A biGWAS strategy reveals the genetic architecture of the interaction between wheat andBlumeria graminis f. sp.tritici
Authored by Jingzhong Xie, Qiaoling Luo, Limin Wang, Dan Qiu, Caihong Zhao, Jinghuang Hu, Jing Zhang, Xinyu Zhao, Zhaogen Chen, Yibo Wang, Yang Yu, Mengzhen Luo, Haoyuan Song, Yuexuan Hou, Zhimeng Zhang, Mou Yin, Haojie Wang, Xuanzhao Li, Xiaomeng Fu, Bei Xiao, Yahui Li, Jiajie Wu, Wenxuan Liu, Yanpeng Wang, Mo Zhu, Yanming Zhang, Alisdair R. Fernie, Wei Wang, Hongjie Li, and
Fei He
Posted
April 15, 2025
Server
bioRxiv
Background Wheat powdery mildew, caused byBlumeria graminis f. sp.tritici (Bgt ) is one of the most significant diseases affecting global wheat production. Breeding for disease resistance (R ) genes againstBgt often 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 cloningR genes, Avr genes remain relatively understudied, limiting our understanding of R-Avr interactions. That said, understandingR-Avr interactions is crucial for developing durable resistance strategies.
Results We conducted whole genome sequencing on 245Bgt isolates 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 bothBgt and wheat, we identified 65Avr loci and 251R loci overlapping with nine and eight clonedAvr orR genes, respectively. On average, each isolate carries eightAvr alleles, ranging from one to 17. Little geographical preference forAvr alleles 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 ofR alleles carried by a wheat line, and the average frequency of anR allele is 2% among the wheat panel, indicating the potential for accumulatingR alleles in breeding programs. We mapped 212R-Avr interactions 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 majorR loci has the potential to confer resistance to half of theAvr loci. As a proof of concept, we successfully verified two previously describedR -Avr pairs using tobacco experiments. Furthermore, we provided molecular validation evidence for three newAvr genes, includingBgt-50651 ,BgtE-5826 andBgtE-20009 , and two newR-Avr interactions. Among them,Bgt-50651 interacts withPm1a ,Pm2a , and another unidentifiedR gene located near thePm6 /Pm52 interval.
Conclusion Our study provides a framework for understanding the genetic interaction between plants and pathogens. The discovery of novelR /Avr loci and their complex interaction network underscores the need to integrate crop and pathogen genetic background, particularly theR /Avr allele 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.
