Location: Hard Winter Wheat Genetics Research
2019 Annual Report
Objectives
OBJECTIVE 1: Strategically characterize wheat genetic resources for priority traits including resistance to damaging fungal pathogens (stripe rust, leaf rust, stem rust, Fusarium head scab), resistance to viruses, resistance to Hessian fly, tolerance to heat and drought stress, and nutritional quality.
Subobjective 1A: Characterize wheat genetic resources for resistance to stripe rust, leaf rust, and stem rust.
Subobjective 1B: Characterize wheat genetic resources for resistance to Fusarium head blight.
Subobjective 1C: Characterize wheat genetic resources for resistance to Wheat streak mosaic.
Subobjective 1D: Characterize wheat genetic resources for resistance to Hessian Fly.
Subobjective 1E: Characterize wheat genetic resources for improved nutritional quality traits.
OBJECTIVE 2: Efficiently and effectively incorporate genetic traits into high yielding winter wheat germplasm, and distribute germplasm to the breeding community.
Subobjective 2A: Incorporate resistance to stripe rust, leaf rust, and stem rust.
Subobjective 2B: Incorporate resistance to Fusarium head blight.
Subobjective 2C: Incorporate resistance to Wheat streak mosaic.
Subobjective 2D: Incorporate resistance to Hessian Fly.
Subobjective 2E: Incorporate tolerance to heat and drought stress.
Subobjective 2F: Incorporated improved nutritional quality traits.
OBJECTIVE 3: Develop efficient molecular marker technologies for genetic traits and transfer these technologies to the breeding community.
Subobjective 3A: Develop new trait-specific SNP markers for important genes.
Subobjective 3B: Develop new genome-wide multiplexed amplicon sequencing assay and imputation protocols for important genes.
Subobjective 3C: Transfer genotyping data and information to the breeding community.
OBJECTIVE 4: Characterize molecular foundations of critical plant-microbe and plant-insect interactions toward development of effective and durable host plant resistance.
Subobjective 4A: Characterize molecular foundations of virulence and resistance for Hessian fly.
Subobjective 4B: Characterize molecular foundations of virulence and resistance for leaf rust.
Approach
Production of hard winter wheat is limited by recurring intractable problems including diseases, insects, heat, and drought stress. Both nutrient deficiencies and antinutrient excesses affect nutritional quality of wheat products. Our first objective is to identify germplasm with improved resistance to leaf rust, yellow rust, stem rust, Hessian fly, Fusarium head blight, and viruses; improved tolerance to heat and drought stress; as well as increased iron and zinc and lower phytate and cadmium concentrations. The second objective is to transfer these traits into adapted backgrounds and release new germplasm for use as parents in cultivar development. Innovative male-sterile approaches will be used to efficiently construct disease resistance gene pyramids in adapted backgrounds and to isolate coupling-phase recombinants. We will launch a novel full-season wheat recurrent selection project to extend floral initiation and grain filling while maintaining test weight and yield under heat stress. The third objective is to develop more efficient wheat breeding techniques using high-throughput genotyping technologies and large-scale data mining techniques. New allele-specific PCR assays, multiplexed amplicon sequencing assays, and genomic databases will be developed and used to characterize breeding material for the presence of genes of interest. Phenotype and genotype data will be distributed to the breeding community through USDA-supported databases. The fourth objective is to characterize the molecular basis for interaction between wheat plants and leaf rust or Hessian fly. Greater understanding of avirulence effectors in the Hessian fly and the leaf rust pathogen may lead to better strategies for durable resistance.
Progress Report
For Objective 1, approximately 5000 wheat breeding lines were screened for resistance to stripe rust at Rossville, Kansas. The test included entries from the regional nurseries, gene mapping populations, and advanced lines from 15 public and private breeding programs (Goal 1A.1). Approximately 1500 lines were screened for resistance to stem rust at Manhattan, Kansas. Unfortunately, excessive rains and resulting flooding destroyed about one third of the stem rust nursery. Approximately 1500 lines were screened for resistance to leaf rust at Manhattan and Hutchinson, Kansas. Stripe rust mapping populations were all advanced one or two generations (Goal 1A.2). The preliminary field evaluation of stripe rust gene Yr36 was completed and demonstrated the utility of the gene, and a seed increase was completed for 226 near-isogenic lines to provide seed for subsequent field trials (Goal 1A.3, 1E.2). Three new mapping populations, ‘CI13227’/’Lakin’, ‘Lyman’/’Overley’, and ‘Overland’/’Everest’, were evaluated in field and in greenhouse conditions for Fusarium head blight (FHB) resistance (Goal 1B.1). Genotyping and phenotyping for wheat streak mosaic virus resistance was completed, and DNA markers were developed that were associated with resistance. Selections also were made from 91 virus-inoculated populations grown in the field in Hays, Kansas, which will accelerate progress in germplasm development (Goal 1C.1, Goal 2C.1). We screened over 4,500 wheat lines from wheat breeders and geneticists across the plains area for resistance to Hessian fly. We mapped Hessian fly resistance genes H4 and H7/H8. H4 was mapped on chromosome 1A and closely linked SNP markers in the region were identified and converted into KASP markers. H7 was reassigned from chromosome 5D to 2B and H8 was assigned to 6A. We found that H7 and H8 were not complementary genes as previously reported. Instead, H7 is a major gene that explained most of the phenotypic variation, whereas H8 is a minor gene with an additive effect to H7. Closely linked markers to both genes were identified and converted into KASP markers for marker-assisted selection (Goal 1D.1).
For Objective 2, field evaluation was completed on the first available families for introgression of new stripe rust resistance traits, including Yr40, Yr47, Yr51, Yr57, Yr63, and Yr79 (Goal 2A.1). Potential coupling phase recombinants (Goal 2A.2) of Sr2 and Fhb1 were identified. Crosses were completed for construction of coupling phase recombinants of SrTA10171 and Lr34/Yr18/Sr57. A new crossing project to couple Sr12 with Fhb1 was initiated. Pyramids of five or more stem rust genes (Goal 2A.3) were evaluated in disease nurseries at five locations, and agronomic performance was tested in multi-location replicated yield trials. Introgression germplasm (BC2F3 and BC3F2) has been selected for seed increase. Second backcrosses were completed toward development of hard winter wheat germplasm that incorporates combinations of major QTLs for Fusarium head blight resistance (Goal 2B.1). Families from crosses to 13 durum landraces with high temperature Hessian fly resistance were screened with Hessian flies, and 765 F2 progeny were vernalized and transplanted to the greenhouse to produce F3 seed (Goal 2D.1). F1 plants (1814 plants) from backcrosses of T. aestivum to T. dicoccoides were grown in the greenhouse (Goal 2E.1). The heat tolerance dominant male-sterile population was grown in the field near Hutchinson, Kansas, and Cycle 1 of field selection was completed with the harvest of 355 individual male-sterile plants from the population (Goal 2E.2). Winter-hardy F4 families of four crosses of hard winter wheat to high-zinc spring lines were selected in the field near Rossville, Kansas (Goal 2F.1), and F2:3 spikes of 15 crosses to low phytate wheats were selected for field evaluation (Goal 2F.1). A combined total of 567 new crosses were made in the greenhouse to support the ongoing development of improved hard winter wheat germplasm. Agronomic performance of inbred lines was evaluated in 2788 yield trial plots.
For Objective 3, we developed a new genome-wide high-throughput genotyping system for background screening and other applications (Goal 3B.2). More than 100,000 wheat breeding samples from 12 breeding programs were analyzed for molecular markers in our genotyping lab. More than 200 million genome-wide and 220,000 sequence-specific data points were generated for wheat geneticists and breeders. The regional wheat nurseries were also characterized with more than 100 sequence-specific markers linked to important traits of interest to breeders. The genotypic data were used in conjunction with phenotypic data by wheat researchers for characterizing and selecting breeding lines with desired combinations of agronomic and pest resistance traits (Goal 3C.1).
For Objective 4, we discovered in Hessian fly a family of genes that originated from a bacterium. The genes encode enzymes that have levanase and inulinase activity. Gaining this family of enzymes allows Hessian fly to utilize levan and inulin, which are fructose polymers otherwise not usable by animal species (Goal 4A.1). We produced recombinant proteins of family-1 effectors from Hessian fly in E. coli. We used the recombinant proteins to produce antibodies. We used the antibodies to detect the distribution of family-1 effectors in wheat tissue once they are injected into host plants. We found that the distribution of family-1 effectors is remarkably different in wheat tissues between resistant and susceptible plants. This differential distribution between resistant and susceptible plants provides us insight into the mechanisms of wheat resistance and susceptibility to Hessian fly (Goal 4A.2). Four mutant Thatcher lines that have a reduction in leaf rust susceptibility are being characterized by microscopy to determine how and when fungal growth is being restricted. Ribonucleic acid (RNA) is also being isolated from these four lines for gene expression and mutation detection analysis. Fifteen different lines are being crossed into Kansas-adapted varieties. Three have been evaluated in the field and the reduced susceptibility phenotypes are being expressed in the field with significant reduction of rust infection (Goal 4B.1). Five effector/avirulence candidates for Lr2A and Lr2C and four for Lr11 have been cloned into a plant expression system. Transient transformation ballistics will be used to test whether these candidates will induce a hypersensitive response in Thatcher isolines containing the leaf rust resistance genes Lr2A, Lr2C or Lr11 (Goal 4B.2).
Accomplishments
1. Cloning of major resistance gene Fhb1 for Fusarium head blight. Fusarium head blight (FHB) is a destructive wheat disease in the USA and many other countries. Fhb1 is a major gene for FHB resistance that was originally identified in Chinese germplasm. It has since been introduced into wheat lines around the world. ARS scientists in Manhattan, Kansas, cloned Fhb1 and showed that the gene encodes a defective form of a putative histidine-rich calcium binding protein. The functional form of the gene, present in susceptible cultivars, appears to be a susceptibility gene that allows the fungus to spread in the spike. Cloning of Fhb1 provides ideal diagnostic markers for selective breeding and opens the possibility of using bioengineering approaches to further enhance FHB resistance.
2. New high-throughput DNA marker system developed. Modern plant breeding requires a robust genome-wide, low cost, high-throughput DNA marker platform. ARS scientists in Manhattan, Kansas, developed a Multiplex Restriction Amplicon Sequencing (MRASeq) marker system that uses polymerase chain reaction and targets DNA fragments flanked by restriction enzyme cutting sites. MRASeq generated thousands of markers that are randomly distributed across wheat and barley genomes. This novel, inexpensive, next-generation-sequencing-based genotyping platform can be used for various breeding applications in wheat and other species.
3. Identification of wheat gene for spikelets per spike. Wheat yields can be broken down into various yield components including plants per acre, spikes per plant, spikelets per spike, kernels per spikelet, and individual kernel weight. A better understanding of the genes controlling differences in wheat grain yield components can accelerate the improvements required to satisfy future food demands. ARS scientists in Manhattan, Kansas, identified a gene on wheat chromosome arm 7AL regulating spikelet number per spike. This gene, designated here as WAPO1, is similar to a rice gene which affects spikelet number. This may open the possibility of manipulating WAPO1 to further increase spikelet number. The resulting larger wheat spikes may lead to higher yields.
4. Stem rust-resistant wheat germplasm release. Stem rust is a re-emerging disease in east Africa and the Middle East. New highly virulent races threaten wheat production around the world. Three hard winter wheat lines with multigenic adult plant resistance to stem rust were officially released by ARS scientists in Manhattan, Kansas. These lines (KS14U6380R5, KS16U6380R10, and KS16U6380R11) are now globally available to breeders to use as parents in crosses to develop winter wheat germplasm resistant to stem rust, including the highly virulent east African races of the disease.
5. Rapid tests of wheat lines for cadmium accumulation. The excessive accumulation of cadmium in harvested crops grown on high cadmium soils has increased public concerns for food safety. Breeding is a promising way to reduce grain cadmium concentration. The current approach to breeding low-cadmium wheat is to measure cadmium in grain after harvest. However, more rapid tests are needed. ARS scientists in Manhattan, Kansas, tested the utility of two selection methods, DNA marker-based selection and hydroponic seedling selection, in offspring of a cross between a low and a moderately high grain-cadmium cultivar. Both DNA marker-based selection and hydroponic selection were effective. These tools can be used by breeders to select wheat lines with low cadmium accumulation when grown on high cadmium soils.
6. Three new Hessian fly resistance genes from durum wheat. Hessian fly is a major pest of wheat in both America and North Africa. This destructive insect has been mainly controlled by breeding and deploying resistant wheat cultivars. Unfortunately, Hessian fly populations typically overcome resistant varieties within a few years after release. To make the host resistance strategy sustainable, new sources of resistance need to be identified and developed continuously. ARS scientists in Manhattan, Kansas, identified three new resistance genes from durum wheat. In addition, molecular markers linked to the genes were identified and made available to breeders. The newly identified resistance genes and markers can be used for marker-assisted breeding of new cultivars with improved resistance to Hessian fly.
7. Meta-analysis of Fusarium head blight reveals six consistently effective resistance genes. Fusarium head blight (FHB) causes significant reductions in wheat grain yield and quality. Many FHB resistance quantitative trait loci (QTLs) have been reported from Chinese sources, but the relationships among those QTLs from different landraces have not been characterized. ARS scientists in Manhattan, Kansas, mapped 31 QTLs on 16 chromosomes in five different Chinese landraces. Meta-analysis identified six reproducible meta-QTLs, with two on chromosome 3B and one each on the chromosomes 2D, 3A, 3D and 4D. Closely linked markers to all the meta-QTLs were successfully converted to breeder-friendly assays for use in marker-assisted selection. These markers are available to breeders for improving resistance to FHB.
8. Barley yellow dwarf disease affects grain quality in wheat. Barley yellow dwarf (BYD) is a disease caused by several aphid-borne viruses that reduce the productivity of important grain crops including wheat, oats, and barley. Using grain samples from untreated plots vs. plots sprayed with insecticide every two weeks, ARS scientists in Manhattan, Kansas, measured starch content and protein content using near-infrared spectroscopy (NIRS). BYD was estimated to increase protein content by 28.4%, decrease starch content by 6.3%, decrease average kernel weight by 31.4%, and decrease yield by 66.4% at 100% BYD incidence. The increase in protein was probably due to the concentrating effect of shriveled grain. NIRS measurement of grain protein and starch content may offer wheat breeding programs a rapid and objective selection method for improved resistance or physiological tolerance to BYD.
9. Hessian fly salivary proteins may hold key to host specificity. Hessian fly, barley midge, and oat midge are important insect pests of small grains. The three closely related species have the same feeding mechanism of injecting saliva into host plant seedlings. This results in identical plant symptoms. However, Hessian fly mainly attacks wheat, barley midge only attacks barley, while oat midge only attacks oat. ARS scientists in Manhattan, Kansas, have identified genes encoding salivary proteins common to the three midges, and genes encoding salivary proteins that are unique to each species. The results provide a basis for future studies to determine how all three species are able to manipulate the metabolism and overcome the defenses only from their own host plants. A better understanding of the host specificity may result in better methods for controlling these destructive insect pests.
Review Publications
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.
Zhang, H., Su, Z., Bai, G., Zhang, X., Ma, H., Li, T., Deng, Y., Mai, C., Yu, L., Liu, H. 2018. Improvement of resistance of wheat cultivars to fusarium head blight in the Yellow–Huai rivers valley winter wheat zone with functional marker selection of Fhb1 gene. Acta Agronomica Sinica. 44(4):505-511. https//doi:10.3724/SP.J.1006.2018.00505.
Su, Z., Jin, S., Zhang, D., Bai, G. 2018. Development and validation of diagnostic markers for Fhb1, a major QTL for Fusarium head blight resistance in wheat. Theoretical and Applied Genetics. 2018. https://doi.org/10.1007/s0012 2-018-3159-6.
Li, G., Carver, B., Cowger, C., Bai, G., Xu, X. 2018. Pm223899, a new recessive powdery mildew resistance gene identified in Afghanistan landrace PI 223899. Theoretical and Applied Genetics. 131(12):2775-2783. https://doi.org/10.1007/s00122-018-3199-y.
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.
Li, G., Xu, X., Tan, C., Carver, B.F., Bai, G., Wang, X., Bonman, J.M., Wu, Y., Hunger, R., Cowger, C. 2019. Identification of powdery mildew resistance loci in wheat by integrating genome-wide association study (GWAS) and linkage mapping. The Crop Journal. 7(3):294-306. https://doi.org/10.1016/j.cj.2019.01.005.
Kuzay, S., Xu, Y., Zhang, J., Katz, A., Pearce, S., Su, Z., Fraser, M., Anderson, J.A., Brown Guedira, G.L., Dewitt, N., Peters Haugrud, A., Faris, J.D., Akhunov, E., Bai, G., Dubcovsky, J. 2019. Identification of a candidate gene for a QTL for spikelet number per spike on wheat chromosome arm 7AL by high-resolution genetic mapping. Theoretical and Applied Genetics. https://doi.org/10.1007/s00122-019-03382-5.
Peiris, K., Bowden, R.L., Todd, T.C., Bockus, W.W., Davis, M.A., Dowell, F.E. 2019. Effects of barley yellow dwarf disease on wheat grain quality. Cereal Chemistry. 00:1-11. https://doi.org/10.1002/cche.10177.
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.
Rudd, J.C., Devkota, R.N., Ibrahim, A.M., Baker, J.A., Baker, S., Lazar, M.D., Sutton, R., Simoneaux, B., Opena, G., Rooney, L.W., Awika, J.M., Liu, S., Xue, Q., Bean, B., Duncan, R.W., Seabourn, B.W., Bowden, R.L., Jin, Y., Chen, M., Graybosch, R.A. 2018. ‘TAM 114’ wheat, excellent bread-making quality hard red winter wheat cultivar adapted to the southern high plains. Journal of Plant Registrations. https://doi.org/10.3198/jpr2017.11.0081crc.
Liu, C., Guttieri, M.J., Waters, B.M., Eskridge, K.M., Baenziger, P. 2018. Selection of bread wheat for low grain cadmium concentration at the seedling stage using hydroponics versus molecular markers. Crop Science. 59(3):945-956. https://doi.org/10.1007/s11104-018-3712-8.
Liu, C., Guttieri, M.J., Water, B., Eskridge, K., Easterly, A., Baenziger, P. 2018. Cadmium concentration in terminal tissues as tools to select low-cadmium wheat genotypes. Plant and Soil. 2018. 430:127-138. https://doi.org/10.1007/s11104-018-3712-8.
Yang, Y., Basnet, B.R., Ibrahim, A.M., Rudd, J.C., Chen, X., Bowden, R.L., Xue, Q., Wang, S., Johnson, C., Metz, R., Mason, R.E., Hays, D.B., Liu, S. 2018. Developing KASP markers on a major stripe rust resistance QTL in TAM 111 using 90K array and genotyping-by-sequencing SNPs. Crop Science. 59(1):165-175. https://doi.org/10.2135/cropsci2018.05.0349.
Sidhu, J., Ramakrishnan, S., Ali, S., Bernando, A., Bai, G., Abdullah, S., Ayana, G., Sehgal, S.K. 2019. Assessing the genetic diversity and characterizing genomic regions conferring Tan Spot resistance in cultivated rye. PLoS One. https://doi.org/10.1371/journal.pone.0214519.
Bassi, F., Brahmi, H., Sabraoui, A., Amri, A., Nsarellah, N., Nachit, M., Al-Abdallat, A., Chen, M., Lazraq, A., El Bouhssini, M. 2019. Genetic identification of loci for Hessian fly resistance in Durum wheat. Molecular Breeding. 39:24. https://doi.org/10.1007/s11032-019-0927-1.
Bernardo, A., St Amand, P.C., Le, H., Su, Z., Bai, G. 2019. Multiplex Restriction Amplicon Sequencing (MRASeq), a novel next generation sequencing based marker platform for high-throughput genotyping. Nucleic Acids Research. https://doi.org/10.1111/pbi.13192.
Nyine, M., Wang, S., Kiani, K., Jordan, K., Liu, S., Byrne, B., Haley, S., Baenziger, S., Chao, S., Bowden, R.L., Akhunov, E. 2019. Genotype imputation in winter wheat using first-generation haplotype map SNPs improves genome-wide association mapping and genomic prediction of traits. G3, Genes/Genomes/Genetics. 9:125-133. https://doi.org/10.1534/g3.118.200664.
Gill, H., Chunxian, L., Jagdeep, S.S., Wenxuan, L., Wilson, D., Bai, G., Gill, B.S., Sehgal, S.K. 2019. Fine mapping of wheat leaf rust resistance gene Lr42. International Journal of Molecular Sciences. 20:2445. https://doi.org/10.3390/ijms20102445.
Lin, M., Liu, S., Zhang, G., Bai, G. 2018. Effects of TaPHS1 and TaMKK3-A genes on wheat PHS resistance. Molecular Breeding. 8(10):210. https://doi.org/10.3390/agronomy8100210.
Li, W., Zhang, Q., Wang, S., Langham, M.A., Singh, D., Bowden, R.L., Xu, S.S. 2018. Development and characterization of wheat-sea wheatgrass (Thinopyrum junceiforme) amphiploids for biotic stress resistance and abiotic stress tolerance. Theoretical and Applied Genetics. 132:163–175. https://doi.org/10.1007/s00122-018-3205-4.
Al-Jbory, Z., El-Bouhssini, M., Chen, M. 2019. Conserved and unique putative effectors expressed in the salivary glands of three related gall midge species. Journal of Insect Science. 18(5):15; 1-9. https://doi.org/10.1093/jisesa/iey135.
Zhao, J., Mohamed, N.R., Khalaf, L., Chuang, W., Zhao, L., Smith, C., Carver, B., Bai, G. 2019. Mapping the wheat curl mite resistance gene in the advanced wheat breeding line OK05312. Theoretical and Applied Genetics. 59:1-9.
Kumssa, T.T., Shoup Rupp, J., Fellers, J.P., Fellers, M.C., Zhang, G. 2019. A new isolate of wheat streak mosaic virus virulent to Wsm2. Plant Pathology. 68(4):783-789. https://doi.org/10.1111/ppa.12989.
Carrera, S., Aguirres-Rojas, L., Sinha, D.K., Khalaf, L., Chuang, W., Chen, M., Smith, C. 2017. Resistance to wheat curl mite in arthropod-resistant rye-wheat translocation lines. Agronomy Journal. 7, 74. https://doi.org/10.3390/agronomy7040074.
Belamkar, V., Guttieri, M.J., Hussain, W., Jarquin, D., El-Basyoni, I., Poland, J., Lorenz, A., Baenziger, P. 2018. Genomic selection in preliminary yield trials in a winter wheat breeding program. G3, Genes/Genomes/Genetics. 8(8):2735-2747. https://doi.org/10.1534/g3.118.200415.
Hadi, A., Bai, G., Zhang, G., Mohammad, B.R., Mohammadi, V., Peyghambari, S.A. 2019. Imputation accuracy of wheat GBS data using barley and wheat genome references. PLoS One. 14(1):e0208614. https://doi.org/10.1371/journal.pone.0208614.
Wang, W., Pan, Q., Tian, B., He, F., Chen, Y., Akhunova, A., Bai, G., Trick, H., Akhunov, E. 2019. Gene editing of the wheat homologs of TONNEAU1-recruiting motif encoding gene affects grain shape and weight in wheat. Plant Journal. https://doi.org/10.1111/tpj.14440.
Kariyawasam, G.K., Hussain, W., Easterly, A., Guttieri, M.J., Belamkar, V., Poland, J., Venegas, J., Baenziger, P., Marais, F., Rasmussen, J.B., Liu, Z. 2018. Identification of quantitative trait loci conferring resistance to tan spot in a biparental population derived from two Nebraska hard red winter wheat cultivars. Molecular Breeding. 38:140. https://doi.org/10.1007/s11032-018-0901-3.
Fellers, J.P., Webb, C., Fellers, M.C., Shoup Rupp, J., De Wolf, E. 2019. Wheat virus identification within infected tissue using nanopore sequencing technology. Plant Disease. https://doi.org/10.1094/PDIS-09-18-1700-RE.
Garrett, K., Bowden, R.L., Forbes, G., Kulakow, P., Zhou, B. 2017. Resistance genes in global crop breeding networks: A complex adaptive system. Current Opinion in Plant Biology. 107:1268-1278. https://doi.org/10.1094/PHYTO-03-17-0082-FI.
Cheng, G., Chen, M., Zhu, L. 2018. 12-Oxo-Phytodienoic Acid enhances wheat resistance to Hessian fly (Diptera: Cecidomyiidae) under heat stress. Journal of Economic Entomology. 111(2):917-922. https://doi.org/10.1093/jee/tox374.
Su, Z., Bernardo, A., Tian, B., Chen, H., Wang, S., Ma, H., Cai, S., Liu, D., Zhang, D., Li, T., Trick, H., St Amand, P.C., Yu, J., Zhang, Z., Bai, G. 2019. A deletion mutation in TaHRC confers Fhb1 resistance to Fusarium head blight in wheat. Nature Genetics. 51:1099-1105. https://doi.org/10.1038/s41588-019-0425-8.
Neugebauer, K., Bruce, M., Todd, T., Trick, H.N., Fellers, J.P. 2018. Wheat differential gene expression induced by different races of Puccinia triticina. PLoS One. 13(6):e0198350. https://doi.org/10.1371/journal.pone.0198350.
Cai, J., Wang, S., Su, Z., Li, T., Zhang, Bai, G. 2019. Meta-analysis of QTLs for Fusarium head blight resistance in Chinese wheat landraces. The Crop Journal. https://doi.org/10.1016/j.cj.2019.05.003.
Serba, D.D., Muleta, K., St Amand, P.C., Bernando, A., Bai, G., Perumal, R., Bashir, E., Morris, G. 2019. Genetic diversity, population structure, and linkage disequilibrium of pearl millet. The Plant Genome. https://doi.org/doi:10.3835/plantgenome2018.11.0091.
