Implications of genome-wide studies for resistance to Fusarium head blight and foliar viruses in US wheat breeding programs

Abstract

Fusarium head blight (FHB) and foliar viruses such as barley yellow dwarf virus (BYDV), and soil-borne wheat mosaic virus (SBWMV) are among the significant plant pathogenic diseases, causing billions of dollars in annual losses in wheat and small grain cereal production. FHB is particularly concerning due to its characteristic production of mycotoxins, which have substantial quality and health implications for both humans and animals. Genetic resistance remains the primary strategy for managing these complex plant pathogenic diseases. Resistance to FHB, BYD, and SBWMV in host wheat plants is a multifaceted trait influenced by numerous genes with small effect sizes. Over several decades, resistance to these diseases has been identified in studies in various wheat germplasms, including wild relatives. The application of genomic tools such as practical haplotype graphs (PHGs), genome-wide association studies (GWAS), and genomic selection (GS) has enabled the mapping and prediction of stable genomic regions associated with FHB, BYDV, and SBWMV resistance traits. High-resolution GWAS has been employed to identify loci associated with resistance to FHB, BYDV, and SBWMV in wheat. The development of shallow exome capture and imputation tools has facilitated the use of GS, which leverages genome-wide markers to predict FHB resistance traits and enhance genetic gain. This study utilized genomic data to construct a customized wheat practical haplotype graph database, evaluate disease severity traits, map genomic regions conferring resistance to FHB, BYDV, and SBWMV, and predict FHB resistance using GS models in a diverse panel of hard winter wheat (HWW) and soft winter wheat (SWW) cultivars representing major United States public wheat breeding programs. The results indicated significant correlations among FHB disease traits (r = 0.32–0.70, P < 0.001) across years and moderate broad-sense heritability (H²) estimates (0.65–0.74). Twenty-six significant loci were identified in multiple GWAS models, many of which affected multiple traits and represent breeding targets for prioritizing FHB resistance. Most associated loci are located within or near previously identified native quantitative trait loci (QTL). Notably, a 1BL haplotype from the soft winter wheat cultivar ‘Jamestown’ reduced the cumulative disease, the area under the disease progress curve (AUPDC) and Fusarium-damaged kernels (FDK) by 25% and, mycotoxin deoxynivalenol (DON) levels by 18%. In the analysis of foliar viruses, 10 and 7 significant genomic regions associated with resistance to BYDV and SBWMV, respectively, were mapped. These regions included the Bdv2 and Sbwm1 loci that conferred resistance to BYDV and SBWMV. The effect sizes ranging 5% to 22% were reported for these novel rare associations. Disease surveys in the nursery confirmed the presence of both BYDV and SBWMV and revealed annual variation in virus populations. Co-infections with multiple viruses were common, underscoring the necessity for breeding lines with resistance to multiple viruses. The application of genomic selection (GS) and forward genomic prediction in this study highlights the potential of a wheat diversity panel and uniform regional FHB nurseries as valuable resources for breeding programs targeting FHB resistance in the United States. Cross-validation prediction accuracies of the GS models in the diversity panel ranged from 0.51 to 0.68 across FHB traits and single nucleotide polymorphism (SNP) densities. Forward genomic prediction accuracy for FHB severity traits in the independent United States Wheat and Barley Scab Initiative (USWBSI) population, external to the training set, was consistent with cross-validation accuracy from the diversity panel in both 2023 and 2024, with accuracies of 0.52 and 0.55, respectively. The integration of genomic selection with the deployment of novel genetic resistance regions, alongside existing resistance loci, is expected to enhance resistance, promote more sustainable disease control, and reduce the risk of wheat yield loss due to FHB, BYDV, and SBWMV.