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Crop Science 41:1584-1589 (2001)
© 2001 Crop Science Society of America

CELL BIOLOGY & MOLECULAR GENETICS

A Microsatellite Marker for Tagging Dn2, a Wheat Gene Conferring Resistance to the Russian Wheat Aphid

Cynthia A. Millera, Ahu Altinkutb and Nora L. V. Lapitan*,c

a Dep. of Human Medical Genetics, Univ. of Colorado Health Sciences Center, Denver, CO 80262
b TUBITAK Marmara Res. Center, The Res. Inst. for Genetic Engineering and Biotechnology, P.O. Box 21, 41470, Gebze-Kocaeli, Turkey
c Dep. of Soil and Crop Sciences, Colorado State Univ., Fort Collins, CO 80523

* Corresponding author (nlapitan{at}lamar.colostate.edu)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The Russian wheat aphid (RWA), Diuraphis noxia Mordvilko, is an economically important pest of wheat (Triticum aestivum L.). An effective means to control the RWA is through the use of resistant cultivars. While a phenotype-based selection has been useful for selection of resistant plants, it has inherent limitations. Screening can only be done during cool months of the year, and symptom expression is influenced by the environment. Pyramiding of two or more RWA resistance genes is also difficult because of the presence of only one aphid biotype in the USA at present. This study was conducted to develop a DNA marker that is tightly linked to Dn2, and to test the effectiveness of the marker as a tag for Dn2 among a limited number of cultivars tested. We report mapping of five microsatellite markers linked to Dn2. The closest marker was Xgwm437 at 2.8 cM, and it distinguished lines containing Dn2 from eight susceptible cultivars and seven resistant cultivars carrying other RWA resistance genes. Xgwm437 should be effective for marker-assisted selection of Dn2-containing plants and for combining Dn2 with other resistance genes in a gene pyramiding program.

Abbreviations: bp, base pairs • IPK, Institute for Plant Genetics and Crop Research • JIC, John Innes Centre • LOD, log of the odds • MAS, marker-assisted selection • PCR, polymerase chain reaction • RFLP, restriction fragment length polymorphism • RWA, Russian wheat aphid


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
THE RUSSIAN WHEAT APHID has caused large-scale crop damage to both wheat and barley (Hordeum vulgare L.) since its introduction into the United States in 1986 (Morrison and Peairs, 1998; Webster et al., 1987). Direct economic losses in small grains incurred from reduced yield and increased production costs during 1987 to 1995 were estimated to be >$485 million. This includes an estimated 8.1 million pounds of insecticides applied by American farmers at a cost of >$95 million (Morrison and Peairs, 1998; Webster et al., 2000). The RWA is a global concern; it was first reported in the Mediterranean region and southern Russia in the early 1900s, and spread by the late 1970s to South Africa (Webster et al., 1987). Control of the RWA with insecticides is neither environmentally nor economically effective because infested susceptible plants exhibit leaf rolling, which protects the aphids from the topical treatment of insecticides (Ma et al., 1998). In addition to leaf rolling, susceptible plants also display leaf streaking, head trapping, and plant death in extreme cases.

The most effective means to control the RWA is through the use of resistant cultivars. There are at least 10 known genes for resistance to RWA, namely Dn1, Dn2 (Du Toit, 1987), dn3 (Nkongolo et al., 1991a), Dn4 (Nkongolo et al., 1991b), Dn5 (Marais and Du Toit, 1993; Saidi and Quick, 1996; Zhang et al., 1998), Dn6 (Saidi and Quick, 1996), Dn7 (Marais and Du Toit, 1993), Dn8, Dn9, and Dnx (Liu et al., 2000). The known chromosome locations of these genes are namely: 7D for Dn1 (Schroeder-Teeter et al., 1994), Dn2 (Ma et al., 1998), Dn5 (Du Toit, 1987; Marais and Du Toit, 1993), Dn8, and Dnx (Liu et al. 2000); 1D for Dn4 (Ma et al. 1998) and Dn9 (Liu et al. 2000); and 1RS for Dn7 (Marais et al., 1994). The allelic relationship among genes located on chromosome 7D was studied, and the results were inconsistent. Dn1 and Dn2 were reported to be nonallelic by Du Toit (1989), and allelic by Saidi and Quick (1996). The dominant gene Dn5 contained in PI 292994 was reported to be allelic with Dn1 and Dn2 (Saidi and Quick, 1996), while another study proposed that Dn5 and Dn1 are linked loci (Marais and Du Toit, 1993). Zhang et al. (1998) reported that PI 292994 contains three classes of genotypes in terms of number and type of genes for resistance to RWA. The three types contain one dominant gene, two dominant independent genes, or one dominant and one recessive gene. All of these characterized RWA resistance genes are present in either unadapted lines or wild relatives of wheat.

Breeding for RWA-resistant cultivars requires a reliable method of selecting plants containing a resistance gene. While a phenotype-based selection method is straightforward, it has several limitations. Greenhouse screening is typically done during cooler months of the year because there is an increased mortality rate of RWA in temperatures above 20°C (Michels and Behle, 1988). Screening cannot be performed in areas where the aphid does not exist. Environmental influence on symptom expression may result in inaccurate classification of phenotypes. An average 10% error rate is typical for the greenhouse screening method (J.S. Quick, 2000, personal communication). It is highly desirable to employ a screening technique that is based on molecular markers linked to the resistance genes (Ma et al., 1993; 1994). Aside from overcoming the problems associated with phenotypic screening, marker-assisted selection (MAS) would enable breeders to combine two or more RWA resistance genes efficiently. Gene pyramiding of RWA resistance genes is laborious because there is only one aphid biotype in the U.S. at present. Yet, there are at least eight known biotypes worldwide (Puterka et al., 1992) and it is possible that new biotypes could appear in the U.S. (Quick et al., 1991).

Mapping of RWA resistance genes in wheat has been accomplished using different types of molecular markers. Restriction fragment length polymorphism (RFLP) markers Xabc156 and Xksua1 were linked to Dn4 and Dn2, respectively (Ma et al., 1998). Xksua1 mapped 9.8 cM from Dn2 on chromosome 7D, and Xabc156 mapped 11.6 cM from Dn4 on chromosome 1D. However, both markers were not linked tight enough to be effective for tagging these genes (Ma et al., 1998). RAPD and SCAR markers linked to Dn2 were developed, with genetic distances ranging from 3.3 cM to 4.4 cM (Myburg et al., 1998). OPB10880c was the closest marker to Dn2 at 3.3 cM; however, it did not distinguish resistant plants containing Dn2 from a resistant line containing Dn4. A microsatellite marker Xgwm111was linked to five RWA resistance genes Dn1, Dn2, Dn5, Dnx, and Dn9, on chromosome 7D (Liu et al., 2000). The genetic distances of the markers from the respective genes were between 1.5 cM and 3.8 cM.

This study was a follow-up on Ma et al.'s (1998) results, and the objectives were: (i) to develop a DNA marker that is tightly linked to Dn2, and (ii) to test the effectiveness of the marker for tagging Dn2 among a limited number of cultivars tested, and for pyramiding with other Dn genes. In this paper, we report mapping of five microsatellite markers linked to Dn2. The closest marker, Xgwm437, was linked at 2.8 cM, and it distinguished lines containing Dn2 from eight susceptible cultivars and eight out of nine resistant cultivars carrying other resistance genes.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Genetic Materials
Development of the mapping population was described by Ma et al. (1998). Briefly, F2-derived F3 families were generated from a cross between RWA-resistant PI 262660 and RWA-susceptible cultivar ‘Carson’, followed by selfing of one F1 plant, and selfing of the F2 individuals. Table 1 lists other wheat cultivars used in this study, the RWA resistance genes they contain, and seed source.


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  		Table 1. Wheat genotypes used in this study, RWA resistance genes they contain, and seed sources.

 
RWA Resistance Screening
The planting and infestation techniques used were according to Saidi and Quick (Saidi and Quick, 1996), and were as described in Ma et al. (1998). RWA resistance screening data from Ma et al. (1998) were used in this study.

DNA Extraction and Bulked Segregant Analysis
DNA extraction was according to Ma and Sorrells (1995). Two pools of DNA or bulked segregants (Michelmore et al., 1991) were constructed by combining DNA from six resistant and six susceptible F3 families. The pair of bulked segregants was screened for polymorphisms in microsatellites.

Primers
Microsatellite markers previously mapped in wheat chromosome 7D were used in this study. These included Xgwm37, Xgwm44, Xgwm111, Xgwm295, Xgwm428, Xgwm437 (Roder et al., 1998b), Xpsp3079, Xpsp3094, Xpsp3113, and Xpsp3123 (Bryan et al., 1997). Primers for Xgwm microsatellites were obtained from the Institute for Plant Genetics and Crop Research (IPK), Gatersleben, Germany, and those for Xpsp microsatellites were from the John Innes Centre (JIC) in Colney, Norwich, UK. Additional primers were synthesized by GIBCO BRL (Rockville, MD) using sequences reported by Roder et al. (1998a)( b).

Polymerase Chain Reaction
The annealing temperatures and polymerase chain reaction (PCR) conditions for the IPK and JIC microsatellites were as previously reported by Roder et al. (1998b) and Bryan et al. (1997), respectively. The thermocycler program consisted of 5 min at 94°C, followed by 30 cycles with 94°C for 1 min, 1 min at either 61° or 63°C (depending on individual microsatellite conditions), 1 min at 72°C, and a final extension step of 5 min at 72°C. Amplification of both primer sets was performed in a PTC-100 MJ thermocycler (MJ Research, Watertown, MA).

Electrophoresis
Polymerase chain reaction products were separated on a 6% denaturing polyacrylamide gel (19:1 acrylamide:Bis, 8 M urea) at 65 V for 2.5 h in 1x TBE buffer (0.09 M Tris-borate and 0.002 M EDTA). Polymerase chain reaction products were detected by silver staining according to the manufacturer's instructions (Promega, Madison, WI). Band sizes were determined by comparison with a 10 base pair (bp) DNA ladder size standard from Gibco-BRL (Rockville, MD).

Linkage Analysis
Microsatellites showing polymorphisms between the pair of bulked segregants were mapped in 108 F3 families. A linkage map was constructed using MapMaker 3.0 program (Lander et al., 1987). A log of the odds (LOD) score of 3.0 was used to determine the order of the loci. Centimorgan units were calculated using the Kosambi mapping function (Kosambi, 1944).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Microsatellite Markers Linked to Dn2
The F2 population derived from the cross between PI 262660 and Carson segregated in a 1:2:1 ratio for resistance to RWA, indicating the presence of a single dominant gene (Ma et al., 1998). To find markers that are useful for tagging Dn2, a pair of bulked segregants differing in the presence or absence of the Dn2 gene was screened for polymorphisms using microsatellite markers previously mapped to wheat chromosome 7D. Five of the ten microsatellites tested showed polymorphisms between the bulked segregants. These were Xgwm44, Xgwm111, Xgwm437, Xpsp3113, and Xpsp3123. These five markers were mapped in 108 F3 families derived from the cross PI 262660 (resistant) x Carson (susceptible). All five microsatellite markers were linked to Dn2 (Fig. 1). Xgwm437 was the nearest marker to Dn2, with a genetic distance of 2.8 cM. On the same side of the gene, Xpsp 3123 mapped at 8.1 cM, and Xpsp3113 linked at a farther distance of 21.7 cM. On the opposite side of the gene, the nearest marker was Xksua1, while Xgwm44 was linked at 12.7 cM. Xgwm111 was linked to Xgwm44 and Xksua1. Its exact position relative to these two markers, however, was ambiguous and its map location is depicted with a bracket between Xgwm44 and Xksua1.



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  		Fig. 1. Linkage map of wheat chromosome 7D containing the Russian wheat aphid resistance gene, Dn2. Genetic distances are given in cM. The marker Xgwm111 was mapped at a log of the odds (LOD) score of <2, while the rest were mapped at a LOD score of 3.

 
Heterogeneity for Xgwm437 Band in PI 262660
The segregation of Xgwm437 in the F2 progeny fits a 1:2:1 ratio (0.75 <= P <= 0.5). However, we observed differences in the pattern of Xgwm437 microsatellite sequences between the resistant progeny and the resistant parental check for PI 262660 (Fig. 2, lane D). The highest band in the resistant progeny was 100 bp (Fig. 2, lanes B, H), whereas the highest band for the PI 262660 check was 104 bp (Fig. 2, lane D). Note that seed from the original PI 262660 plant that was crossed with Carson to produce the mapping population was not available, and the PI 262660 check used in this study came from another plant of PI 262660. This observation suggested that there is heterogeneity for this microsatellite sequence in PI 262660. We tested this by amplifying Xgwm437 sequences from six individual plants of PI 262660 obtained from the National Small Grains Collection in Aberdeen, ID. Three unique types of banding patterns were observed. Types I, II, and III had highest band sizes of 104, 102, and 100 bp, respectively (Fig. 2, lane E). The F2 progeny contained the Type III band.



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  		Fig. 2. Silver-stained polyacrylamide gel showing polymerase chain reaction (PCR) amplification products of microsatellite Xgmw437 from DNA of B, six resistant F2 progeny; C, six susceptible F2 progeny; D, PI 262660 parental check; E, PI 262660 plant containing 104 base pairs (bp) as the highest band (Type I); F, PI 262660 plant containing 102 bp as the highest band (Type II); G, PI 262660 plant containing 100 bp as the highest band (Type III); H, a resistant F3 progeny; I, a susceptible F3 progeny; and J, a resistant progeny heterozygous for Xgwm437 which was not among the 6 resistant F2 bulked in lane B. Lane A contains a 10-bp DNA ladder (Gibco BRL, Rockville, MD).

 
We then tested whether there were differences in response to RWA among PI 262660 plants containing the three types of Xgwm437 patterns. Six individual plants of PI 262660 were grown in the greenhouse, infested with RWA, and scored for their reaction. DNA from the infested plants was amplified using Xgwm437 primers. One, three, and two plants exhibited Types I, II, and III, respectively. With the exception of one plant, all showed no leaf rolling and were scored as resistant to RWA. One plant with a type II pattern showed mild rolling of leaves and was classified as mildly resistant. Based on the results, there was no clear association between resistance (or susceptibility) and the three types of patterns for Xgwm437 microsatellite sequences.

Effectiveness of Xgwm437 as a Tag for Dn2
Polymerase chain reactions using Xgwm437 primers were performed on different wheat cultivars to determine the effectiveness of Xgwm437as a tag for Dn2 (Fig. 3). The cultivars tested included eight containing resistance genes other than Dn2 (Table 1), and nine susceptible cultivars.



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  		Fig. 3. Silver-stained polyacrylamide gel showing PCR amplification products of microsatellite Xgmw437 from DNA of various wheat cultivars. The amplification products of Xgwm437 from PI 262660 are distinct from those in susceptible cultivars and resistant cultivars containing genes other than Dn2. The first lane contains a 10-bp DNA ladder (Gibco BRL, Rockville, MD).

 
PI 262660 plants containing Types I, II, or III patterns of Xgwm437 were distinct from all nine susceptible cultivars tested (eight of the nine are shown in Fig. 3). PI 262660 plants with Types I and III patterns were also distinct from the eight resistant genotypes tested containing genes other than Dn2. PI 262660 with the Type II pattern, however, was indistinct from PI 372129, which contains Dn4. If these two PI lines are used to pyramid Dn2 and Dn4, Xgwm437 alone would not be able to distinguish progeny that contain both Dn2 and Dn4 from those that only contain Dn4.

The resistant cultivars Halt, Prairie Red, and Tam 200R, which all contain Dn4 (Quick et al., 1996), have Xgwm437 patterns distinct from those in PI 262660 (Fig. 3). The banding pattern of Prairie Red was similar to its susceptible parent Tam 107, while that of Tam200R was similar to its susceptible parent Tam200 (Fig. 3). Therefore, it is possible to use Xgwm437to tag Dn2 in a background containing Dn4 when the Dn4-containing parent does not have the Type II pattern of Xgwm437. Of course, a marker that effectively tags Dn4 would also be required in this pyramiding scheme.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
This paper reports the identification of a microsatellite marker (Xgwm437) which proved to be effective for tagging the RWA resistance gene, Dn2. We set two criteria for evaluating the effectiveness of a molecular marker for tagging Dn2. First, the marker must distinguish plants containing Dn2 from plants that do not contain it, which include susceptible cultivars and resistant plants containing other Dn genes. Second, the marker must be linked to the gene at a genetic distance less than 10 cM, to provide a greater efficiency for selection than what can be achieved using the phenotypic screening method ({approx}10%) (Quick, 2000, personal communication).

The marker Xgwm437 met both criteria. The genetic distance of Xgwm437 from Dn2 was 2.8 cM and it is the closest marker reported for this gene thus far (Liu et al., 2000; Ma et al., 1998; Myburg et al., 1998). The effectiveness of this marker as a tag for Dn2 was shown by the distinct band patterns of amplified Xgwm437 sequences from PI 262660 compared with those in nine susceptible cultivars and eight resistant genotypes containing other Dn genes. The type II pattern of Xgwm437 found in some plants of PI 262660, however, was also present in PI 372129 (Dn4 source). Therefore, caution must be used in a pyramiding program to combine Dn2 and Dn4 by selecting a Dn4 donor which does not contain the Type II pattern of Xgwm437. The use of additional markers on the other side of Dn2 may also be considered for pyramiding it with Dn4. Previous tests we had done showed that the nearest marker on the opposite side of Dn2, Xksua1, is not useful for this purpose because Xksua1 did not detect polymorphism between PI 262660 and PI 372129 using eight different enzymes tested (N.L.V. Lapitan and Z.Q. Ma, 1998, unpublished data). Although the two microsatellite markers Xgwm44 and Xgwm111 are at least 12.7 cM from Dn2, either of these may be useful tags in conjunction with Xgwm437 if they prove to be polymorphic between PI 262660 and PI 372129.

Pyramiding several Dn genes may result in a cultivar that can survive the appearance of new aphid biotypes. The ability to pyramid several genes for RWA resistance is one of the most important advantages of using MAS. Because of the presence of only one biotype in the U.S. at present, progeny testing will need to be done after each backcross to identify the presence of more than one gene. This step can be eliminated when using MAS, hence the cultivar development time can be reduced by about half of the length of time it would take using phenotype-based selection. There may be at least three nonallelic RWA resistance genes (Dn1/Dn2/Dn5, Dn8, and Dnx) on chromosome 7D (Marais and Du Toit, 1993; Saidi and Quick, 1996; Zhang et al., 1998). When two or more of these genes are combined with Dn2 in a pyramiding program, greater marker density will be required in order to detect where crossovers occur.

The map presented combines microsatellite markers previously mapped in two wheat maps (Gale et al., 1995; Roder et al., 1998b; Stephenson et al., 1998). The order of Xgwm44, Xgwm111, and Xgwm437 and their genetic distances are consistent with the map of Roder et al. (1998b). The order of Xpsp3123 and Xpsp3113, however, are flipped relative to their order in Stephenson et al.'s (1998) map. This discrepancy may be verified by mapping additional markers distal to Xpsp3113 from Stephenson et al.'s (1998) map to the present map. Dn2 was previously linked to Xgwm111at a distance of 3.2 cM (Liu et al., 2000). Xgwm111was mapped in this study with a LOD score <2, and its exact position on the map is ambiguous, which is similar to its status in Roder et al.'s (1998b) map.

Liu et al. (2000) assigned Dn2 to the short arm of 7D based on the disappearance of a 200-bp band of Xgwm111from wheat ditelosomic line 7DL, which lacks the short arm of 7D. However, it is noted that Roder et al.'s (1998b) map placed Xgwm111 and Xgwm437 on the long arm. Xksua1, which is linked to Dn2, was also mapped on 7DS by hybridization to genomic blots containing wheat deletion lines (Boyko et al., 1999).

Microsatellites have been shown to detect much higher levels of polymorphism and informativeness in hexaploid wheat than any other marker system (Bryan et al., 1997; Roder et al., 1995,1998a; Stephenson et al., 1998). Unlike RFLPs, microsatellites have proven to be useful for detecting polymorphisms between wheat cultivars or lines (Chague et al., 1999). The results of this study demonstrate the usefulness of microsatellites for mapping genes in an F2 population derived from a cross between two wheat cultivars. Using this same population, Ma et al. (1998) previously screened >200 RFLP markers and found only one marker linked to Dn2. Furthermore, since microsatellite markers are PCR-based, these can be used for routine screening in a breeding program.


   ACKNOWLEDGMENTS
 
We thank Garret Anderson for technical support, Zhengqiang Ma for the segregation data and Cenkmen Uncuoglu for preparing the figures. We are grateful to Jim Quick, the National Small Grains Collection, and Frans Marais for seeds, and the John Innes Center and Institute for Plant Genetics and Crop Research for microsatellite primers. This project was partially supported by USDA Contract No. 98-34205-6375, USDA NRI Competitive Grant Program Contract No. 96-35300-3776, and Hatch Funds 644. We thank TUBITAK Marmara Research Center in Turkey for A.H.'s fellowship support.

Received for publication September 20, 2000.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 




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