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

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.

Doomed by popularity: The broad use of the Pm8 resistance gene in wheat resulted in hypermutation of the AvrPm8 gene in the powdery mildew pathogen

“…In order to identify the AvrPm8 gene we performed GWAS, using a diversity panel of 79 B.g. tritici isolates from a worldwide collection (Sotiropoulos et al ., 2022) and the chromosome-scale genome assembly of Pm8 avirulent isolate ISR_7 (Müller et al ., 2022) as a reference (Fig. 1a).…”

“…1f) and high expression levels during early infection stages (Fig. S2) (Bourras et al ., 2015; Praz et al ., 2017; Bourras et al ., 2019; Hewitt et al ., 2020; Müller et al ., 2022). BgISR7-10067 was therefore considered an excellent AvrPm8 candidate gene.…”

“…The newly identified AvrPm8 is no exception to this rule and exhibits common features like small size, presence of a signal peptide, a Y/FxC motif, and a conserved cysteine towards the C-terminus. Like AvrPm17, it furthermore belongs to effector family E003, previously shown to contain effectors with a predicted RNAse-like structure (Saur et al ., 2019; Bauer et al ., 2021; Müller et al ., 2022). The recently identified AvrPm3 a2/f2 , AvrPm3 b2/c2 , AvrPm3 d3 and AvrPm17 , are recognized by NLRs encoded by the Pm3 allelic series and the Pm3 homologous rye NLR Pm17, respectively.…”

“…The NLR proteins encoded by the Pm3 allelic series and Pm17 , where shown to provide race specific resistance against B.g. tritici through recognition of mildew encoded effector proteins (avirulence factors, AVRs ) (Brunner et al ., 2010; Bourras et al ., 2015; Bourras et al ., 2019; Müller et al ., 2022). The B.g.…”

“…For example, gain-of-virulence mutations in the AvrPm3 and AvrPm17 effector genes were exclusively found to generate single amino acid polymorphisms, likely allowing B.g. tritici to evade NLR recognition while preserving effector virulence function (McNally et al ., 2018; Bourras et al ., 2019; Müller et al ., 2022).…”