Research Project: Cereal Rust: Pathogen Biology and Host Resistance

Location: Cereal Disease Lab

2019 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
In the second full year of the project, USDA-ARS scientists located in St. Paul, Minnesota, made progress in the following objectives: Objective 1: Monitor, collect, and characterize U.S. cereal rust pathogens. In 2018, 32 races of P. triticina were identified from 238 isolates. Race MNPSD with virulence to Lr1, Lr3a, Lr9, Lr24, Lr3ka, Lr11, Lr17, Lr30, LrB, Lr14a, and Lr39 was the most common race overall in the United States at 35% of isolates. This race was predominant in the Great Plains region where hard red winter wheat and spring is grown. In the soft red winter wheat area, race MBTNS with virulence to Lr11 was predominant. In the mid-southern Great Plains region races with virulence to Lr9, Lr24, Lr37, and Lr39 were common. In the northern spring wheat area of Minnesota, North Dakota, and South Dakota, race TBBGS with virulence to Lr2a, Lr21 and Lr39 was common. In 2018 and in past years, the predominant races of Puccinia triticina in the different regions were highly virulent to the cultivars with the leaf rust resistance genes characteristic of that wheat market class, which indicated the continual selection for additional virulence in the P. triticina population by leaf rust resistance genes in the host population. As of 2018, all deployed race-specific leaf rust resistance genes in U.S. wheat cultivars had selected virulent races of P. triticina. As of June 3, 2019, 92 samples of wheat leaf rust collected from across the United States have been received at the USDA-ARS research facility located in St. Paul, Minnesota. These collections and others obtained in July and August will be processed for virulence phenotype (race) identification in the fall and winter of 2019-2020. In FY18, a total of 108 isolates derived from 37 stem rust samples from wheat and barley were analyzed. Race QFCSC continues to be the dominant race in the Great Plains. Stem rust was not observed in the Midwest region during this timeframe. Race QFCNC was detected for the first time from a barley stem rust sample collected in northern MN. Diverse races (8 in total) were identified from barley stem rust samples collected in Corvallis, Oregon, indicating that sexual cycle on the alternate hosts may have played a role in generating these races. A total of 6 races were identified from 24 oat stem rust samples collected from six states. Races TGN and TJS were the dominant races. A novel race, TGG, was found for the first time in a sample from NY. A total of 300 international stem rust samples were analyzed. The government shutdown severely impacted this work. New variants in the Ug99 race group were detected in samples from Kenya, attacking resistance gene Sr8155B1, an important gene for breeding germplasm and released varieties for stem rust resistance. Novel and significant virulence combinations were also identified in samples from Spain and Georgia. In 2018, a total of 41 collections of P. coronata (oat crown rust) from various regions of the U.S. were received. From that sample 42 individual isolates were purified and tested on the oat differential lines carrying various resistance genes. To date, we have received 19 collections in 2019 from various regions of the U.S. and are in process of characterizing the fungal population diversity. A total of 2 collections of the barley leaf rust pathogen (Puccinia hordei) were received between February and May of 2018. From the total of 11 collections received in 2018, 25 isolates were derived. A total of 585 isolates/samples of P. graminis f. sp. tritici (Pgt) were genotyped from Africa, Central Asia, Europe, Middle East, and the United States. A continued spread of highly virulent races of Pgt in the Middle East and northeastern Africa was observed. Progress was made on developing DNA based tools for P. graminis continues. A molecular assay based a set of 16 SNP markers was developed for monitoring the nine predominant North American race/race groups. Six U.S. isolates of Pga were sequenced as part of study of the P. graminis species complex. Data analysis has begun. Elongation Factor 1-alpha gene was sequenced from 55 isolates of Pgt, five isolates of Pgs and 10 isolates of Pga. Nine distinct alleles have been identified. Success rate of genotyping herbarium samples of P. graminis with either Pgt SNP chip or by sequencing has been very low. Objective 2: Further develop genomic resources of cereal rust pathogens and identify fungal genes involved in pathogenicity and development. An additional 30 isolates of Pgt from natural sexual populations in the Pacific Northwest have been increased, race phenotyped and genotyped. SNP assay developed for North American Pgt isolates was used to check for contamination of common isolates. Mapping effector genes in Pgt has been hampered by problems with assembling complete genetic map. Fifty additional isolates were increased, checked for purity and race phenotyped. This has resulted in a significant delay in mapping and identifying effector genes. A total of 60 isolates (30 for 1990 and 30 for 2015) of P. coronata from the United States were sequenced for analysis of genetic diversity and possible sources of pathogenicity. Results indicate that the 2015 population is substantially more virulent than that of 1990. Additionally, there has been a drastic genetic shift in the population from 1990 to 2015. Both populations show high genetic diversity and admixture, and low levels of differentiation at a regional level. There are reduced levels of linkage disequilibrium and clonality in regions with buckthorn. Utilizing the genomic data, a candidate for a fungal effector gene has been identified displaying a presence/absence variation and evidence of selective sweep. 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. Wheat breeding lines from the 2019 uniform regional nurseries (UESR, USSR, NRPN, SRPN, and URN) were tested for seedling leaf rust resistance with 11 leaf rust races. Leaf rust resistance gene postulations were made for the entries and the results communicated to the nursery coordinators. Winter and spring wheat breeding lines from a commercial collaborator were tested for seedling leaf rust resistance with 10 leaf rust races. Leaf rust resistance gene postulations were made for the entries. Double haploid populations of Linkert x LMPG6 and Linkert x Foremost have been evaluated for leaf rust resistance in field plots and in seedling greenhouse tests. The segregating leaf rust resistance genes will be mapped using 90K SNP wheat chip. A total of 1760 elite breeding lines from public and private wheat breeding programs in the United States were screened with 9 domestic and 7 foreign stem rust races at the seedling stage and with 5 domestic races in field stem rust nursery. Resistance genes, especially those effective against Ug99 and other foreign races with significant virulence combinations, were postulated. Data was promptly distributed to collaborators. Over 388 oat breeding lines from different programs in the United States and Canada were evaluated for crown rust resistance in field plots. An additional 138 advanced oat breeding lines from the regional programs were analyzed for crown rust reaction. Nearly 487 lines from a USDA-ARS facility located in Aberdeen, Idaho, were also evaluated for adult plant resistance to oat crown rust in the buckthorn nursery. Additionally, we are 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. Analysis of five different oat recombinant inbred line populations has yielded several strong QTL loci explaining from 30% to 50% of phenotypic variance for adult plant crown rust resistance. Easy to use PCR based markers (KASP) have been developed flanking these QTL regions. These markers were used to further validate and verify the significance of these genomic regions. A program to pyramid 4 of these regions has been initiated to combine their influence in a single line for use by the various breeding programs. Wheat lines, with and without the Sr9h-Sr28 linkage block, were increased for one generation in the greenhouse and planted as a field increase in the spring of 2019. Marker-assisted backcrossing facilitated the generation of fixed BC4F2:3 families with or without the Sr15-Sr22 linkage block. Seed of advanced lines with Sr15-Sr22 were distributed to spring wheat breeders. Combining of additional Sr genes on chromosome 2B (Sr36, Sr39, Sr40, Sr47, Sr193883) in the background of the homozygous ph1b mutant gene allowed 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. A total of 1657 wheat lines and 233 barley lines were assessed in Kenya and Ethiopia. Lines included candidate cultivars, advanced breeding lines, preliminary breeding lines, and mapping populations from USDA-ARS, universities throughout the U.S, and private breeding programs.

Accomplishments
1. A genetic map for a leaf rust resistance gene on chromosome 1DS. ARS scientists located in St. Paul, Minnesota, have identified a gene on the short arm of chromosome 1D of wheat present in the Thatcher line RL6149, which was mapped using molecular (SNP-KASP, single nucleotide polymorphism-kompetitive allele specific) markers. This gene conditions resistance to a wide range of Puccinia triticina races currently found in the United States, and may be a previously uncharacterized leaf rust resistance gene. A KASP marker mapped within 0.6cM to the gene can be used to add this resistance gene to wheat breeding lines to improve leaf rust resistance in common wheat.

2. The wheat cultivar AC Taber with durable leaf rust resistance has leaf rust resistance genes that map to chromosomes 2BS and 3BS. ARS scientists located in St. Paul, Minnesota, used a recombinant inbred line population of Thatcher/AC Taber segregated for major quantitative trait loci (QTL) for leaf rust resistance in field plot tests on chromosomes 2BS and 3BS. The QTL on 2BS is Lr13, and the QTL on 3BS mapped on the same chromosome arm as Lr74. The QTL on 3BS is a relatively new source of long-lasting resistance to leaf rust. KASP (kompetitive allele specific) markers developed for SNP (single nucleotide polymorphism) markers in the 3BS region can be used by wheat breeders and pathologists to select wheat breeding lines with this adult plant durable resistance gene.

3. Population genomics of a world-wide collection of Puccinia triticina reveal long distance migration. ARS scientists located in St. Paul, Minnesota, utilized a collection of 565 Puccinia triticina isolates from 11 world-wide wheat growing regions was genotyped using the Sequence Based Genotyping technique. The regional populations were analyzed for nucleotide variation and genetic relationships using 6745 SNPs (single nucleotide polymorphisms) across 1104 contigs. Populations from Russia and Central Asia, North and South America, Europe and Pakistan, and New Zealand and South Africa were highly related for SNP genotypes. Isolates from durum wheat found around the world were highly different for SNP genotype compared to all isolates that originated from common wheat. Specific isolates from Ethiopia collected from durum wheat were unrelated to any isolates from durum or common wheat. Recent isolates from Europe, North America, South America, Ethiopia, and Pakistan with virulence to Lr17a, and avirulent to Lr2a were highly related for SNP genotype which indicated migration of these races and SNP genotypes across global regions. A molecular clock phylogenetic approach, based on SNP variation between isolate genotype groups and mutation rate determined that isolates from Ethiopia with virulence only to durum wheat are the oldest form of P. triticina on wheat, followed by isolates found worldwide with virulence to durum wheat, and then isolates with virulence to common wheat. This finding should help develop a more effective plan to combat this disease pathogen in wheat.

4. Identification of wheat breeding lines with resistance to new virulent stem rust pathogen races in Ethiopia. Virulent races of the stem rust pathogen in addition to Ug99 have rapidly spread throughout Ethiopia. ARS scientists in St. Paul, Minnesota, led the identification of international wheat breeding lines with resistance effective to the most virulent stem rust pathogen races in Ethiopia. The work was facilitated by the implementation of single-race field nurseries in Ethiopia in collaboration with CIMMYT (International Maize and Wheat Improvement Center) and the Ethiopian Institute of Agricultural Research. Three wheat lines including 'Kingbird' were identified that possessed adult plant resistance and significantly greater resistance than the widely deployed variety 'Danda'a' in Ethiopia. Deployment of these genes in improved wheat cultivars should provide for more durable resistance.

5. Identification of new sources of resistance to wheat stem rust in Aegilops spp. in the tertiary genepool of wheat. Stem rust reaction in wild wheat relatives (Aegilops species) considered as the tertiary genepool were investigated to identify novel sources of resistance to virulent stem rust races, including Ug99, to increase the diversity of plant genes utilized. We evaluated 1,422 accessions of Aegilops spp. for resistance to three highly virulent races of Puccinia graminis f. sp. tritici. Species studied include Ae. biuncialis, Ae. caudata, Ae. comosa, Ae. cylindrica, Ae. geniculata, Ae. neglecta, Ae. peregrina, Ae. triuncialis, and Ae. umbellulata that do not share common genomes with cultivated wheat. High frequencies of resistance were observed, and the resistance genes effective against multiple races. These sources of resistance will be valuable in wheat improvement for stem rust resistance.

6. Presence of a sexual population of Puccinia graminis f. sp. tritici in Georgia provides a hotspot for genotypic and phenotypic diversity. In global surveillance for new virulence in stem rust populations, scientists located in St. Paul, Minnesota, analyzed 68 wheat stem rust samples collected between 2013 and 2015 from Georgia where stem rust is known for frequent observation of stem rust infection in wheat fields and having the alternate host (common Barberry). This study was to understand the potential roles that the alternate host may play in pathogen variations and disease epidemiology. Virulence analyses identified 25 races, many of which were detected for the first time. Novel virulence combinations and diverse genotypes pose new challenges to breeding. The virulence and genotypic diversity strongly indicate that the stem rust pathogen population in Georgia is sexual.

7. Wheat stem rust pathogen population in Jordan. Wheat is an important crop in Jordan, but little is known about the wheat stem rust population and how it compares to the Middle East and northeastern Africa. USDA-ARS scientists located in St. Paul, Minnesota, lead an effort with scientists in Jordan to characterize the wheat stem rust population from collections made in 2018. Five races of the wheat stem rust pathogen were described. These races can defeat most of the common stem rust resistance genes. Genotyping using SNP (single nucleotide polymorphism) markers identified five genotypes which have been recently found in Central Asia, Middle East and Northeast Africa and indicate that Jordan is part of larger regional wheat stem rust population that is undergoing regular population shifts. This finding is critical in better understanding the movement of this pathogen across the globe and how it would impact the United States wheat crops.

8. Oat crown rust virulence in the United States has increased dramatically. ARS scientists located in St. Paul, Minnesota, have identified 60 oat crown rust isolates (30 isolates for 1990 and 30 isolates for 2015) from the United States indicating a significant increase in virulence of this pathogen over the time period. This increase has now made many of the previously used single gene seedling resistance ineffective. There has been a drastic genetic shift in the population from 1990 to 2015, both in terms of virulence and genetic makeup. Both populations show high genetic diversity and admixture, and low levels of differentiation at a regional level. There are reduced levels of linkage disequilibrium and clonality in regions with buckthorn. Utilizing the genomic data, a candidate for a fungal effector gene has been identified from this study displaying a presence/absence variation and evidence of selective sweep. This finding indicates the vulnerability of current oat varieties grown across the United States and the need for additional research to identify more resistance genes to combat this devastating disease.

Review Publications
Miller, M.E., Zhang, Y., Omidvar, V., Sperschneider, J., Schwessinger, B., Raley, C., Palmer, J.M., Garnica, D., Upadhyaya, N., Rathjen, J., Tayler, J., Park, R.F., Dodds, P.N., Hirsch, C., Kianian, S., Figueroa, M. 2018. De novo assembly and phasing of dikaryotic genomes from two isolates of Puccinia coronata f. sp. avenae, the causal agent of oat crown rust. mBio. 9(1):1-21. https://doi: 10.1128/mBio.01650-17.
Moghimi, A., Yang, C., Miller, M.E., Kianian, S., Marchetto, P.M. 2018. A novel approach to assess salt stress tolerance in wheat using hyperspectral imaging. Frontiers in Plant Science. 9(1182). https://doi.org/10.3389/fpls.2018.01182.
Olivera, P., Rouse, M.N., Jin, Y. 2019. Identification of new sources of resistance to wheat stem rust in Aegilops spp. in the tertiary genepool of wheat. Frontiers in Plant Science. 9:1719. https://doi.org/10.3389/fpls.2018.01719.
Arora, S., Steuernagel, B., Chandramohan, S., Long, Y., Matny, O., Johnson, R., Periyannan, S., Hatta, M.A., Szabo, L.J., Xu, S.S., Wulff, B.B. 2019. Resistance gene discovery and cloning by sequence capture and association genetics. Nature Biotechnology. 37(2):139-143. https://doi.org/10.1038/s41587-018-0007-9.
Hiebert, C.W., Kassa, M.T., McCartney, C.A., You, F.A., Rouse, M.N., Fobert, P., Fetch, T.G. 2017. Genetics and mapping of seedling resistance to Ug99 stem rust in the winter wheat cultivar Triumph 64 and differentiation of SrTmp, SrCad, and Sr42. Theoretical and Applied Genetics. 129:2171-2177.
Kiszonas, A., Higgenbotham, R., Chen, X., Garland-Campbell, K.A., Bosque-Perez, N.A., Pumphrey, M., Rouse, M.N., Hole, D., Wen, N., Morris, C.F. 2019. Agronomic traits in durum wheat germplasm possessing puroindoline genes. Agronomy Journal. 111(3):1254-1265. https://doi.org/10.2134/agronj2018.08.0534.
Della Coletta, R., Hirsch, C.N., Rouse, M.N., Lorenz, A., Garvin, D.F. 2019. Genetic dissection of nonhost resistance to wheat stem rust in Brachypodium distachyon. Molecular Plant-Microbe Interactions. 32(4):392-400. https://doi.org/10.1094/MPMI-08-18-0220-R.
Anderson, J.A., Wiersma, J.J., Reynolds, S.K., Caspers, R., Linkert, G.L., Kolmer, J.A., Jin, Y., Rouse, M.N., Dykes, L., Ohm, J. 2019. Registration of 'Shelly' hard red spring wheat. Journal of Plant Registrations. 13(2):199-206. https://doi.org/10.3198/jpr2018.07.0049crc.
Kolmer, J.A., Hughes, M.E. 2017. Physiologic specialization of Puccinia triticina on wheat in the United States in 2015. Plant Disease. 101:1568-1973.
Kolmer, J.A. 2017. Genetics of leaf rust resistance in the hard red winter wheat cultivars Santa Fe and Duster. Crop Science. 57:2500-2505.
Kolmer, J.A., Hughes, M.E. 2018. Physiologic specialization of Puccinia triticina on wheat in the United States in 2016. Plant Disease. 102(6):1066-1071. https://doi.org/10.1094/PDIS-11-17-1701-SR.
Kolmer, J.A., Zhi, S., Bernardo, A.N., Hayden, M.J., Chao, S. 2018. Mapping and characterization of the new adult plant leaf rust resistance gene Lr77 derived from Santa Fe winter wheat. Journal of Theoretical and Applied Genetics. 131(7):1553-1560. https://doi.org/10.1007/s00122-018-3097-3.
Kolmer, J.A., Garvin, D.F., Hayden, M., Spielmeyer, W. 2018. Adult plant leaf rust resistance derived from the wheat landrace cultivar Americano 44d is conditioned by interaction of three QTL. Euphytica. 214:59. http://doi.org/10.1007/s10681-018-2141-3.
Kolmer, J.A., Su, Z., Bernardo, A., Bai, G., Chao, S. 2018. A backcross line of Thatcher wheat with adult plant leaf rust resistance derived from Duster wheat has Lr46 and Lr77. Phytopathology. https://doi.org/10.1094/phyto-06-18-0184-r.
Ando, K., Krishnan, V., Rouse, M.N., Danilova, T., Friebe, B., See, D.R., Pumphrey, M. 2019. Introgression of a novel Ug99-effective stem rust resistance gene into wheat and development of Dasypyrum villosum chromosome specific markers via genotyping-by-sequencing (GBS). Plant Disease. https://doi.org/10.1094/PDIS-05-18-0831-RE.
Hundie, B., Girma, B., Tadesse, Z., Edae, E., Olivera, P., Abera, E.H., Bulbula, W.D., Abeyo, B., Badebo, A., Cisar, G., Brown Guedira, G.L., Gale, S.W., Jin, Y., Rouse, M.N. 2019. Characterization of Ethiopian wheat germplasm for resistance to four Puccinia graminis f. sp. tritici races facilitated by single race nurseries. Plant Disease. https://doi.org/10.1094/PDIS-07-18-1243-RE.
Randhawa, M.S., Sing, R.P., Dreisigacker, S., Bhavani, S., Huerta-Espino, J., Rouse, M.N., Nirmala, J., Sandoval-Sanchez, M. 2018. Identification and validation of a common stem rust resistance locus in two bi-parental populations. Frontiers in Plant Science. https://doi.org/10.3389/fpls.2018.01788.
Kolmer, J.A. 2019. Virulence of Puccinia triticina, the wheat leaf rust fungus, in the United States in 2017. Plant Disease. https://doi.org/10.1094/PDIS-09-18-1638-SR.
Gao, L., Babiker, E.M., Nava, I.C., Nirmala, J., Bedo, Z., Lang, L., Chao, S., Gale, S.W., Jin, Y., Anderson, J.A., Bansal, U., Park, R.F., Rouse, M.N., Bonman, J.M., Bariana, H. 2018. Temperature-sensitive wheat stem rust resistance gene Sr15 is effective against Puccinia graminis f. sp. tritici race TTKSK. Plant Pathology. http://doi.org/10.1111/ppa.12928.
Qureshi, N., Bariana, H., Kolmer, J.A., Miah, H., Urmil, B. 2017. Genetic and molecular characterization of leaf rust resistance in two durum landraces against the durum-specific Puccinia triticina races. Phytopathology. 107:1381-1387.
Rahmatov, M., Otambekova, M., Huminjanov, H., Rouse, M.N., Otambekova, M., Nazari, K., Steffenson, B.J., Johansson, E. 2019. Characterization of stem, stripe, and leaf rust resistance in Tajik bread wheat accessions. Euphytica. 215:15. https://doi.org/10.1007/s10681-019-2377-6.
Xue, S., Kolmer, J.A., Wang, S., Yan, L. 2018. Mapping of leaf rust resistance genes and molecular characterization of the 2NS/2AS translocation in the wheat cultivar 'Jagger'. G3, Genes/Genomes/Genetics. https://doi.org/10.1534/g3.118.200058.
Omidvar, V., Dugyala, S., Li, F., Rottschaefer, S.M., Miller, M.E., Ayliffe, M.A., Moscou, M.J., Kianian, S., Figueroa, M. 2018. Detection of race-specific resistance against Puccinia coronata f. sp. avenae in Brachypodium species. Phytopathology. 108(12):1443-1454. https://doi.org/10.1094/phyto-03-18-0084-r.
Kolmer, J.A., Jin, Y., Hughes, M.E. 2017. Wheat rusts in the United States in 2016. Wheat Newsletter. 63:74.
Bartaula, R., Melo, A., Connolly, B., Jin, Y., Hale, I. 2018. An interspecific barberry hybrid enables genetic dissection of non-host resistance to the wheat stem rust pathogen. Journal of Experimental Botany. 69:2483-2493. https://doi.org/10.1093/jxb/ery066.
Chen, J., Upadhyaya, N.M., Ortiz, D., Sperschneider, J., Li, F., Bouton, C., Breen, S., Dong, C., Xu, B., Zhang, X., Mago, R., Newell, K., Xia, X., Bernoux, M., Taylor, J.M., Steffenson, B.J., Jin, Y., Zhang, P., Kanyuka, K., Figueroa, M., Ellis, J.G., Park, R.F., Dodds, P.N. 2017. Somatic recombination in wheat stem rust leads to virulence for Ug99-effective SR50 resistance. Science. 358:1607-1610.
Kolmer, J.A., Ordonez, M.E., German, S., Morgounov, A., Pretorius, Z., Visser, B., Goyeau, H., Anikster, Y., Acevedo, M. 2019. Multilocus genotypes of the wheat leaf rust fungus Puccinia triticina in worldwide regions indicate past and current long distance migration. Phytopathology. https://doi.org/10.1094/phyto-10-18-0411-r.