Location: Cereal Disease Lab
2018 Annual Report
Objectives
Objective 1: Monitor, collect, and characterize U.S. cereal rust pathogens.
Sub-objective 1.A. Monitor, collect, and characterize cereal rust pathogen populations in the U.S. for virulence to rust resistance genes in current cultivars.
Sub-objective 1.B. Determine levels of genetic variation in Puccinia triticina, P. graminis and P. coronata populations.
Sub-objective 1.C. Refine phylogenetics and systematics of P. graminis from Mahonia and other native Berberis spp. in North America.
Objective 2: Further develop genomic resources of cereal rust pathogens and identify fungal genes involved in pathogenicity and development.
Sub-objective 2.A. Identify effectors of P. graminis f. sp. tritici involved in fungal pathogenicity and host resistance.
Sub-objective 2.B. Develop genomic resources and tools for more detailed analysis of P. coronata.
Objective 3: Improve host resistance in cereal crops to rust pathogens through investigations in sources and genetics of rust resistance, characterization of various germplasm, and incorporation into adapted germplasm.
Sub-objective 3.A. Evaluate wheat, oat and barley germplasm from U.S. breeding programs for rust resistance.
Sub-objective 3.B. Identify and characterize new sources of rust resistance in wheat, barley, and oat; and incorporate into adapted germplasm.
Approach
Cereal rust fungi (Puccinia coronata, P. graminis, and P. triticina) are dynamic leading to constant changes in the U.S. population and erosion of effective rust resistance in cereal crops. In addition, introduction of foreign isolates, such as Ug99, further threaten cereal production. Development of cereal cultivars with effective rust resistance and management strategies of these diseases depend on monitoring, collection, virulence phenotyping, and genotypic characterization of cereal rust pathogen populations. Rust resistant cereal germplasm will be selected by testing wheat, oat, and barley lines from breeding programs throughout the U.S. and other sources for resistance to these pathogens using the prevalent races, and races that have high virulence to rust resistance genes common in released cultivars and breeding lines. Testing with selected isolates of the cereal rust pathogens and host genetics studies will identify the rust resistance genes in breeding lines and germplasm. Advanced germplasm lines with combinations of rust resistance genes will be selected and released for further use in cultivar development. Rust fungi produce a large arsenal of effector proteins in order to infect and colonize the plant host. Genetic and genomic approaches will be used to identify and characterize effector genes from P. graminis and P. coronata.
Progress Report
Progress was made on all objectives.
Objective 1: Monitor, collect, and characterize United States cereal rust pathogens.
A total of 83 samples of wheat leaf rust (Puccinia triticina) were collected or received from across the United States. These collections and others obtained later in the season will be processed for virulence phenotype (race) identification in the fall and winter of 2018-2019.
In 2017 in the United States, 65 races of P. triticina were identified. Race MBTNB with virulence to Lr1, Lr3a, Lr3ka, Lr11, Lr17, Lr30, LrB, and Lr14a was the most common race overall in the U.S. at 11.3% of isolates. This race was also predominant in the soft red winter wheat regions of the southeast and Ohio Valley states. In the soft red winter wheat area, races with virulence to Lr11 were predominant. In Kansas and Nebraska, race MBDSD with virulence to Lr1, Lr3a, Lr17, LrB, Lr10, Lr14a, and Lr39, was the most common race. Race TFTSB, with virulence to Lr2a, Lr24, Lr26, and Lr11 was the most common race in Texas and Oklahoma. In the southern-mid Great Plains region, races with virulence to Lr39 were common. In the northern spring wheat area of Minnesota, North Dakota, and South Dakota, race TNBJJ, with virulence to Lr2a, Lr9, Lr24, and Lr39 was the most common race. Race TBBGS with virulence to Lr2a, Lr21 and Lr39 was also common in this region.
Five hundred and fifty isolates of Puccinia triticina from 11 different wheat-growing regions worldwide were characterized using the genotype by sequence technology. Over 5,000 single nucleotide polymorphisms (SNPs) were found among the different isolates. The dataset is currently being analyzed to determine the evolutionary relationships between the different populations of P. triticina.
Twenty one collections of P. graminis f. sp. tritici (wheat stem rust), 23 collections of P. graminis f. sp. avenae (oat stem rust), and 3 collections of P. graminis f. sp. secalis (rye stem rust) from the United States were obtained by the USDA-ARS in St. Paul, Minnesota. Of the isolates tested thus far, all P. graminis f. sp. tritici isolates were race QFCSC and P. graminis f. sp. avenae isolates included races TJS and TGN.
A total of 159 collections of P. coronata (oat crown rust) from various regions of the United States were received at the USDA-ARS in St. Paul, Minnesota. From that sample, 250 individual isolates were purified and tested on oat differential lines carrying various resistance genes. The USDA-ARS in St. Paul, Minnesota has currently received 32 collections from various regions of the United States and are in process of characterizing the fungal population diversity.
A total of 673 isolates/samples of P. graminis f. sp. tritici were genotyped from Africa, Central Asia, Europe, Middle East and United States. Two P. graminis f. sp. tritici strains that were first observed in 2014 in collections from southeastern Europe have spread into the central Europe, Middle East and northeastern Africa.
A total of 5 collections of the barley leaf rust pathogen were received between February and May 2018. From the total of 44 collections received in 2017, 65 isolates were derived. Virulence was observed on all barley leaf rust resistance genes (Rph genes) except Rph15. Unfortunately virulence was also observed to previously resistant line Tunisia 34.
Objective 2: Further develop genomic resources of cereal rust pathogens and identify fungal genes involved in pathogenicity and development.
An additional 85 isolates of P. graminis f. sp. tritici from United States, Europe and Africa were sequenced and data analysis has begun. Increases and characterization on progeny from crosses of P. graminis f. sp. triciti has continued.
De novo genome sequence assembly and phasing of diakroytic genomes of two isolates of P. coronata was completed and published. This genome assembly was annotated using transcriptome of rust fungi collected at various time points of infection as well as fungal germination. The two isolates show different virulence patterns to the oat differential lines thus providing additional guidance on possible underlying effector genes. A total of 60 isolates (30 isolates for 1990 and 30 isolates for 2015) from the United States were sequenced and sequences are being characterized for analysis of genetic diversity and possible sources (i.e., the role of sexual vs. mutational derived variation) of pathogenicity.
Objective 3: Improve host resistance in cereal crops to rust pathogens through investigations in sources and genetics of rust resistance, characterization of various germplasm, and incorporation into adapted germplasm.
A recombinant inbred line (RIL) population of Tc*3/CI13227 had major quantitative trait loci for adult plant leaf rust resistance on chromosomes 7A and 1BL. The QTL on 1BL may be Lr46, while the QTL on 7A has not been previously designated as a leaf rust resistance gene.
A recombinant inbred line population of Thatcher/AC Taber segregated for major quantitative trait loci for leaf rust resistance on chromosomes 2B, 2D, 3B, 5B, 5D, and 7B in seedling and adult plant stages. Further analysis will be conducted to determine if any of these QTLs are new genes for leaf rust resistance.
Wheat breeding lines from the Uniform Eastern Soft Red Winter wheat nursery, the Uniform Eastern Soft Red Winter Wheat Nursery, the North Regional Performance Nursery, the Southern Regional Performance Nursery, and the Uniform Spring Wheat Nursery were tested for seedling leaf rust resistance with 10 leaf rust races. Leaf rust resistance gene postulations were made for the entries.
Wheat breeding lines and cultivars from the Kazakhstan-Siberia winter wheat program administered by CIMMYT-Ankara were tested for seedling leaf rust resistance with 10 leaf rust races. Leaf rust resistance gene postulations were made for the entries.
Winter and spring wheat breeding lines from Monsanto were tested for seedling leaf rust resistance with 10 leaf rust races. Leaf rust resistance gene postulations were made for the entries.
Backcrossing of linkage blocks of two Ug99-effective Sr genes was initiated. Marker-assisted backcrossing facilitated the generation of fixed BC4F2:3 families with or without the Sr9h-Sr28 linkage block and BC4F1 seed of the Sr15-Sr22 linkage block. Crosses generated double cross F1 plants seed for the purpose of combining additional Sr genes on chromosome 2B (Sr36, Sr39, Sr40, Sr47, Sr193883) in the background of the homozygous ph1b mutant gene that allows for homoeologous recombination. Recurrent parents used for backcrossing were obtained from the University of Minnesota, South Dakota State University, North Dakota State University, and Montana State University.
Over 750 oat breeding lines from different programs in the United States and Canada were evaluated for crown rust resistance in field plots. Additional 30 advanced oat breeding lines from the regional programs were analyzed for crown rust reaction. Nearly 328 lines from the USDA-ARS Aberdeen program were also evaluated for their adult plant resistance to oat crown rust in the buckthorn nursery. Additionally, the project at USDA-ARS in St. Paul, Minnesota is assessing the effectiveness of several adult plant resistance genes in the buckthorn for future use in the effort to pyramid and develop more durable resistant germplasm.
Selected (top 22 resistant and susceptible lines each per population) of oat recombinant inbred line populations (OtanaA/CI8000-4 and OtanaD/PI260616-1), that had been evaluated for adult plant resistance in the buckthorn nursery for several years, were genotyped using the Illumina oat 6K assay. Data analysis indicates two QTL regions per population that significantly contribute to the APR phenotype. These QTL marker associations are being verified by further genotyping and pyramided with previously identified genes to develop a pyramid of APR genes in a single line for use by the oat breeding programs in the United States.
A total of 1760 wheat breeding lines from the uniform regional nurseries, preliminary regional nurseries, and individual breeding programs from across the United States were tested with multiple stem rust races from the United States in greenhouse and in the field. Entries were also tested with races in the Ug99 races group and other races of foreign origin with significant virulence combinations. Resistance genes effective against these races were postulated. Data were provided to nursery coordinators and individual breeders, and were posted at the USDA-ARS St. Paul, Minnesota website. About 600 lines of genetic materials from ARS and university scientists, who collaborated in stem rust resistance discovery and characterization, were tested with stem rust races in greenhouse and field experiments. Contributed to the documentation of germplasm/variety releases.
Scientists at the USDA-ARS in St. Paul, Minnesota coordinated the African field assessment of spring-habit United States wheat and barley lines. A total of 488 barley lines were assessed in both Kenya and Ethiopia during February-May 2018. A total of 1950 and 3761 wheat lines were assessed in Kenya and Ethiopia, respectively. Lines included candidate cultivars, advanced breeding lines, preliminary breeding lines, and mapping populations from 8 United States Universities, USDA-ARS, Syngenta, Limagrain, and Anheuser-Busch. Data are valuable for breeders to select wheat and barley lines with field resistance to Ug99 and other emerging virulent stem rust pathogen races.
Accomplishments
1. A genetic map for leaf rust resistance gene Lr64. ARS scientists in St. Paul, Minnesota transferred a gene from wild emmer wheat (Triticum turgidum ssp. dicoccoides) to the common wheat variety Thatcher, gives resistance to a wide range of P. triticina races in seedling plants. The objective of this study was to develop a genetic map of this gene on chromosome 6BL. Gene Lr64 mapped within a region of 2.6 cM, as determined with seven single nucleotide (SNP) markers. These SNP markers were converted to KASP markers that can be used to add Lr64 to wheat breeding lines to improve leaf rust resistance in common wheat.
2. The wheat cultivar 'Duster' has the durable leaf rust resistance genes Lr46 and Lr77. The wheat cultivar 'Duster' has been widely grown in Oklahoma since release in 2006. Unlike most winter wheat cultivars, 'Duster' has had very good long lasting resistance to leaf rust. ARS scientists in St. Paul, Minnesota determined that Duster has durable leaf rust resistance genes Lr46 and Lr77. Both of these genes provide resistance in adult plant stage to many races of leaf rust and have been found in other cultivars with long lasting leaf rust resistance. A KASP marker for Lr77 can be used in wheat improvement programs to select for this gene.
3. Cloning of a wheat stem rust resistance gene from diploid wheat. Wheat stem rust is a devastating disease that is threatening global wheat production. The emergence of new virulent races of this pathogen in Africa, including the Ug99 race group, has prompted global efforts to find effective resistance genes. In collaboration with Davis, California, ARS scientists in St. Paul, Minnesota identified stem rust resistance gene Sr21 that is effective against the Ug99 race group. We developed a diagnostic marker to accelerate its deployment in wheat breeding programs and demonstrated that the introduction of two Sr21 copies in transgenic wheat results in high levels of resistance. An unusual characteristic of Sr21 is its increased resistance to stem rust at high temperatures. Identification of temperature-sensitive Sr21 will be useful for controlling the stem rust pathogen in our changing environment.
4. Identification of stem rust resistance gene combinations in United States spring wheat germplasm. Stem rust of wheat historically caused major yield losses of wheat worldwide. To understand the genetic basis of stem rust resistance in contemporary North American spring wheat, scientists at the USDA-ARS in St. Paul, Minnesota conducted genome-wide association analysis on a panel of 250 elite lines. Molecular markers strongly associated with seedling and/or field resistance to particular stem rust pathogen races were identified. At the seedling stage, the most significant marker-trait associations were detected in the regions of known major genes Sr6, Sr7a, and Sr9b. Additionally, the scientists found that over half of the panel possessed three or more Sr genes, and most commonly included various combinations of Sr6, Sr7a, Sr8a, Sr9b, Sr11, Sr12, and Sr57. Most of these genes confer resistance to specific P. graminis f. sp. tritici races accounting for the prevalent stem rust resistance in North American spring wheat.
5. A sexual population of Puccinia graminis f. sp. tritici contributed to the stem rust epidemics in northern Kazakhstan. ARS scientists in St. Paul, Minnesota analyzed stem rust isolates collected from wheat and barberry in stem rust epidemic areas in northern Kazakhstan revealing a large diversity in virulence and genotypes. This diversity can occur in a sexual population only. Thus, the alternate host in that region has played a significant role in generating new virulent races, and in stem rust epidemiology.
6. Unique virulences in P. graminis f. sp. tritici were detected. By participating global surveillance for stem rust, ARS scientists in St. Paul, Minnesota analyzed stem rust samples from international collaborators and detected unique virulences that are able to attack important resistance genes, such as Sr22, Sr32, Sr33, Sr40, Sr47, and Sr50 that that have been considered universally resistant and used worldwide for developing resistance to Ug99.
7. De novo genome sequence assembly and phasing of diakroytic genomes of Puccinia coronata. Disease management strategies to manage oat crown rust are challenged by the rapid evolution of P. coronata f. sp. avenae (Pca), which renders resistance genes in oat varieties ineffective. In spite of the economic importance of understanding Pca, resources to study the molecular mechanisms underpinning pathogenicity and emergence of new virulence traits are lacking. Such limitations are partly driven by the obligate biotrophic lifestyle of Pca as well as the dikaryotic nature of the genome, features that are also shared with other important rust pathogens. This study reports the first release of a haplotype-phased genome assembly for a dikaryotic fungal species and demonstrates the amenability of using emerging technologies to investigate genetic diversity in populations of Pca.
8. Identification, introgression, and molecular marker genetic analysis and selection of a highly effective novel oat crown rust resistance from diploid oat, Avena strigosa. A new highly effective resistance to oat crown rust (Puccinia coronata f. sp. avenae) was identified in the diploid wild oat, Avena strigosa, and introgressed into hexaploid cultivated oat. USDA-ARS scientists located in St. Paul, Minnesota discovered tightly linked molecular markers and transferred this novel adult plant oat crown rust resistance gene into adapted cultivars. This gene confers broad resistance (i.e., field resistance to a wide diversity of the pathogen population) to this devastating disease of oat making it highly valuable to scientists across the globe. Additionally, the details of this process will be of value to other plant science researchers interested in developing more durable resistant cultivars.
Review Publications
Kolmer, J.A., Chao, S., Brown Guedira, G.L., Bansal, U., Bariana, H. 2018. Adult plant leaf rust resistance derived from the soft red winter wheat cultivar Caldwell maps to chromosome 3BS. Crop Science. 58:152-158.
Miyazaki, Y., Ngoc, P., Liberatore, K.L., Kianian, S., Vladutu, C., Mori, N. 2017. Evaluation of grain dimension and weight using backcross recombinant inbred lines (BRILs) between wild and domesticated emmer wheat. Crop Research. 62:31-36.
Nazareno, E.S., Li, F., Madeleine, S., Park, R.F., Kianian, S., Figueroa, M. 2017. Puccinia coronata f. sp. avenae: a threat to global oat production. Molecular Plant Pathology. http://doi.org/10.1111/mpp.12608.
Kolmer, J.A., Bernardo, A.N., Bai, G., Hayden, M.J., Chao, S. 2018. Adult plant leaf rust resistance derived from Toropi wheat is conditioned by Lr78 and three minor QTL. Phytopathology. 108:246-253.
Aoun, M., Kolmer, J.A., Chao, S., Bulbula, W.D., Elias, E., Rouse, M.N., Acevedo, M. 2017. Inheritance and bulked segregant analysis of leaf rust and stem rust resistance genes in eight durum wheat genotypes. Phytopathology. 107:1496-1506.
Graybosch, R.A., Baenziger, S.P., Bowden, R.L., Dowell, F.E., Dykes, L., Jin, Y., Marshall, D.S., Ohm, J., Caffe-Treml, M. 2017. Release of 19 waxy winter wheat germplasm, with observations on their grain yield stability. Journal of Plant Registrations. 12(1):152-156. https://doi.org/10.3198/jpr2017.03.0018crg.
Haley, S.D., Johnson, J.J., Peairs, F.B., Stromberger, J.A., Hudson-Arns, E.E., Seifert, S.A., Anderson, V.A., Rosenow, A.A., Bai, G., Chen, X., Bowden, R.L., Jin, Y., Kolmer, J.A., Chen, M., Seabourn, B.W. 2018. Registration of 'Langin' hard red winter wheat. Journal of Plant Registrations. 12:232-236. https://doi.org/10.3198/jpr2017.11.0082crc.
Hiebert, C.W., Rouse, M.N., Jayaveeramuthu, N., Fetch, T. 2016. Genetic mapping of stem rust resistance to Puccinia graminis f. sp. tritici race TRTTF in the Canadian wheat cultivar 'Harvest'. Phytopathology. 107:192-197.
Johnson, J.W., Chen, Z., Buck, J.W., Buntin, G.D., Babar, M.A., Mason, R.E., Harrison, S.A., Murphy, J.P., Ibrahim, A.M., Sutton, R.L., Simoneaux, B.E., Bockelman, H.E., Baik, B-K., Marshall, D.S., Cowger, C., Brown Guedira, G.L., Kolmer, J.A., Jin, Y., Chen, X., Cambron, S.E., Mergoum, M. 2018. ‘Savoy’: An adapted soft red winter wheat cultivar for Georgia and the South East regions of the USA. Journal of Plant Registrations. 12:85-89.
Mourad, A.M., Sallam, A., Belamkar, V., Wegulo, S., Bowden, R.L., Jin, Y., Mahdy, E., Bakheit, B., El-Wafaa, A., Poland, J., Baenziger, P.S. 2018. Genome-wide association study for identification and validation of novel SNP markers for Sr6 stem rust resistance gene in bread wheat. Frontiers in Plant Science. 9:380. https://doi.org/10.3389/fpls.2018.00380.
Nirmala, J., Saini, J., Newcomb, M., Olivera, P., Gale, S.W., Klindworth, D.L., Elias, E., Talbert, L., Chao, S., Faris, J.D., Xu, S.S., Jin, Y., Rouse, M.N. 2017. Discovery of a novel stem rust resistance allele in durum wheat that exhibits differential reactions to Ug99 isolates. G3, Genes/Genomes/Genetics. https://doi.org/10.1534/g3.117.300209.
Rutter, W.B., Salcedo, A., Akhunova, A., Wang, S., Bolus, S., Chao, S., Rouse, M.N., Szabo, L.J., Bowden, R.L., Akhunov, E., Dubcovsky, J. 2017. Variation in the AvrSr35 effector determines Sr35 resistance against wheat stem rust race Ug99. Science. 358(6370):1604-1606. https://doi:10.1126/science.aao7294.
Zhang, W., Chen, S., Abate, Z., Nirmala, J., Rouse, M.N., Dubcovsky, J. 2017. Identification and characterization of Sr13, a tetraploid wheat gene that confers resistance to the Ug99 stem rust race group. Proceedings of the National Academy of Sciences. http://www.pnas.org/cgi/doi/10.1073/pnas.1706277114.
Zurn, J.D., Rouse, M.N., Chao, S., Aoun, M., Macharia, G., Hiebert, C.W., Pretorius, Z.A., Bonman, J.M., Acevedo, M. 2018. Dissection of the multigenic wheat stem rust resistance present in the Montenegrin spring wheat accession PI 362698. BMC Genomics. 19:67. https://doi.org/10.1186/s12864-018-4438-y.
Gao, L., Rouse, M.N., Mihalyov, P.D., Bulli, P., Pumphrey, M.0., Anderson, J.A. 2017. Genetic characterization of stem rust resistance in a global spring wheat germplasm collection. Crop Science. 57:1-15.
Barnes, C.W., Ordóñez, M.E., Hambleton, S., Dadej, K., Szabo, L.J., Fetch, T.G. 2018. Detection of wheat stem rust race RRTTF in Ecuador in 2016. Plant Disease. 102(2)448. https://doi.org/10.1094/PDIS-08-17-1161-PDN.
Chen, S., Zhang, W., Bolus, S., Rouse, M.N., Dubcovsky, J. 2018. Identification and characterization of wheat stem rust resistance gene Sr21 effective against the Ug99 race group at high temperature. PLoS Genetics. 14(4):e1007287. https://doi.org/10.1371/journal.pgen.1007287.
Edae, E.A., Pumphrey, M.O., Rouse, M.N. 2018. A genome-wide association study of field and seedling response to stem rust pathogen races reveals combinations of race-specific resistance genes in North American spring wheat. Frontiers in Plant Science. https://doi.org/10.3389/fpls.2018.00052.
Flath, K., Miedaner, T., Olivera Firpo, P., Rouse, M.N., Jin, Y. 2018. Genes for wheat stem rust postulated in German cultivars in seedling stage and their resistance in adult-plant field tests. Plant Breeding. 137:301-312. https://doi.org/10.1111/pbr.12591.
Marais, G.F., McCallum, B., Kolmer, J.A., Pirseyedi, S., Bisek, B.R., Somo, M. 2018. Registration of spring wheat sources of the resistance genes Lr53, Lr56, Lr59 and Lr62. Journal of Plant Registrations. 12:157-161.
Rines, H.W., Miller, M.E., Carson, M.L., Chao, S., Tiede, T., Wiersma, J., Kianian, S. 2017. Identification, introgression, and molecular marker genetic analysis and selection of a highly effective novel oat crown rust resistance from diploid oat, Avena strigosa. Theoretical and Applied Genetics. 131(3):721-733. http://doi.org/10.1007/s00122-017-3031-0.
Anderson, J.A., Wiersma, J.J., Linkert, G.L., Reynolds, S., Kolmer, J.A., Jin, Y., Rouse, M.N., Dill-Macky, R., Hareland, G.A., Ohm, J.-B. 2018. Registration of 'Linkert' spring wheat with good straw strength and adult plant resistance to the Ug99 family of stem rust races. Journal of Plant Registrations. 12(2):208-214. http://doi.org/10.3198/jpr2017.07.0046crc.
Anderson, J.A., Wiersma, J.J., Linkert, G.L., Reynolds, S., Kolmer, J.A., Jin, Y., Rouse, M.N., Dill-Macky, R., Hareland, G.A., Ohm, J.-B. 2018. Registration of 'Norden' hard red spring wheat. Journal of Plant Registrations. 12(1):90-96. http://doi.org/10.3198/jpr2017.07.0045crc.
Anderson, J.A., Wiersma, J.J., Linkert, G.L., Reynolds, S., Kolmer, J.A., Jin, Y., Rouse, M.N., Dill-Macky, R., Hareland, G.A., Ohm, J.-B. 2018. Registration of 'Bolles' hard red spring wheat with high grain protein concentration and superior baking quality. Journal of Plant Registrations. 12(2):215-221. http://doi.org/10.3198/jpr2017.08.0050crc.
Chen, S., Guo, Y., Briggs, J., Dubach, F., Chao, S., Zhang, W., Rouse, M.N., Dubcovsky, J. 2017. Mapping and characterization of wheat stem rust resistance genes SrTm5 and Sr60 from Triticum monococcum. Theoretical and Applied Genetics. 131(3):625-635. https://doi.org/10.1007/s00122-017-3024-z.
Saini, J., Faris, J.D., Zhang, Q., Rouse, M.N., Jin, Y., Long, Y., Klindworth, D.L., Elias, E.M., McClean, P.E., Edwards, M.C., Xu, S.S. 2018. Identification, mapping, and marker development of stem rust resistance genes in durum wheat 'Lebsock'. Molecular Breeding. 38:77. https://doi.org/10.1007/s11032-018-0833-y.
Muleta, K.T., Rouse, M.N., Rynearson, S., Chen, X., Buta, B.G., Pumphrey, M. 2017. Characterization of molecular diversity and genome-wide mapping of loci associated with resistance to stripe rust and stem rust in Ethiopian bread wheat accessions. Biomed Central (BMC) Plant Biology. https://doi.org/10.1186/s12870-017-1082-7.
