Research Project: Improving Control of Stripe Rusts of Wheat and Barley through Characterization of Pathogen Populations and Enhancement of Host Resistance

Location: Wheat Health, Genetics, and Quality Research

2021 Annual Report

Objectives
Stripe rust is one of the most important diseases of wheat throughout the U.S. and stripe rust of barley causes significant yield losses in western U.S. Significant progress has been made in understanding biology of the pathogen, virulence compositions of the pathogen population, identification of new sources of resistance, disease forecasting, and control of the disease using fungicides. However, research is needed to develop more effective strategies for sustainable control of stripe rusts. Therefore, this project has the following objectives for the next five years: Objective 1: Monitor and characterize stripe rust pathogen populations for providing essential information to growers for implementing appropriate measures to reduce damage on wheat and barley. Subobjective 1A: Identify virulent races of stripe rust pathogens to determine effectiveness of resistance genes in wheat and barley. Subobjective 1B: Develop molecular markers and characterize stripe rust pathogen populations to identify factors and mechanisms of pathogen dynamics for developing new management strategies. Objective 2: Enhance resistance in wheat and barley cultivars for sustainable control of stripe rusts. Subobjective 2A: Identify and map new genes for stripe rust resistance, and develop new germplasm for use in breeding programs. Subobjective 2B: Screen breeding lines for supporting breeding programs to develop wheat and barley cultivars with adequate and durable resistance to stripe rust. Accomplishment of these objectives will lead to improved knowledge of the disease epidemiology for developing more effective control strategies, more resistance genes and resistant germplasm to be used by breeders to develop stripe rust resistant wheat and barley cultivars, and more effective technology to be used by wheat and barley growers to achieve sustainable control of stripe rust.

Approach
Monitoring the prevalence, severity, and distribution of stripe rust and identify races of the pathogens, commercial fields, monitoring nurseries, trap plots, and experimental plots of wheat and barley, as well as wild grasses, will be surveyed during the plant growing-season. Recommendations will be made based on stripe rust forecasts and survey data to control stripe rust on a yearly basis. Rust samples will be collected by collaborators and ourselves during surveys and data-recording of commercial fields, experimental plots, and monitoring nurseries. Stripe rust samples will be tested in our laboratory for race identification. New races will be tested on genetic stocks, commercial cultivars, and breeding lines to determine their impact on germplasm and production of wheat and barley. Isolates of stripe rust pathogens will also be characterized using various molecular markers to determine population structure changes. To identify new genes for resistance to stripe rust in wheat, the mapping populations, which have been and will be developed in our laboratory, will be phenotyped for response to stripe rust in fields and/or greenhouse and genotyped using different approaches and marker techniques such as simple sequence repeat (SSR), single-nucleotide polymorphism (SNP), and /or genotyping by sequencing (GBS) markers. Linkage maps will be constructed with the genotype data using software Mapmaker and JoinMap. Genes conferring qualitative resistance will be mapped using the phenotypic and genotypic data using JoinMap or MapDisto, and quantitative trait locus (QTL) mapping will be conducted using the composite interval mapping program in the WinQTL Cartographer software. Relationships of genes or QTL to previous reported stripe rust genes will be determined based on chromosomal locations of tightly linked markers, type of resistance and race spectra, and origins of the resistance gene donors. Allelism tests will be conducted with crosses made between lines with potentially new gene with previously reported genes in the same chromosomal arms to confirm the new genes. A homozygous line carrying a identified new gene with improved plant type and agronomic traits will be selected from the progeny population using both rust testing and molecular markers. Lines with combinations of two genes in a same chromosome will be selected and confirmed using phenotypic and marker data. The new germplasm lines will be provided to breeding programs for developing resistant cultivars. To support breeding programs for developing cultivars with stripe rust resistance, wheat and barley nurseries will be evaluated in two locations: Pullman (eastern Washington) and Mount Vernon (western Washington) under natural infection of the stripe rust pathogens. Variety trials and uniform regional nurseries will also be tested in seedling and adult-plant stages with selected races of the stripe rust pathogen under controlled greenhouse conditions. The data will be provided to breeding programs for releasing new cultivars with adequate level and potentially durable stripe rust resistance.

Progress Report
Progress was made on the two objectives and four sub-objectives, all of which fall under National Program 303 Plant Diseases. Under Sub-objective 1A, ARS scientists in Pullman, Washington, completed all tests for identifying races from the stripe rust collections in the United States in 2020, and reported the results to the cereal community of researchers, developers, and growers. During the 2021 growing season, they conducted field surveys, made recommendations for control of stripe rust, and collected stripe rust samples in the Pacific Northwest. Through collaborators in other regions, they received 308 stripe rust samples from ten states. Spores from these samples were recovered and multiplied on susceptible wheat plants in the greenhouse to establish isolates. Each isolate was tested on the set of wheat or barley differentials for identifying races of the wheat or barley stripe rust pathogen. From the 2020 samples, they identified 19 races (including 2 new races) of the wheat stripe rust pathogen and 10 races (including 1 new race) of the barley stripe rust pathogen and determined the distributions and frequencies of the races and virulence factors. From the 2021 collection, nine races of the wheat stripe rust pathogen and three races of the barley stripe rust pathogen have been identified so far. Based on the virulence data of the races, resistance genes, such as Yr5, Yr15, and many other genes identified by this program and other programs in the world, have been determined to be effective against all populations of the wheat stripe rust pathogen in the United States, and these genes can be used in breeding programs for developing stripe rust resistant wheat cultivars. Similar information has also been obtained for the barley stripe rust pathogen and barley resistance genes. Based on virulence patterns, distributions, and frequencies, they selected races for use in their wheat and barley germplasm screening research. This progress is on schedule. Under Sub-objective 1B, ARS scientists in Pullman, Washington, characterized the wheat stripe rust collections from 2010 to 2017 in the United States using a set of simple sequence repeat (SSR) markers. In this study, they identified 1,454 multi-locus genotypes (MLGs) from 2,247 isolates of the wheat stripe rust pathogen established over the eight years. In general, the pathogen populations in the western United States (states west of the Rocky Mountains) had more MLGs and higher diversities than the populations in the eastern United States (states east of the Rocky Mountains). The stripe rust pathogen population varied from year to year with the 2010 and 2011 populations were more different from the other years. Genetic variation was higher among years than among regions, indicating the fast changes of the population. The pathogen was more diverse among the different epidemiological regions in the west than among regions in the east. Gene flow was stronger among the regional populations in the east than in the west. Phylogenic analyses classified the isolates into three major molecular groups (MGs) and 10 sub-MGs by combining the genotypic data of 2010-2017 isolates with those of 1968-2009 in a previous study. MG1 contained both 1968-2009 isolates (23.1%) and 2010-2017 isolates (76.9%); MG2 had 99.4% isolates from 1968-2009; and MG3, which was the most recent and distinct group, had 99.1% isolates from 2010-2017. Of the 10 sub-MGs, 5 were detected only from 2011-2017. The SSR genotypes had a moderate, but significant correlation with the virulence phenotype data. The random association analysis based on either regional or yearly populations indicated that the wheat stripe rust populations in the United States are clonal. This study determined the high diversity, fast dynamics, and various levels of differentiation of the U.S. wheat stripe rust population over the years and among epidemiological regions. The results are useful for managing wheat stripe rust. Under Sub-objective 2A, ARS scientists in Pullman, Washington, have continued to identify and map genes in wheat for resistance to stripe rust. They have assembled three wheat germplasm panels including two winter wheat panels and one spring wheat panel (each panel consisting of 420 to 520 entries) for genome-wide association studies (GWAS) for identifying more genes for resistance to stripe rust. In 2021, they have phenotyped the three panels at Mount Vernon, Washington for stripe rust response data and genotyped the entries with single-nucleotide polymorphism (SNP) markers identified through genotyping by multiplex sequencing (GMS). They are currently conducting GWAS analysis to identify genes for stripe rust resistance. Continuing their studies for identifying and mapping stripe rust resistance in 40 winter wheat bi-parental mapping populations, they phenotyped 20 selected lines of each mapping population used in the bulk segregant analysis (BSA) at Mount Vernon, Washington, to validate the phenotype data of these lines. They also phenotyped the whole population of eight crosses for validating the resistance loci identified from the BSA studies and further mapping individual genes in these crosses. They have completed a study of identifying a gene for high-temperature adult-plant (HTAP) resistance in a wheat near-isogenic line (NIL) for all-stage resistance gene Yr17. Originally from wild grass Aegilops ventricose, Yr17 has been widely used in wheat breeding programs in the United States and many other countries for developing wheat varieties with resistance to stripe rust and other rusts. This gene is present in many wheat varieties grown in the United States, and its NIL is included in the set of wheat genotypes used to differentiate races of the wheat stripe rust pathogen. The virulence to Yr17 appeared in the United States in the early 1970s and has increased in frequency since the 1990s. Especially since 2010, more than 80% of wheat stripe rust isolates obtained every year were virulent to Yr17, but wheat varieties with Yr17, including the Yr17 NIL, has shown various levels of resistance, which causes confusion about stripe rust pathogen races in different years and regions. To test the hypothesis that the Aegilops ventricosa chromosome translocated to wheat varieties carries another gene for HTAP resistance in addition to the race-specific, all-stage resistance gene Yr17, ARS scientists in Pullman, Washington, developed mutant lines from the Yr17 NIL using ethyl methanesulfonate mutagenesis, which separated the HTAP resistance from the Yr17 resistance. They crossed one of the mutant lines carrying only the HTAP resistance with the recurrent parent and developed a mapping population. Using the mapping population, they identified a gene for HTAP resistance and mapped it to the translocated part of chromosome from Aegilops ventricosa, with the location similar to Yr17. This study shows the usefulness of the wheat varieties carrying the Aegilops ventricosa translocation and the importance of combining all-stage resistance with HTAP resistance in developing wheat cultivars with durable resistance. Under Sub-objective 2B, ARS scientists in Pullman, Washington, planted more than 20,000 wheat and barley entries in the fields near Pullman and Mount Vernon, Washington, for screening the materials for resistance to stripe rust. Some of the nurseries were also planted in three additional locations. They have completed stripe rust response data for the nurseries planted in different locations. Due to the extremely dry conditions in 2021, the field sites in eastern Washington did not produce adequate stripe rust for reliable evaluation. They obtained excellent stripe rust data for all nurseries at Mount Vernon in western Washington. They also have tested the wheat and barley variety trial nurseries and uniform nurseries from various wheat and barley production regions of the United States in both seedling and adult-plant stages with selected races of the stripe rust pathogen in the greenhouse. The tests in both field and greenhouse allow identifying different types of resistance to stripe rust as well as different levels of resistance. They have provided the data to various breeding programs throughout the country for selecting resistant lines for releasing as new varieties. The test results of currently grown varieties are used to update stripe rust reactions for the varieties listed in Seed-Buying Guides to be selected by growers to grow. Growing resistant varieties will reduce the potential risk of stripe rust damage.

Accomplishments
1. Determined population diversity, dynamics, and differentiation of the wheat stripe rust pathogen in the United States. Molecular characterization of the stripe rust pathogen population is important for understanding the pathogen variation and epidemiology of the disease. ARS scientists in Pullman, Washington, have recently published a paper on molecular characterization of the wheat stripe rust collections from 2010 to 2017 in the United States. Using a set of simple sequence repeat (SSR) markers, they identified 1,454 genotypes from 2,247 isolates, clustered them into three major molecular groups (MGs) and 10 sub-MGs by combining the genotypic data of 2010-2017 isolates with those of 1968-2009 in a previous study. Through various population genetic analyses, they determined that the western populations had more genotypes and higher diversities than the eastern populations; the pathogen population varied from year to year and from region to region; and gene flow was stronger among the regional populations in the east than in the west. They identified a new MG and five sub-MGs that have been introduced or developed in the United States since 2011, identified a moderate but significant correlation of the molecular data with the virulence data, and determined that the U.S. wheat stripe rust populations are asexually reproduced. This study improves the understanding the mechanisms of the pathogen evolution, and the results are useful for managing wheat stripe rust.

2. Identified races of the wheat and barley stripe rust pathogens. The wheat and barley stripe rust pathogens evolve rapidly to produce new races that can overcome resistance in currently grown varieties, and the information of races with their virulence factors is essential for breeding programs to use effective genes for developing new varieties with adequate and durable resistance. ARS scientists in Pullman, Washington, identified 19 races, including two new races, of the wheat stripe rust pathogen and 10 races, including one new race, of the barley stripe rust pathogen from the United States, 2020 collections, and determined the frequencies and distributions of these races and virulence factors in various epidemic regions. The results can be used by breeders to select effective resistance genes for developing new varieties and by pathologists to select important races for screening wheat and barley germplasm for releasing new varieties with adequate and durable resistance to stripe rust.

3. Identified a new gene conferring durable resistance to stripe rust in an important source of wheat germplasm. Stripe rust is best controlled through developing and growing resistant varieties with genes for durable high-temperature and adult-plant (HTAP) resistance and effective all-stage resistance. ARS scientists in Pullman, Washington, have completed a study of identifying a gene for durable HTAP resistance in a wheat near-isogenic line (NIL) for all-stage resistance gene Yr17 originally from wild grass Aegilops ventricose. They developed mutant lines from a Yr17 NIL using ethyl methanesulfonate mutagenesis, which separated the HTAP resistance from the Yr17 resistance and developed a mapping population by crossing one of the mutant lines carrying only the HTAP resistance with the recurrent parent. Through phenotyping and genotyping the mapping population, they identified a gene for HTAP resistance and mapped the gene to the translocated part of chromosome from Aegilops ventricosa, with the location similar to Yr17. This study shows the usefulness of the wheat varieties carrying the Aegilops ventricosa translocation and the importance of combining all-stage resistance with HTAP resistance in developing wheat varieties with durable resistance.

4. Screened wheat and barley germplasm for resistance to stripe rust. Developing resistant varieties is the most effective, easy-to use, and environmental-friendly approach to control stripe rust. ARS scientists in Pullman, Washington, screened more than 20,000 wheat and barley germplasm from breeding programs throughout the United States in the field and in the greenhouse for response to stripe rust in 2021. They provided the data to various breeding programs for releasing new resistant varieties and to growers for selecting released resistant varieties to grow. Based on their stripe rust data in the recent years, they collaborated with various breeding programs in releasing and registering 14 new wheat varieties with resistance to stripe rust. Growing these new varieties will reduce potential risk of stripe rust.

Review Publications
Liu, L., Yuan, C., Wang, M., See, D.R., Chen, X. 2020. Mapping quantitative trait loci for high level resistance to stripe rust in spring wheat PI 197734 using a doubled haploid population and genotyping by multiplexed sequencing. Frontiers in Plant Science. 11. Article 596962. https://doi.org/10.3389/fpls.2020.596962.
Chen, X., Sprott, J.A., Evans, C.K. 2021. Evaluation of Pacific Northwest spring wheat cultivars to fungicide application for control of stripe rust in 2020. Plant Disease Management Reports. 15. Article 031.
Chen, X., Evans, C.K., Sprott, J.A. 2021. Evaluation of foliar fungicides for control of stripe rust on spring wheat in 2020. Plant Disease Management Reports. 15. Article CF031. https://www.plantmanagementnetwork.org/pub/trial/pdmr/reports/2021/CF029.pdf.
Chen, X., Sprott, J.A., Evans, C.K., Qin, R. 2021. Evaluation of Pacific Northwest winter wheat cultivars to fungicide application for control of stripe rust in 2020. Plant Disease Management Reports. 15:CF030.
Chen, X., Evans, C.K., Sprott, J.A. 2021. Evaluation of foliar fungicides for control of stripe rust on winter wheat in 2020. Plant Disease Management Reports. 15:CF028.
Gill, K.S., Kumar, N., Carter, A.H., Randhawa, H.S., Morris, C.F., Baik, B.V., Higginbotham, R.W., Engle, D.A., Guy, S.O., Burke, I.C., Lyon, D., Murray, T.D., Chen, X. 2020. Registration of ‘Curiosity CL+' soft white winter wheat. Journal of Plant Registrations. 14(3):377-387. https://doi.org/10.1002/plr2.20066.
Esvelt Klos, K.L., Hayes, P., Del Blanco, I., Chen, X., Filichkin, T., Helgerson, L., Fisk, S., Bregitzer, P.P. 2020. Quantitative trait loci for field resistance to barley stripe rust derived from malting line 95SR316A. Crop Science. 60(4):184-1853. https://doi.org/10.1002/csc2.20154.
Zhang, G., Martin, T.J., Frtiz, A.K., Regan, R., Bai, G., Chen, M., Bowden, R.L., Jin, Y., Chen, X., Kolmer, J.A., Chen, Y.R., Seabourn, B.W. 2020. Registration of ‘KS Venada’ hard white winter wheat. Journal of Plant Registrations. 14:153–158. https://doi.org/10.1002/plr2.20026.
Carter, A.H., Allan, R.E., Balow, K., Burke, A., Chen, X., Engle, D.A., Garland Campbell, K.A., Hagemeyer, K., Morris, C.F., Murray, T., Paulitz, T.C., Shelton, G. 2020. How ‘Madsen’ has shaped Pacific Northwest wheat and beyond. Journal of Plant Registrations. 14(3):223-233. https://doi.org/10.1002/plr2.20049.
Carter, A.H., Balow, K.A., Shelton, G.B., Burke, A.B., Hagemeyer, K., Worapong, J., Higginbotham, R.W., Chen, X., Engle, D.A., Murray, T.D., Morris, C.F. 2020. Registration of ‘Purl’ soft white winter wheat. Journal of Plant Registrations. 14:(3)398-405. https://doi.org/10.1002/plr2.20069.
Gill, K.S., Randhawa, H.S., Murphy, K., Carter, A.H., Morris, C.F., Higginbotham, R.W., Engle, D.A., Guy, S.O., Lyon, D.J., Murray, T.D., Chen, X., Schillinger, W.F. 2021. Registration of 'Resilience CL+' soft white winter wheat. Journal of Plant Registrations. 15(1):196-205. https://doi.org/10.1002/plr2.20118.
Griffey, C., Malla, S., Brooks, W., Seago, J., Christopher, A., Thomason, W., Pitman, R., Markham, R., Vaughn, M., Dunaway, D., Beahm, M., Barrack, C.L., Rucker, E., Behl, H., Hardiman, T., Beahm, B., Browning, P., Schmale Iii, D., Mcmaster, N., Curtis, J.T., Gulick, S., Ashburn, S.B., Jones Jr., N., Baik, B.V., Bockelman, H.E., Marshall, D.S., Fountain, M.O., Brown Guedira, G.L., Cowger, C., Cambron, S.E., Kolmer, J.A., Jin, Y., Chen, X., Garland Campbell, K.A., Sparry, E. 2020. Registration of ‘Hilliard’ wheat. Journal of Plant Registrations. 14(3):406-417. https://doi.org/10.1002/plr2.20073.
Zhang, G., Martin, T.J., Fritz, A.K., Li, Y., Bai, G., Bowden, R.L., Chen, M., Chen, X., Kolmer, J.A., Seabourn, B.W., Chen, Y., Marshall, D.S. 2020. Registration of ‘KS Dallas’ hard red winter wheat. Journal of Plant Registrations. https://doi.org/10.1002/plr2.20108.
Zhang, G., Fritz, A.K., Haley, S., Li, Y., Bai, G., Bowden, R.L., Chen, M., Jin, Y., Chen, X., Kolmer, J.A., Seabourn, B.W., Chen, Y., Marshall, D.S. 2020. Registration of ‘KS Western Star’ hard red winter wheat. Journal of Plant Registrations. https://doi.org/10.1002/plr2.20104.
Carter, A.H., Balow, K.A., Shelton, G.B., Burke, A.B., Hagemeyer, K.E., Stowe, A., Worapong, J., Higginbotham, R.W., Chen, X., Engle, D.A., Murray, T.D., Morris, C.F. 2020. Registration of 'Stingray CL+' soft white winter wheat. Journal of Plant Registrations. 15(1):161-171. https://doi.org/10.1002/plr2.20109.
Brucker, P., Berg, J., Lamb, P., Kephart, K., Eberly, J., Miller, J., Chen, C., Torrion, J., Pradhan, G., Ramsfield, R., Nash, D., Holen, D., Cook, J., Gale, S.W., Jin, Y., Kolmer, J.A., Chen, X., Bai, G. 2020. Registration of ‘Bobcat’ hard red winter wheat. Journal of Plant Registrations. 2020:1-6. https://doi.org/10.1002/plr2.20057.
Brandt, K.M., Chen, X., Tabima, J.F., See, D.R., Zemetra, R.S. 2021. QTL analysis of adult plant resistance to stripe rust in a winter wheat recombinant inbred population. Plants. 10(3). Article 572. https://doi.org/10.3390/plants10030572.
Hu, Y.S., Tao, F., Su, C., Zhang, Y., Li, J., Wang, J.H., Xu, X.M., Chen, X., Shang, H.S., Hu, X.P. 2020. NBS-LRR gene TaRPS2 is positively associated with the high-temperature seedling-plant resistance of wheat against Puccinia striiformis f. sp. tritici. Phytopathology. https://doi.org/10.1094/PHYTO-03-20-0063-R.
Sinha, P., Chen, X. 2021. Potential Infection Risks of the Wheat Stripe Rust (Puccinia striiformis f. sp. tritici) and Stem Rust (P. graminis f. sp. tritici) Pathogens on Alternate Host Barberry in Asia and Southeastern Europe. Phytopathology. 10(5). Article 957. https://doi.org/10.3390/plants10050957.
Carter, A.H., Balow, K.A., Shelton, G.B., Burke, A.B., Hagemeyer, K.E., Stowe, A., Worapong, J., Higginbotham, R.W., Chen, X., Engle, D.A., Murray, T.D., Morris, C.F. 2020. Registration of ‘Scorpio’ hard red winter wheat. Journal of Plant Registrations. 15(1):113-120. https://doi.org/10.1002/plr2.20076.
Carter, A.H., Balow, K.A., Shelton, G.B., Burke, A.B., Hagemeyer, K.E., Stowe, A., Worapong, J., Higginbotham, R.W., Chen, X., Engle, D.A., Murray, T.D., Morris, C.F. 2020. Registration of ‘Devote’ soft white winter wheat. Journal of Plant Registrations. 15(1):113-120. https://doi.org/10.1002/plr2.20079.
Nazarov, T., Chen, X., Carter, A., See, D.R. 2021. Fine mapping of high-temperature adult-plant resistance to stripe rust in wheat cultivar Louise. Journal of Plant Protection Research. 60(2):126-133. https://doi.org/10.24425/jppr.2020.132213.
Yao, F.J., Long, L., Wang, Y.Q., Duan, L.Y., Zhao, X.Y., Jiang, Y., Pu, Z.E., Li, W., Jiang, Q.T., Wang, J.R., Wei, Y.M., Ma, J., Kang, H.Y., Dai, S.F., Q, P.F., Zheng, Y.L., Chen, G.Y., Chen, X. 2020. Population structure and genetic basis of the stripe rust resistance of 140 Chinese wheat landraces revealed by a genome-wide association study. Molecular Plant Pathology. 301. Article 110688. https://doi.org/10.1016/j.plantsci.2020.110688.
Garland Campbell, K.A., Allan, R., Burke, A., Chen, X., DeMacon, P., Higginbotham, R., Engle, D., Klarquist, E., Mundt, C., Murray, T., Morris, C.F., See, D.R., Wen, N. 2021. Registration of “ARS Crescent” soft white winter club wheat. Journal of Plant Registrations. 15(3):515-526. https://doi.org/10.1002/plr2.20135.
Garland Campbell, K.A., Carter, A.H., Allan, R., Chen, X., Steber, C.M., DeMacon, P., Esser, A., Higginbotham, R., Engle, D., Klarquist, E., Morris, C.F., Mundt, C., Murray, T., See, D.R., Wen, N. 2021. Registration of Castella soft white winter club wheat. Journal of Plant Registrations. 15(3):504-514. https://doi.org/10.1002/plr2.20132.
Liu, T., Bai, Q., Wang, M., Li, Y., Wan, A., See, D.R., Xia, C., Chen, X. 2021. Genotyping Puccinia striiformis f. sp. tritici isolates with SSR and SP-SNP markers reveals dynamics of the wheat stripe rust pathogen in the United States from 1968 to 2009 and identifies avirulence associated markers. Phytopathology. https://doi.org/10.1094/PHYTO-01-21-0010-R.
Chen, X., Wang, M., Wan, A., Bai, Q., Li, M., Lopez, P.F., Maccaferri, M., Mastrangelo, A., Barnes, C.W., Campan, D., Tenuta, A., Abdelrhim, A. 2021. Virulence characterization of Puccinia striiformis f. sp. tritici collections from six countries in 2013 to 2020. Canadian Journal of Plant Pathology. https://doi.org/10.1080/07060661.2021.1958259.
Bai, Q., Wan, A., Wang, M., See, D.R., Chen, X. 2021. Population diversity, dynamics, and differentiation of wheat stripe rust pathogen Puccinia striiformis f. sp. tritici from 2010 to 2017 and comparison with 1968 to 2009 in the United States. Frontiers in Microbiology. 12. Article 696835. https://doi.org/10.3389/fmicb.2021.696835.
Merrick, L.F., Burke, A.B., Chen, X., Carter, A.H. 2021. Breeding with Major and Minor Genes: Genomic Selection for Quantitative Disease Resistance. Frontiers in Plant Science. 12. Article 713667. https://doi.org/10.3389/fpls.2021.713667.