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Background

Wheat powdery mildew, caused byBlumeria graminisf. sp.tritici(Bgt) is one of the most significant diseases affecting global wheat production. Breeding for disease resistance (R) genes againstBgtoften follows a ‘boom-bust’ cycles, where cultivars with effective resistance are widely deployed on an expanding area until virulence emerges in the avirulence (Avr) pathogen population. While extensive effort has been devoted to identifying and cloningRgenes, Avr genes remain relatively understudied, limiting our understanding of R-Avr interactions. That said, understandingR-Avrinteractions is crucial for developing durable resistance strategies.

Results

We conducted whole genome sequencing on 245Bgtisolates collected from major wheat-growing regions in China, identifying 120 genetically unique isolates. Each of these unique isolates was inoculated and phenotyped on a diverse panel of wheat germplasm. Through Genome-Wide Association Analysis (GWAS) in bothBgtand wheat, we identified 65Avrloci and 251Rloci overlapping with nine and eight clonedAvrorRgenes, respectively. On average, each isolate carries eightAvralleles, ranging from one to 17. Little geographical preference forAvralleles or their combinations was observed, suggesting that disease resistance breeding against this pathogen should be coordinated at the national level. The level of resistance level is positively correlated with the number ofRalleles carried by a wheat line, and the average frequency of anRallele is 2% among the wheat panel, indicating the potential for accumulatingRalleles in breeding programs. We mapped 212R-Avrinteractions based on joint GWAS using both plant and pathogen genomes and cross-species epistasis, where a network of interactions was formed between wheat andBgt. These interactions indicate that pyramiding five majorRloci has the potential to confer resistance to half of theAvrloci. As a proof of concept, we successfully verified two previously describedR-Avrpairs using tobacco experiments. Furthermore, we provided molecular validation evidence for three newAvrgenes, includingBgt-50651,BgtE-5826andBgtE-20009, and two newR-Avrinteractions. Among them,Bgt-50651interacts withPm1a,Pm2a, and another unidentifiedRgene located near thePm6/Pm52interval.

Conclusion

Our study provides a framework for understanding the genetic interaction between plants and pathogens. The discovery of novelR/Avrloci and their complex interaction network underscores the need to integrate crop and pathogen genetic background, particularly theR/Avrallele composition, into breeding program design. These findings have significant implications for developing durable resistance strategies in wheat alongside offering valuable insights into the broader dynamics of plant-pathogen interactions.