV. At maturity, soybean plots were visually scored according to the number of plants that exhibited terminal bud death. A major QTL was identified and mapped on linkage group (LG) F by the RFLP marker K644_1. It accounted for 82% of the variation in bud blight score. To verify the genomic location of the major bud blight QTL, a second population of Young x PI 416937 that consisted of 180 F_2:3 lines was evaluated. In this population, simple sequence repeat (SSR) markers on LG F near the putative genomic location of the bud blight QTL were utilized. The major QTL conditioning bud blight resistance was confirmed and found to be closely linked to the Satt510 marker.

Abbreviations: CIM, composite interval mapping • cM, centimorgan • LG, linkage group • MAS, marker-assisted selection • QTL, quantitative trait locus • RFLP, restriction fragment length polymorphism • SMV, Soybean mosaic virus • SSR, simple sequence repeat • TRSV, Tobacco ringspot virus

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
BUD BLIGHT, caused by TRSV, can significantly reduce the seed yield and seed quality of soybean [Glycine max (L.) Merr.]. Tobacco ringspot virus is a member of the nepovirus group of plant viruses and consists of two single-stranded RNA molecules. Tobacco ringspot virus affects the foliage and may cause almost total seed loss due to flower abortion. The virus moves into the roots and root nodules and significantly impairs symbiotic N fixation (Orellana, 1981). Symptoms of the virus include stunted growth, discoloration of stems and branches, and curvature of the terminal meristem (Tu, 1986). The most striking symptom is the curvature of the terminal bud to form a crook. The buds on the plant become brown, necrotic, and brittle. Adventitious leaf and floral buds may proliferate excessively (Demski and Kuhn, 1999). Pods are generally severely underdeveloped or aborted and those that set before infection often develop dark blotches.

The mode of transmission of the virus in nature is not known, but the virus has been shown to be mechanically transmitted by grasshoppers (Melanoplus differentialis Thomas), nematodes (Xiphinema americanum Cobb), and thrips (Thrips tabaci Lindeman) (Dunleavy, 1957; Bergeson et al., 1964). In soybean, the virus is transmitted primarily by infected seed and nematodes (Bergeson et al., 1964). Tobacco ringspot virus infection is most detrimental when plants are infected during the early stages of plant development (Kahn and Latterell, 1955; Demski and Kuhn, 1999). Bud blight can cause 25 to 100% yield reduction in soybean (Crittenden et al., 1966). In China, bud blight is one of the three most important diseases of soybean and is considered very destructive in tropical and subtropical regions (Orellana, 1981). Tobacco ringspot virus has had no recent reports relative to the diversity of isolates from soybean (Sue Tolin, 2003, personal communication).

Flor (1947) has defined the gene-for-gene model of host–pathogen interactions. According to this model, the pathogen produces an avirulence (Avr) factor that elicits resistance if the host carries a resistance (R) gene of particular specificity. In Arabidopsis thaliana, genetic studies revealed the identification of a single incompletely dominant locus (TTR1) controlling resistance to TRSV (Lee et al., 1996a).

DNA marker technology has been developed and integrated into soybean breeding programs (Boerma and Mian, 1999; Cregan et al., 1999). Verification and confirmation of the QTL are recommended before the application of MAS in a practical breeding program (Boerma and Mian, 1999). Marker-assisted breeding may accelerate the development of virus-resistant cultivars. Restriction fragment length polymorphism markers have been used extensively in soybean and provide the framework for the construction of linkage maps. Simple sequence repeat markers have been developed in soybean, and they are abundant, highly polymorphic, and distributed throughout the genome (Rongwen et al., 1995; Cregan et al., 1999). Simple sequence repeat markers are highly amenable for automation and allele sizing, which allows for their high-throughput application and makes them an excellent source of DNA markers in a breeding program (Diwan and Cregan, 1997; Mitchell et al., 1997).

The objectives of this study were to identify and map QTLs conditioning resistance to bud blight and validate their genomic location with two populations derived from the cross of ‘Young’ (resistant) x PI 416937 (susceptible).

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
Mapping Population
A soybean population of 116 F_4:7 lines from the cross of Young x PI 416937 was created. Young is a highly productive cultivar that belongs to Maturity Group VI (Burton et al., 1987). The 116 F_4:7 randomly selected inbred lines were developed with the single seed descent breeding method (Lee et al., 1996b). The F₁ seed were produced at Clayton, NC, in 1990 and the F₁ plants were grown at the winter nursery in Isabela, PR. The F₂ plants were advanced in 1991 and individual F₄ plants were harvested at Clayton, NC, in 1992. Progeny rows were increased near Windblow, NC, in 1993. The population and its parents have been characterized for several agronomic and seed traits (Lee et al., 1996b; Mian et al., 1996).

An initial linkage map of this population was generated with 155 RFLP markers that covered 1600 cM and were distributed in 31 LGs (Lee et al., 1996b). In a later study, the map was reconstructed and included SSR markers as they became publicly available (Narvel et al., 2003). The linkage map was constructed with marker data by the Kosambi map function of Gmendel 3.0 as if the data were derived from F₄ lines (Holloway and Knapp, 1993). For grouping linked markers, a minimum LOD (likelihood of odds) of 3.0 and a maximum recombination frequency (rmax) of 0.38 (approximately equal to 50 cM) were used. Linkage groups were assigned to their corresponding LG on the USDA/Iowa State University public genetic map (Cregan et al., 1999). The more recent genetic linkage map of this population consists of 232 RFLP and SSR markers mapped to 30 LGs covering 2100 cM (Narvel et al., 2003).

In 1995, the parents and the 116 F_4:7 lines were evaluated. The experiment was planted on 25 May 1995 near Athens, GA, at the University of Georgia Plant Sciences Farm, in a randomized complete block design with two replications. The entries were grown in one-row plots with a row length of 3 m and a row spacing of 1 m. Each row plot consisted of 80 plants. The soil type at this site was an Appling loamy coarse sand (fine, kaolinitic, thermic Typic Kanhapludults). The plots were naturally infected with TRSV. On the basis of observation of the plots containing the susceptible parent PI 416937, the infestation was uniform throughout the experiment. The presence of the virus was verified by sampling leaves from the experiment and sending them to Agdia, Inc. (Elkhart, IN) for verification of the virus through an ELISA test. The soybean samples were tested for 10 different viruses including TRSV, Soybean mosaic virus (SMV; Genus: Potyvirus; Family: Potyviridae), and the potyvirus group. Two samples of leaves were collected from 20 plots that were either free of virus symptoms (Sample 1) or exhibiting TRSV symptoms (Sample 2). Sample 1 was negative for TRSV. Sample 2 was positive for TRSV and negative for all other viruses. At maturity, soybean plots were visually scored according to the number of plants that exhibited terminal bud death on a scale of 0 (no plants exhibiting bud blight symptoms) to 6 (6 or more plants exhibiting terminal bud death). The scale of 0 to 6 was devised after evaluating the plots of Young and PI 416937. Since the virus infestation rate in the field was low, the scoring scale of 0 to 6 was used. Data were analyzed by ANOVA with Agrobase software (Agronomix Software Inc., Winnipeg, Canada).

Bud blight data from the F_4:7 lines were combined with the RFLP data. For the 155 RFLP marker loci used, the marker class means (Young/Young vs. PI 416937/PI 416937) were compared for the determination of significant difference (P 0.05) by an F test from the Type III mean squares obtained from the General Linear Model procedure of SAS (SAS Institute, 1988). The RFLP data of Lee et al. (1996b) along with SSR data on LG F (Narvel et al., 2003) were utilized to run CIM (Zeng, 1994). QTL Cartographer (Windows version 1.21) was used to more accurately identify the QTL position (Basten et al., 1999; Wang et al., 2001). Zmapqtl Model 6 and a forward regression method were used for CIM. In the Zmapqtl Model 6, two-control markers and a 5-cM window size were selected.

Confirmation Population
A second independent population of 180 F_2:3 lines from the cross of Young x PI 416937 was developed. The initial cross was made in 1993. The F₁ generation was grown in the greenhouse in Athens, GA. The F₂ generation was grown at the University of Georgia Plant Sciences Farm near Athens, GA, in 1994. At maturity, 180 F₂ plants were individually harvested. The parents and 180 lines were grown in 1995 at the University of Georgia Plant Sciences Farm in a randomized complete block design with three replications. The soil type at this site was an Appling loamy coarse sand. Ten entries of each parent were randomized within each replication for a total of 200 entries. The experiment was planted on 5 June 1995 in hill plots with 12 seeds per plot. Hills were planted every 0.45 m along rows spaced 0.76 m apart. Three weeks after planting, each plot was thinned to six plants per plot. After thinning, young trifoliolate leaves from 12 plants (two replications, six plants/replication) of each line were sampled for DNA extraction at the V5 stage of development (Fehr et al., 1971).

Plants were naturally infected with TRSV. On the basis of observation of the plots containing the susceptible parent, the infestation was uniform across the experiment. The presence of the virus was verified as described above for the F_4:7 mapping population. At maturity, the hill plots of Young were compared with the hill plots of PI 416937 for viral symptoms. Since the infestation rate within the field was high, each hill plot was visually scored for the percentage of plants in a hill with delayed leaf drop and severe discoloration of stems and branches. Data were analyzed by ANOVA with Agrobase software (Agronomix Software Inc., Winnipeg, Canada).

DNA was extracted from leaf tissue by the modified CTAB procedure (Keim et al., 1988). It was then quantified with the UV/VIS Spectrometer and diluted to 20 ng µL^-1. Seventeen SSR markers developed by Cregan et al. (1999) were tested in a 66-cM region of LG F (proposed location of the QTL). Five of the 17 SSR markers were found to be polymorphic between Young and PI 416937. Fluorescence primers were synthesized (PE-ABI, Foster City, CA) with phosphoramidite chemistry. Polymerase chain reactions were prepared with the protocol by Diwan and Cregan (1997). The reactions were performed in a dual 384-well and 96-well GeneAmp PCR System 9700 or a 384-well ABI 877 robotic thermal cycler (PE-ABI, Foster City, CA). The cycling consisted of 1 min at 95°C, followed by 32 cycles of 25 s for denaturation at 94°C, 25 s of annealing at 46°C, and 25 s of extension at 68°C. At the end of the cycling procedure, the reaction mixtures were held at 4°C. Electrophoresis was run on an ABI-Prism 377 DNA Sequencer (PE-ABI, Foster City, CA) with 120-mm plates at 750 V for 2 h. Lanes were loaded on a 4.8% acrylamide:bisacrylamide (19:1) gel with KLOEHN micro-syringes (Kloehn Ltd., Las Vegas, NV). Genescan (Version 3.0) was used to analyze DNA fragments which were scored with Genotyper (Version 2.1).

As an initial screen, four bulks were evaluated for their DNA fragments at each SSR marker. DNA bulks consisted of 10 F_2:3 lines without bud blight symptoms and 10 F_2:3 lines with bud blight symptoms (Michelmore et al., 1991). A total of four bulks were created, two susceptible (S1 and S2) where each line averaged 100% of plants with bud blight symptoms, and two resistant bulks (R1 and R2) where lines averaged from 0 to 5.7% of plants with symptoms. After the bulk segregant analysis, the population of 180 F_2:3 lines was evaluated with the five polymorphic markers. The linkage map for the LG F was constructed with the Kosambi map function of MAPMAKER/EXP (Lander et al., 1987). A minimum LOD of 3.0 and a maximum distance of 37.2 cM was used for establishing linkages among markers. Interval mapping was conducted with the computer program MAPMAKER/QTL (Lincoln et al., 1992) to determine associations between SSR markers on LG F and bud blight incidence. A minimum LOD score of 2.5 was used to declare the presence of a QTL.

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
In the mapping population that consisted of F_4:7 lines, the mean bud blight rating for Young was 0.0 (based on a 0 to 6 rating scale), whereas that for PI 416937 was 5.6. The F_4:7 progeny lines exhibited a range of bud blight ratings from 0 to 6 (Fig. 1). The RFLP marker classes (Young/Young vs. PI 416937/PI 416937) were tested for association of specific marker bands with differences in bud blight resistance among lines by one-way ANOVA. Seven significant RFLP markers associated with resistance to bud blight were detected on LG F, LG G, and LG D2 (Table 1). Three of the seven markers represent putative independent QTLs.

View larger version (15K): [in this window] [in a new window]   Fig. 1. Distribution of 116 F4:7 soybean lines of the mapping population of ‘Young’ x PI 416937 for bud blight rating (Rating: 0 = no plants exhibiting bud blight symptoms to 6 = 6 or more plants exhibiting terminal bud death).

Multiple regression analysis is useful for determining the most important markers among and within LGs and resolving whether multiple peaks are caused by single or multiple QTLs on the same LG. Composite interval mapping combines interval mapping with multiple regression (Zeng, 1994). To increase the marker density on LG F that harbors the major QTL, the RFLP data (Lee et al., 1996b) were combined with the SSR data of LG F (Narvel et al., 2003) and CIM was utilized. Composite interval mapping was conducted with QTL Cartographer and identified one major QTL on LG F (Fig. 2). No additional QTL on other LGs were detected, suggesting that the minor QTL on LG G and D2 identified from one-way ANOVA were most likely Type I errors. The major QTL for bud blight resistance is located within a 5.8-cM interval, between the RFLP loci Blt025_1 and A069_b, with a LOD score of 64 (Fig. 2). The high LOD score and the sharpness of the peak position indicates that bud blight resistance is likely governed by one major gene located on LG F. These results are in agreement with those of Arabidopsis thaliana (L.) Heynh., where genetic mapping studies revealed that TRSV resistance is controlled by a single major gene (Lee et al., 1996a).

View larger version (12K): [in this window] [in a new window]   Fig. 2. QTL-likelihood plot for bud blight on Linkage Group F for the F4:7 soybean lines of ‘Young’ x PI 416937 based on composite interval mapping. The significance threshold is indicated by a line at LOD = 2.5.

The utilization of RFLP markers for MAS in a breeding program is difficult because of their low polymorphic content and their high technical demand. Although RFLP-based maps provide a framework for MAS, mapping QTLs with SSR markers would greatly facilitate MAS, because SSRs are practical for high throughput application (Akkaya et al., 1995; Maughan et al., 1995; Powell et al., 1996; Diwan and Cregan, 1997). Toward this end, SSR markers on LG F were utilized in a second population of Young x PI 416937 to confirm the genomic position of the QTL for bud blight resistance.

In this study, the confirmation population consisted of F_2:3 lines that possessed from 0 to 100% of plants infected with bud blight (Fig. 3). Of the 180 F_2:3 lines, 36 lines had 100% incidence of bud blight and 13 lines had a 0% incidence. PI 416937, the susceptible parent, averaged 98% bud blight incidence whereas the resistant parent, Young, averaged 6% incidence (Fig. 3). The range of bud blight incidence among the 10 entries of Young was 0 to 19%, and that of PI 416937 was 93 to 100%.

View larger version (20K): [in this window] [in a new window]   Fig. 3. Distribution of 180 F2:3 soybean lines of the confirmation population of ‘Young’ x PI 416937 for percentage of plants exhibiting bud blight.

After the initial screening with bulk segregant analysis, the entire population of 180 F_2:3 lines was evaluated with the five SSR markers on LG F. Interval mapping confirmed that the QTL conditioning bud blight on LG F was located in the 13.9-cM interval between Satt114 and Satt510 (Fig. 4). The most likely QTL location was 4 cM from Satt510. On the USDA/Iowa State University soybean linkage map, Satt510 is located 2.3 cM from RFLP marker K644_1, while on the University of Utah map it is within 4.3 cM (Cregan et al., 1999). In the F_4:7 lines (mapping population of Young x PI 416937), the QTL for bud blight resistance was found to be located between RFLP markers K644_1 and A069_b (Fig. 2). In the F_2:3 lines (confirmation population of Young x PI 416937), the QTL for bud blight resistance was verified and mapped to this same region of LG F 4 cM from Satt510 (Fig. 4).

View larger version (11K): [in this window] [in a new window]   Fig. 4. Linkage Group F (LG F) for the Young x PI 416937 F2:3 soybean population showing the five SSR markers and their distance in cM. Location of RFLP marker K644_1 is approximated based on Cregan et al. (1999).

View larger version (30K): [in this window] [in a new window]   Fig. 5. Mean incidence of bud blight in 180 F2:3 soybean lines homozygous for the ‘Young’ (Y/Y) band, homozygous for the PI 416937 (PI/PI) band, and heterozygous (Y/PI) for bands at Satt510.

	ACKNOWLEDGMENTS

 
This research was supported by funds allocated to Georgia Agricultural Experiment Stations and by grants from the Georgia Agric. Commodity Commission for Soybeans, Georgia Seed Development Commission, and the United Soybean Board.

Received for publication May 2, 2002.

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TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 

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