Genome-wide association mapping of resistance to the foliar diseases septoria nodorum blotch and tan spot in a global winter wheat collection

Abstract

Septoria nodorum blotch (SNB) and tan spot, caused by the necrotrophic fungal pathogens Parastagonospora nodorum and Pyrenophora tritici-repentis, respectively, often occur together as a leaf spotting disease complex on wheat (Triticum aestivum L.). Both pathogens produce necrotrophic effectors (NEs) that contribute to the development of disease. Here, genome-wide association analysis of a diverse panel of 264 winter wheat lines revealed novel loci on chromosomes 5A and 5B associated with sensitivity to the NEs SnTox3 and SnTox5 in addition to the known sensitivity genes for NEs Ptr/SnToxA, SnTox1, SnTox3, and SnTox5. Sensitivity loci for SnTox267 and Ptr ToxB were not detected. Evaluation of the panel with five P. nodorum isolates for SNB development indicated the Snn3-SnTox3 and Tsn1-SnToxA interactions played significant roles in disease development along with additional QTL on chromosomes 2A and 2D, which may correspond to the Snn7-SnTox267 interaction. For tan spot, the Tsc1-Ptr ToxC interaction was associated with disease caused by two isolates, and a novel QTL on chromosome 7D was associated with a third isolate. The Tsn1-ToxA interaction was associated with SNB but not tan spot. Therefore some, but not all, of the previously characterized host gene-NE interactions in these pathosystems play significant roles in disease development in winter wheat. Based on these results, breeders should prioritize the selection of resistance alleles at the Tsc1, Tsn1, Snn3, and Snn7 loci as well as the 2A and 7D QTL to obtain good levels of resistance to SNB and tan spot in winter wheat.

Supplementary information: The online version contains supplementary material available at 10.1007/s11032-023-01400-5.

Keywords: Association mapping; Disease resistance; Necrotrophic effector; Septoria nodorum blotch; Tan spot; Wheat.

Fig. 1

Boxplots showing the distribution of the average disease reaction scores in the winter wheat collection to P. nodorum isolates Sn4, Sn2000, AR2-1, SnIr05H71a, and NOR4, and the P. tritici-repentis isolates Pti2 (race1), 86–124 (race 2), DW5 (race 5), and AR CrossB10. P. nodorum was scored on a scale of 0–5 as described by Liu et al. (2004a), and P. tritici-repentis was scored on a scale of 1–5 as described by Lamari and Bernier (1989a)

Fig. 2

Scatter plot of the first two principal components (PC1 and PC2) derived from principal component analysis for this winter wheat panel. PC1 explained 13.9% and PC2 explained 9.2% of the total variation. Model-based cluster analysis using the first four PCs suggested there were 7 subgroups/classes

Fig. 3

Manhattan plots for the association mapping to sensitivity to the necrotrophic effectors SnToxA, SnTox1, SnTox3, and SnTox5. The mapping model used for SnToxA, SnTox1, and SnTox3 was MLM and for SnTox5 was Blink. The x-axis is the physical distribution of all the SNP markers on the 21 common wheat chromosomes based on the alignment to the IWGSC Chinese Spring Ref Seg v2. The y-axis is the –Log₁₀(FDR) for the SNP markers. Reactions were scores on a 0–3 scale as described by Zhang et al. (2011). To the right of each Manhattan plot is the Q-Q plot associated with that data and model used

Fig. 4

Manhattan plots for the association mapping to disease caused by various Parastagonospora nodorum isolates. The isolates are Sn4, Sn2000, AR2-1, SnIr05H71a, and NOR4, and the mapping model used for each isolate was MLM, Blink, MLM, Blink, and MLM, respectively. The x-axis is the physical distribution of all the SNP markers on the 21 common wheat chromosomes based on the alignment to the IWGSC Chinese Spring Ref Seg v2. The y-axis is the –Log₁₀(FDR) for the SNP markers. Reactions were scores on a 0–5 scale as described by Liu et al. (2004a). To the right of each Manhattan plot is the Q-Q plot associated with that data and model used

Fig. 5

Manhattan plots for the association mapping to disease caused by various Pyrenophora tritici-repentis isolates. The isolates are Pti2 (race 1), DW5 (race 5), and AR CrossB10, and the mapping model used for each isolate was Blink, Blink, and MLM, respectively. The x-axis is the physical distribution of all the SNP markers on the 21 common wheat chromosomes based on the alignment to the IWGSC Chinese Spring Ref Seg v2. The y-axis is the –Log₁₀(FDR) for the SNP markers. Reactions were scores on a 1–5 scale as described by Lamari and Bernier (1989a). To the right of each Manhattan plot is the Q-Q plot associated with that data and model used