Two pathogen loci determine Blumeria graminis f. sp. tritici virulence to wheat resistance gene Pm1a

Authors: KLOPPE, TIM - North Carolina State University; Whetten, Rebecca; KIM, SAET-BYUL - North Carolina State University; POWELL, OLIVER - John Innes Center; LUCK, STEFANIE - Leibniz Institute Of Plant Genetics And Crop Plant Research; DOUCHKOV, DIMITAR - Leibniz Institute Of Plant Genetics And Crop Plant Research; WHETTEN, ROSS - North Carolina State University; Hulse-Kemp, Amanda; Balint-Kurti, Peter; Cowger, Christina

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/26/2023
Publication Date: 2/11/2023
Citation: Kloppe, T., Whetten, R.B., Kim, S., Powell, O., Luck, S., Douchkov, D., Whetten, R., Hulse-Kemp, A.M., Balint Kurti, P.J., Cowger, C. 2023. Two pathogen loci determine Blumeria graminis f. sp. tritici virulence to wheat resistance gene Pm1a. New Phytologist. 238:1546-1561. https://doi.org/10.1111/nph.18809.
DOI: https://doi.org/10.1111/nph.18809

Interpretive Summary: The fungus Blumeria graminis f. sp. tritici (Bgt) causes wheat powdery mildew, which is damaging to wheat in many parts of the world. Wheat resistance genes (Pm genes) can be quickly overcome when the pathogen evolves to become virulent to them. Even though the resistance gene Pm1a has been used in U.S. wheat production, virulence to it has disappeared from the Bgt population quickly when the gene is withdrawn from production. By contrast, in the Bgt populations from other countries, Pm1a virulence seems to persist. We thought there might be a unique virulence mutation in U.S. Bgt that is different from the one(s) in other countries. We did a genome-wide association study (GWAS) on 216 Bgt strains from six continents, including the U.S. We did find a virulence mutation apparently unique to the U.S. in the avirulence gene AvrPm1a on Bgt chromosome 6, which had previously been mapped by other researchers and shown to trigger and immune response (avirulence) in the presence of wheat resistance gene Pm1a. In addition, we found another gene on chromosome 8 of Bgt and confirmed that it also triggers an immune response (avirulence) when there is interaction with Pm1a. This second gene, BgtE-51526, is part of the same family of Bgt genes as AvrPm1a. In our study, 95% of the virulent or avirulent reactions that occurred when the 216 Bgt strains were individually inoculated onto Pm1a-bearing wheat leaves were explained by a model in which both AvrPm1a and BgtE-51526 could interact with Pm1a. Further, proteins predicted to be encoded by the two genes share 89% of their structure. This is the first time in the Bgt-wheat disease system in which two different pathogen genes have been shown to trigger avirulence through an interaction with the same host resistance gene. That a pathogen isolate must have virulence mutations at both genetic loci in order to escape wheat host recognition may help explain why Pm1a virulence is so low in the U.S., because frequencies of virulence-associated alleles are low at both loci.

Technical Abstract: Blumeria graminis f. sp. tritici (Bgt) is a globally important fungal pathogen of wheat that can rapidly evolve to defeat wheat powdery mildew (Pm) resistance genes. Despite periodic regional deployment of the Pm1a resistance gene in US wheat production, Bgt strains that overcome Pm1a have been notably nonpersistent in the United States, while on other continents, they are more widely established. A genome-wide association study (GWAS) was conducted to map sequence variants associated with Pm1a virulence in 216 Bgt isolates from six countries, including the United States. A virulence variant apparently unique to Bgt isolates from the United States was detected in the previously mapped gene AvrPm1a (BgtE-5612) on Bgt chromosome 6; an in vitro growth assay suggested no fitness reduction associated with this variant. A gene on Bgt chromosome 8, Bgt-51526, was shown to function as a second determinant of Pm1a virulence, and despite <'30% amino acid identity, BGT-51526 and BGTE-5612 were predicted to share >'85% of their secondary structure. A co-expression study in Nicotiana benthamiana showed that BGTE-5612 and BGT-51526 each produce a PM1A-dependent hypersensitive response. More than one member of a B. graminis effector family can be recognized by a single wheat immune receptor, and a two-gene model is necessary to explain virulence to Pm1a.