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PCR Markers for Triticum speltoides Leaf Rust Resistance Gene Lr51 and Their Use to Develop Isogenic Hard Red Spring Wheat Lines

^a INTA EEA Marcos Juárez, CC 21, 2580-Marcos Juárez, Argentina
^b Dep. of Agronomy and Range Science, One Shields Ave., Univ. California, Davis, CA 95616, USA
^c USDA-ARS, Cereal Disease Lab., 1551 Lindig Ave, Univ. of Minnesota, St. Paul, MN 55108

^* Corresponding author (jdubcovsky{at}ucdavis.edu)

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
New leaf rust resistance genes are needed in wheat (Triticum aestivum L.) to provide additional sources of resistance to the highly variable and dynamic leaf rust pathogen Puccinia triticina Eriks. Leaf rust resistance gene Lr51, located within a segment of Triticum speltoides Taush chromosome 1S translocated to the long arm of chromosome 1B of bread wheat, is resistant to the current predominant races of leaf rust in the USA. The objectives of this study were to determine the genetic length of the translocated 1S segment, develop a PCR marker for Lr51, and use this marker to generate isogenic lines for this gene. Characterization of two translocation lines (F-7-3 and F-7-12) with 10 molecular markers indicated that F-7-3 has an interstitial T. speltoides chromosome segment of 14 to 32 cM long including loci XAga7 and Xmwg710, whereas line F-7-12 has a complex series of translocations among chromosomes of homeologous group 1. On the basis of the DNA sequence of the A, B, D, and S alleles of the XAga7 locus, we designed a cleavage amplified polymorphic sequence (CAPS) marker for the S genome allele. Primers S30-13L and AGA7-759R preferentially amplified the XAga7 1S (819 bp) and 1B alleles (783 bp). These amplification products can be separated in agarose gels after digestion with PstI or BamHI restriction enzymes. This CAPS marker was validated in a collection of 32 common wheat cultivars and was used to develop three pairs of hard red spring isogenic lines from the donor parent F-7-3. These isogenic lines will be valuable for future assessment of the effect of this chromosome introgression on agronomic performance and end-use quality.

Abbreviations: BC, backcross • CAPS, cleaved amplified polymorphic sequence • CS, Chinese Spring • HRS, hard red spring • MAS, marker assisted selection • PCR, polymerase chain reaction • RFLP, restriction fragment length polymorphism

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
LEAF RUST (caused by Puccinia triticina Eriks.) is one of the most common and widespread diseases of wheat worldwide; therefore, incorporating genetic resistance to this pathogen into adapted germplasm is a major goal of most wheat breeding programs. In the USA, yield losses due to leaf rust occur annually throughout the soft red winter wheat region of the eastern states, the hard red winter wheat region of the southern and mid Great Plains states, and the northern spring wheat area of the upper Midwest. Yield losses of 10% or more occur when heavy rust infections defoliate flag leaves during grain filling (Chester, 1946).

Utilizing disease resistance genes minimizes the need for the application of costly fungicides, thus reducing environmental contamination risks and decreasing production costs. Approximately 50 leaf rust resistance genes from wheat and wheat relatives have been cataloged (McIntosh et al., 2003), and molecular markers are available for many of them (Procunier et al., 1995; Gold et al., 1999; Helguera et al., 2000; Huang and Gill, 2001; Helguera et al. (2003), http://maswheat.ucdavis.edu/; verified 18 November 2004). Unfortunately, many of the race specific genes are no longer effective against new virulent races of this pathogen. Wild relatives of wheat may be a useful source of additional resistance genes to counter balance the continuous evolution of leaf rust populations.

Triticum speltoides Taush (2n = 14, S genome) is an attractive source of high levels of resistance to leaf, stem, and stripe rust of wheat (Dvorak, 1977), and leaf rust resistance genes Lr28, Lr35, Lr36, and Lr47 were derived from this species (McIntosh et al., 2003). Crosses between this species and hexaploid wheat (T. aestivum L. 2n = 42, ABD genomes), followed by selection of resistant progeny, frequently resulted in translocations between the T. speltoides and common wheat chromosomes since many T. speltoides genotypes have the ability to promote homeologous chromosome pairing when hybridized with wheat (Dvorak, 1977).

The wheat breeding line ‘Neepawa’*6/Triticum speltoides F-7 was selected from the cross T. aestivum cv. Neepawa x T. speltoides accession F (Dvorak, 1977). A 3-to-1 segregation ratio of resistant to susceptible plants in the F₂ population indicated that a single gene determined this source of resistance. Monosomic and ditelosomic analysis provided evidence that the resistance gene was transferred to chromosome arm 1BL (41% recombination with centromere) (Dvorak and Knott, 1980). This gene, temporarily named LrF7, has been designated Lr51 (B. McIntosh, personal communication).

In tests for resistance to P. triticina race 5, plants homozygous for Lr51 were highly resistant with hypersensitive flecks, whereas heterozygous plants showed slightly lower levels of resistance with small pustules surrounded by necrosis and chlorosis, indicating incomplete dominance (Dvorak, 1977). The Neepawa*6/Triticum speltoides F-7 line exhibited very low infection types with the seven leaf rust races tested (Dvorak and Knott, 1980).

In spite of its high levels of resistance to predominant leaf rust races, Lr51 has not been widely deployed in breeding programs, probably because of negative genetic effects associated with the presence of large T. speltoides chromosome segments and/or additional homeologous translocations in other wheat chromosomes. The objectives of this study were to (i) determine the length of the T. speltoides translocations in distinct Lr51 lines, (ii) explore the presence of additional structural changes induced by T. speltoides, (iii) develop a set of PCR markers for efficient selection of Lr51 among segregating progeny, and (iv) develop hard red spring (HRS) Lr51 isogenic lines for use in evaluating the effect of this alien chromosome introgression on agronomic performance and bread-making quality.

	MATERIALS AND METHODS

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Seeds from the two lines derived from Neepawa*6/Triticum speltoides F-7 line (Dvorak, 1977; Dvorak and Knott, 1980), F-7-3, and F-7-12 were kindly provided by Dr. J. Dvorak (University of California, Davis). He also provided seeds of the original recurrent parent Neepawa, Chinese Spring nullisomic-tetrasomic lines N1AT1B, N1BT1D, and N1DT1A (Sears, 1954), T. speltoides (accessions # S3362, S3343), T. tauschii (Cosson) Schmalh. (D genome, accession DV148), and T. urartu Tum. (A genome, accession G3221).

Recurrent HRS cultivars Express (WestBred), Kern (University of California), and breeding line UC1037 (University of California) were crossed with the Neepawa*6/Triticum speltoides F-7-3 line. The F₁s were backcrossed six times with the respective recurrent parents, and in each generation, two individuals heterozygous for Lr51 were selected by marker-assisted selection (MAS). Finally, BC₆ plants heterozygous for Lr51 were self-pollinated and homozygous plants were selected among BC₆F₂ plants using the molecular marker described below. After six backcrosses, selected plants are expected to be more than 99% identical to the recurrent parent.

Finally, a diverse set of 32 wheat cultivars and breeding lines (mainly from USA and Argentina) was analyzed to validate the Lr51 CAPS marker (Table 1).

Four to six BC₆F₃ plants from one or two independent homozygous BC₆F₂ plants per genotype were evaluated for seedling resistance to leaf rust at the Cereal Disease Laboratory (St. Paul, MN), as previously described (Kolmer et al., 2003). Plants were grown in a greenhouse set at 18 to 21°C with 8 h of metal halide supplemental lighting at 400 to 450 µmol m^–2 s^–1 at bench level. Seedlings were inoculated with leaf rust races THBJ (avirulence/virulence formula 9, 24, 3ka, 11, 17, 30, 18/1, 2a, 2c, 3, 16, 26, 10) and MCDS (avirulence/virulence formula 1, 3, 26, 17, 10/2a, 2c, 9, 16, 24, 3ka, 11, 30, 18), which are common races in the USA (Kolmer et al., 2003). A preliminary screening of the recurrent parents and the Lr51 donor line indicated that race THBJ was virulent on Express but avirulent on Lr51 donor line. Race MCDS was virulent on Kern and UC1037 and was avirulent on the Lr51 donor line. Seedlings were inoculated at 7 to 8 d after planting, when the primary leaves were fully extended. For each race, an oil-spore mixture was atomized onto the seedling plants. The plants were allowed to dry, and were then placed in a dew chamber for 18 h, with no light. After incubation, the plants were placed in a greenhouse set at 18 to 21°C with supplemental metal halide lighting. Infection types were scored 12 d after inoculation by the scale in Long and Kolmer (1989).

DNA Extraction and RFLP Procedures
A large-scale DNA isolation procedure (Dvorak et al., 1988) was used for the restriction fragment length polymorphism analysis (RFLP) and to optimize the amplification conditions for PCR markers. A fast, small-scale DNA isolation procedure more appropriate for MAS (Wining and Langridge, 1991) was used to test BC and BC-F₂ populations. Procedures for Southern blots and hybridization were as described previously (Dubcovsky et al., 1994). A total of 10 low copy probes previously mapped on chromosome 1A^m from T. monococcum (Dubcovsky et al., 1996) were used to characterize the T. speltoides segment carrying the leaf rust resistance gene Lr51 (Fig. 1) .

View larger version (28K): [in this window] [in a new window]   Fig. 1. Inferred RFLP map of the translocated chromosomes in Neepawa F-7-3 and F-7-12. The T. speltoides segment is indicated in black and regions involved in additional translocations among chromosomes from homeologous group 1 are indicated in gray. The + and – signs in the right panels indicate the presence or absence of RFLP fragments from the A, B, D, and S genomes. Underlined ± signs indicate a relatively higher hybridization intensity. The order and distances among markers were inferred from a T. monococcum map including the same markers (Dubcovsky et al., 1996).

For the CAPS markers, 10 µL of the PCR amplification products were digested with restriction enzymes PstI or BamHI (Promega) by adding 5 units of enzyme to the PCR product. Samples were separated by electrophoresis in 2% (w/v) agarose gel and visualized by means of ethidium bromide and UV light.

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
Infection Types to Puccinia triticina
The presence of Lr51 in F-7-3 improved resistance to leaf rust isolates BBDL, MCDS, MDRL, MBRL, SBDB, TFGQ, and THBJ relative to the recurrent parent Neepawa (data not shown). Seedlings of the recurrent parent Express had high infection types with race THBJ, whereas Kern and UC1037 had high infection types with race MCDS (Table 3). All the plants homozygous for the T. speltoides chromosome segment carrying the Lr51 gene derived from backcrosses with Express, UC1037, and Kern, were homogeneous for very low infection types (hypersensitive flecks), similar to the Neepawa*6/Triticum speltoides F-7-3 line, the 1S#F7L translocation donor. As expected, all sister line plants lacking the T. speltoides segment were homozygous susceptible, with high infection types similar to those observed in the original parental lines (Table 3). These results demonstrate that the Lr51 gene was successfully transferred into these three recurrent parents by MAS and that Lr51 was effective in the three genetic backgrounds tested in this study.

Since the original T. speltoides F7 accession was not available, it was not possible to determine if the absence of polymorphisms in the markers flanking XAga7 and Xmwg710 was originated in the absence of the T. speltoides segment or in the lack of polymorphism between the S and B genomes. The first hypothesis is more likely, since T. speltoides is an outcrossing species with very high levels of polymorphism (Dvorak et al., 1998). Previous studies that compared the alleles present in T. speltoides populations with those present in the B genome, found that almost all RFLP loci were polymorphic using only one restriction enzyme (J. Dvorak, personal communication). Since none of the four restriction enzymes used in this study (EcoRI, BamHI, HindIII, and XbaI) detected polymorphisms for the markers flanking XAga7 and Xmwg710, we assumed this indicated that the T. speltoides segment did not extend to those flanking markers. On the basis of this assumption, the minimum and maximum estimates for the genetic length of the interstitial 1S chromosome segment were 14 cM (XAga7 and Xmwg710) and 32 cM (Xmwg984 and XksuE11), respectively (Fig. 1). These genetic distances were based on a T. monococcum map (Dubcovsky et al., 1996) that included all of the markers used in this study.

Translocations in F-7-12 were more complex than in F-7-3. Although T. speltoides bands for the XAga7 and Xmwg710 loci were found in both lines, the missing bands from the B genome extended to loci Xmwg984 and XksuG34 in F-7-12 (Fig. 1). In addition, D genome fragments were missing for all of the markers, B genome fragments showed double hybridization intensity for markers distal to the XAga7 locus, and A genome fragments showed double hybridization intensity for markers proximal to Xmwg710. The double intensity restriction fragments suggest the presence of duplicated chromosome segments. A translocation of the T. speltoides segment and its distal 1B chromosome segment to chromosome 1A, followed by a second translocation distal to XGlu-1 to chromosome 1D would explain the absence of D genome loci at both sides of T. speltoides segment and the duplicated 1A chromosome segment in the proximal region and for chromosome 1B in the distal region (Fig. 1).

The presence of complex translocations among the three homeologous group 1 chromosomes in F-7-12 could explain the limited use of this line in breeding programs. The chromosome duplications would generate multivalents during meiosis, reducing fertility and generating off type plants. In addition the large deletion in chromosome 1D may have a negative effect on agronomic or end-use quality characteristics. On the basis of these results, we decided to introgress Lr51 from the Neepawa F-7-3 line, which does not have the complex homeologous translocations found in F-7-12.

Selection of the RFLP Probe to Be Converted into a PCR Marker
Of the two RFLP loci detected within the T. speltoides chromosome segment, XAga7 has a more simple hybridization pattern compared with Xmwg710 and, therefore, was selected for conversion into a PCR marker. The XAga7 locus was detected by probe AGA7, a 1798-bp cDNA coding for the large subunit of the wheat endosperm ADP-glucose pyrophosphorylase gene (AGP2, GenBank # X14350.1, Olive et al., 1989). AGP2 homeologous genes are located on the long arms of chromosomes 1A, 1B and 1D, approximately 80 cM away from the centromere (Ainsworth et al., 1995).

The interstitial T. speltoides chromosome segment is not expected to recombine with the 1BL chromosome segment in the presence of the Ph gene and the absence of the rest of the T. speltoides chromosomes (Dvorak, 1977). Therefore, a single marker located within this segment should be sufficient to transfer the Lr51 gene into breeding lines. We tested the homozygous BC₆F₂ lines from the three recurrent parents with markers for both XAga7 and Xmwg710 loci and found no recombination between these markers or between these two markers and the Lr51 gene (Table 3). These results indicate that there was no recombination among these loci during the six generations of backcrossing and one generation of self-pollination in any of the five BC₆F₂ homozygous Lr51 lines tested (Table 3). This is equivalent to detecting complete linkage in a backcross or double haploid segregating population of 40 plants.

Sequence Analysis of the XAga7 locus
Two PCR fragments of approximately 790 and 830 bp were amplified with primers AGA7-342F and AGA7-759R (Table 2) from Neepawa, but only the 830-bp fragment was present in Neepawa-F-7-3, suggesting that the 790-bp fragment was amplified from the B genome. This hypothesis was confirmed by nullitetrasomic analysis: the 790-bp fragment was amplified in lines N1AT1B, N1DT1A but it was absent in N1BT1D (data not shown). The 830-bp fragment did not disappear in any of the three nullitetrasomic lines indicating that is likely a mixture of products from the XAga7-A and XAga7-D loci. The 830-bp fragment also was detected in PCR amplifications from DNAs of diploid T. urartu, T. tauschii, and T. speltoides accessions S3343 and S3362.

The 790-bp amplification product was cloned from Neepawa and Chinese Spring (CS) (B genome) and the 830-bp band was cloned from Neepawa-F-7-3 (expected mixture of A, D, and S products) and from the three diploid species (separate A, D, and S products). The three 790-bp B-genome clones (795 bp based on sequence) were almost identical, and only the sequence from the Neepawa B-genome clone (pNee-2, GenBank AY589012) is presented in Fig. 2 .

View larger version (96K): [in this window] [in a new window]   Fig. 2. Best-fit alignment of partial nucleotide sequences from wheat clones from the A (pNF7-17), D (pNB-25), S (pNF7-16), and B (pNee-2) genomes. Gaps were introduced to maximize nucleotide alignment and are indicated with dashes. Locations of PCR primers AGA7-342F and S30-13L are indicated with arrows and sequences from the primers are italicized. BamHI and PstI restriction sites used to develop the CAPS marker are underlined with letters in gray color. Exons are numbered from the first transcribed exon and indicated above the sequences.

Development of a Cleavage Amplified Polymorphic Sequence Marker
Primers S30-13L and AGA7-759R (Table 2) amplified preferentially alleles from the S (pNF7-16) and B (pNee-2) genomes, respectively (Fig. 2). The AGA7-759R primer is not genome-specific, but the 3' end of the S30-13L primer was selected to match a cytosine (position 38, Fig. 2) that differentiates the S and B genome alleles from the A (pNF7-17) and D (pNB-25) genome alleles. An additional polymorphism, a thymine at position 32, differentiates the S allele from the alleles in the other three genomes. The presence of this difference alone did not interfere with the amplification of the B genome allele, probably because of the internal position of the polymorphisms within the primer. PCR amplification of nullitetrasomic DNAs with these primers produced a 783-bp fragment (B-allele) in lines N1AT1B and N1DT1A but no PCR product in N1BT1D, demonstrating that these primers do not amplify the A or D genome alleles under the PCR conditions used in this study (Fig. 3 , Lanes 1, 2, and 3).

View larger version (54K): [in this window] [in a new window]   Fig. 3. Undigested and PstI digested PCR amplification products with CAPS primers S30-13L and AGA7-759R. 1-3) Chinese Spring nullisomic-tetrasomic lines. 1) N1AT1B, 2) N1BT1D, 3) N1DT1A, 4) Neepawa, 5) Neepawa*6/Triticum speltoides F-7-3. The gray arrowhead indicates the 780-bp product band from the B genome. The black arrowhead indicates the PstI digested product from the S genome. "M" indicates the molecular markers in bp (100-bp ladder, Biodynamics Corp., Seattle, WA).

View larger version (56K): [in this window] [in a new window]   Fig. 4. BamHI digestion of PCR products obtained from genomic DNAs amplified using CAPS primers S30-13L and AGA7-759R. Genomic DNAs were extracted from Neepawa (Nee) and Neepawa*6/Triticum speltoides F-7-3 (NeeF7), and from five BC6F2 plants. Letters "BS" and "SS" indicates plants heterozygous and homozygous for the presence of Lr51, respectively. Parental line Neepawa (Lane 7) is the only BB plant in this figure. The black arrowhead indicates the 819-bp PCR amplification product from the S genome allele and the gray arrowhead indicates the larger of the two BamHI digested fragments from the B genome allele of XAga7. "M" indicates the size molecular marker (100-bp ladder, Biodynamics).

View larger version (43K): [in this window] [in a new window]   Fig. 5. PstI and BamHI digestion of PCR products obtained with XAga7 CAPS primers S30-13L and AGA7-759R. Genomic DNAs were extracted from 1) Neepawa*6/Triticum speltoides F-7-3, 2) Neepawa, 3) Madsen, 4) Hyak, 5) Penawawa, 6) Buck Manantial, 7) Prointa Milenium, 8) Prointa Granar, and 9) Klein Pegaso. Gray and black arrowheads indicate amplification products from the B and S genome alleles, respectively. "M" indicates the size molecular marker (100-bp ladder, Biodynamics).

The development of molecular markers for Lr51 will facilitate combining this gene with additional leaf rust resistance genes. We are currently combining Lr51 with Lr47 and Lr37 before releasing it in a commercial cultivar. This is now possible because molecular markers are available for all three genes (Dubcovsky et al., 1998; Helguera et al., 2000, 2003). We have developed isogenic lines for Lr51, Lr47, and Lr37 in Express, Kern, and UC1037 backgrounds and are currently intercrossing the UC1037 lines to develop a single line with all three genes. An alternative strategy that can be used to extend the useful life of Lr51 is combining this gene with the slow rusting genes Lr34 and Lr46, for which molecular markers also are now available (Schnurbusch et al., 2004; Suenaga et al., 2003; William et al., 2003).

If future comparisons of the Lr51 isogenic lines reveal the presence of negative effects on yield or end-use quality associated with the introgression of the T. speltoides segment, the molecular map presented here can be used to select shorter alien chromosome segments through a second round of homeologous recombination.

	ACKNOWLEDGMENTS

 
J. Dubcovsky acknowledges financial support from USDA-CSREES competitive grant IFAFS 2001-04462. M. Helguera expresses gratitude to the Argentinean National Institute of Agricultural Technology (INTA) and to Fulbright for fellowships during this work. The authors express their gratitude to B.S. Gill, A. Graner, and M. Sorrells for supplying the RFLP clones; and especially to Dr. J. Dvorak for the Neepawa*6/Triticum speltoides F-7-3 and F-7-12 seeds and his valuable suggestions.

Received for publication April 22, 2004.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 

• Ainsworth, C., F. Hosein, M. Tarvis, F. Weir, M. Burrell, K.M. Devos, and M.D. Gale. 1995. Adenosine diphosphate glucose pyrophosphorylase genes in wheat: Differential expression and gene mapping. Planta 197:1–10.[ISI][Medline]
• Chester, K.S. 1946. The nature and prevention of the cereal rusts as exemplified in the leaf rust of wheat. Chronica Botanica, Waltham, MA.
• Dubcovsky, J., A.F. Galvez, and J. Dvorak. 1994. Comparison of the genetic organization of the early salt stress response gene system in salt-tolerant Lophopyrum elongatum and salt-sensitive wheat. Theor. Appl. Genet. 87:957–964.[ISI]
• Dubcovsky, J., M.-C. Luo, G.-Y. Zhong, R. Bransteiter, A. Desai, A. Kilian, A. Kleinhofs, and J. Dvorak. 1996. Genetic map of diploid wheat, Triticum monococcum L., and its comparison with maps of Hordeum vulgare L. Genetics 143:983–999.[Abstract]
• Dubcovsky, J., M. Echaide, E.F. Antonelli, and A.J. Lukaszewski. 1998. Molecular characterization of two Triticum speltoides interstitial translocations carrying leaf rust and green bug resistance genes. Crop Sci. 38:1655–1660.[Abstract/Free Full Text]
• Dvorak, J. 1977. Transfer of leaf rust resistance from Aegilops speltoides to Triticum aestivum. Can. J. Genet. Cytol. 19:133–141.[ISI]
• Dvorak, J., and D.R. Knott. 1980. Chromosome location of two leaf rust resistance genes transferred from Triticum speltoides to T. aestivum. Can. J. Genet. Cytol. 22:381–389.[ISI]
• Dvorak, J., P.E. McGuire, and B. Cassidy. 1988. Apparent sources of the A genomes of wheats inferred from the polymorphism in abundance and restriction fragment length of repeated nucleotide sequences. Genome 30:680–689.
• Dvorak, J., M. Luo, and Z. Yang. 1998. Restriction fragment length polymorphism and divergence in the genomic regions of high and low recombination in self-fertilizing and cross-fertilizing Aegilops species. Genetics 148:423–434.[Abstract/Free Full Text]
• Gold J., D. Harder, F. Townley-Smith, T. Aung and J. Procunier. 1999. Development of a molecular marker for rust resistance genes Sr39 and Lr35 in wheat breeding lines. Electron. J. Biotechnol. 2(1); available at http://www.scielo.cl/scielo.php?script=sci_arttext&pid=S0717-34581999000100004&lng=es&nrm=iso&tlng=en; verified 18 November 2004.
• Helguera, M., I.A. Khan, J. Kolmer, D. Lijavetzki, L. Zhong-qi, and J. Dubcovsky. 2003. PCR assays for the Lr37-Yr17-Sr38 cluster of rust resistance genes and their use to develop isogenic hard red spring wheat lines. Crop Sci. 43:1839–1847.[Abstract/Free Full Text]
• Helguera, M., I.A. Khan, and J. Dubcovsky. 2000. Development of PCR markers for wheat leaf rust resistance gene Lr47. Theor. Appl. Genet. 100:1137–1143.[ISI]
• Huang, L., and B.S. Gill. 2001. An RGA-like marker detects all known Lr21 leaf rust resistance gene family members in Aegilops tauschii and wheat. Theor. Appl. Genet. 103(6–7):1007–1013.[ISI]
• Kolmer, J.A., D.L. Long, E. Kosman, and M.E. Hughes. 2003. Physiologic specialization of Puccinia triticina on wheat in the United States in 2001. Plant Dis. 87:859–866.
• Long, D.L., and J.A. Kolmer. 1989. A North American system of nomenclature for Puccinia recondita f. sp. tritici. Phytopathology 79:525–529.[ISI]
• McIntosh, R.A., Y. Yamazaki, K.M. Devos, J. Dubcovsky, W.J. Rogers, and R. Appels. 2003. Catalogue of gene symbols for wheat. In Proceedings of the 10th International Wheat Genetics Symposium. Volume 4. Instituto Sperimentale per la Cerealicoltura, Rome, Paestum, Italy.
• Olive, M.R., R.J. Ellis, and W.W. Schuch. 1989. Isolation and nucleotide sequences of cDNA clones encoding ADP-glucose pyrophosphorylase polypeptides from wheat leaf and endosperm. Plant Mol. Biol. 12:525–538.[ISI]
• Procunier, J.D., T.F. Townley-Smith, S. Fox, S. Prashar, M. Gray, W.K. Kim, E. Czarnecki, and P.L. Dyck. 1995. PCR-based RAPD/DGGE markers linked to leaf rust resistance genes Lr29 and Lr25 in wheat (Triticum aestivum L.). J. Gene. Breed. 49:87–92.
• Schnurbusch, T., S. Paillard, A. Schori, M. Messmer, G. Schachermayr, M. Winzeler, and B. Keller. 2004. Dissection of quantitative and durable leaf rust resistance in Swiss winter wheat reveals a major resistance QTL in the Lr34 chromosomal region. Theor. Appl. Genet. 108:477–484.[ISI][Medline]
• Sears, E.R. 1954. The aneuploids of common wheat. Res. Bull. Univ. Missouri Agric. Exp. Stn. 572:1–59.
• Suenaga, K., R.P. Singh, J. Huerta-Espino, and H.M. William. 2003. Microsatellite markers for genes Lr34/Yr18 and other quantitative trait loci for leaf rust and stripe rust resistance in bread wheat. Phytopathology 93:881–890.[Medline]
• Tatusova, T.A., and T.L. Madden. 1999. Blast 2 sequences-a new tool for comparing protein and nucleotide sequences. FEMS Microbiol. Lett. 174:247–250.[ISI][Medline]
• Wining, S., and P. Langridge. 1991. Identification and mapping of polymorphism in cereals based on polymerase chain reaction. Theor. Appl. Genet. 82:209–216.[ISI]
• William, M., R.P. Singh, J. Huerta-Espino, S.O. Islas, and D. Hoisington. 2003. Molecular marker mapping of leaf rust resistance gene Lr46 and its association with stripe rust resistance gene Yr29 in wheat. Phytopathology 93:153–159.[Medline]

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