Ancient variation of the AvrPm17 gene in powdery mildew limits the effectiveness of the introgressed rye Pm17 resistance gene in wheat

Article


Müller, Marion C., Kunz, Lukas, Schudel, Seraina, Lawson, Aaron W., Kammerecker, Sandrine, Isaksson, Jonatan, Wyler, Michele, Graf, Johannes, Sotiropoulos, Alexandro G.s, Praz, Coraline R., Manser, Beatrice, Wicker, Thomas, Bourras, Salim and Keller, Beat. 2022. "Ancient variation of the AvrPm17 gene in powdery mildew limits the effectiveness of the introgressed rye Pm17 resistance gene in wheat." Proceedings of the National Academy of Sciences (PNAS). 119 (30). https://doi.org/10.1073/pnas.2108808119
Article Title

Ancient variation of the AvrPm17 gene in powdery mildew limits the effectiveness of the introgressed rye Pm17 resistance gene in wheat

Article CategoryArticle
AuthorsMüller, Marion C., Kunz, Lukas, Schudel, Seraina, Lawson, Aaron W., Kammerecker, Sandrine, Isaksson, Jonatan, Wyler, Michele, Graf, Johannes, Sotiropoulos, Alexandro G.s, Praz, Coraline R., Manser, Beatrice, Wicker, Thomas, Bourras, Salim and Keller, Beat
Journal TitleProceedings of the National Academy of Sciences (PNAS)
Journal Citation119 (30)
Article Numbere2108808119
Number of Pages12
Year2022
PublisherNational Academy of Sciences
Place of PublicationUnited States
ISSN0027-8424
1091-6490
Digital Object Identifier (DOI)https://doi.org/10.1073/pnas.2108808119
Web Address (URL)https://www.pnas.org/doi/full/10.1073/pnas.2108808119
Abstract

Introgressions of chromosomal segments from related species into wheat are important sources of resistance against fungal diseases. The durability and effectiveness of introgressed resistance genes upon agricultural deployment is highly variable—a phenomenon that remains poorly understood, as the corresponding fungal avirulence genes are largely unknown. Until its breakdown, the Pm17 resistance gene introgressed from rye to wheat provided broad resistance against powdery mildew (Blumeria graminis). Here, we used quantitative trait locus (QTL) mapping to identify the corresponding wheat mildew avirulence effector AvrPm17. It is encoded by two paralogous genes that exhibit signatures of reoccurring gene conversion events and are members of a mildew sublineage specific effector cluster. Extensive haplovariant mining in wheat mildew and related sublineages identified several ancient virulent AvrPm17 variants that were present as standing genetic variation in wheat powdery mildew prior to the Pm17 introgression, thereby paving the way for the rapid breakdown of the Pm17 resistance. QTL mapping in mildew identified a second genetic component likely corresponding to an additional resistance gene present on the 1AL.1RS translocation carrying Pm17. This gene remained previously undetected due to suppressed recombination within the introgressed rye chromosomal segment. We conclude that the initial effectiveness of 1AL.1RS was based on simultaneous introgression of two genetically linked resistance genes. Our results demonstrate the relevance of pathogen-based genetic approaches to disentangling complex resistance loci in wheat. We propose that identification and monitoring of avirulence gene diversity in pathogen populations become an integral part of introgression breeding to ensure effective and durable resistance in wheat.

Keywordswheat ; avirulence gene; gene conversion ; resistance introgression ; powdery mildew
ANZSRC Field of Research 2020310407. Host-parasite interactions
310510. Molecular evolution
310506. Gene mapping
Byline AffiliationsUniversity of Zurich, Switzerland
Max Planck Institute for Plant Breeding Research, Germany
Swedish University for Agricultural Sciences, Sweden
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