Javier Sánchez-Martín

Blumeria graminis f. sp. tritici ( Bgt) is a globally important fungal wheat pathogen. Some wheat genotypes contain powdery mildew resistance ( Pm) genes encoding immune receptors that recognize specific fungal-secreted effector proteins, defined as avirulence (Avr) factors. Identifying Avr factors is vital for understanding the mechanisms, functioning, and durability of wheat resistance. Here, we present AvrXpose, an approach to identify Avr genes in Bgt by generating gain-of-virulence mutants on Pm genes. We first identified six Bgt mutants with gain of virulence on Pm3b and Pm3c. They all had point mutations, deletions or insertions of transposable elements within the corresponding AvrPm3 b2/c2 gene or its promoter region. We further selected six mutants on Pm3a, aiming to identify the yet unknown AvrPm3 a3 recognized by Pm3a, in addition to the previously described AvrPm3 a2/f2 . Surprisingly, Pm3a virulence in the obtained mutants was always accompanied by an additional gain of virulence on the unrelated tandem kinase resistance gene WTK4. No virulence toward 11 additional R genes tested was observed, indicating that the gain of virulence was specific for Pm3a and WTK4. Several independently obtained Pm3a-WTK4 mutants have mutations in Bgt-646, a gene encoding a putative, nonsecreted ankyrin repeat-containing protein. Gene expression analysis suggests that Bgt-646 regulates a subset of effector genes. We conclude that Bgt-646 is a common factor required for avirulence on both a specific nucleotide-binding leucine-rich repeat and a WTK immune receptor. Our findings suggest that, beyond effectors, another type of pathogen protein can control the race-specific interaction between powdery mildew and wheat. [Formula: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license .

Summary Staying ahead of the arms race against rust and mildew diseases in cereal crops is essential to maintain and preserve food security. The methodological challenges associated with conventional resistance breeding are major bottlenecks for deploying resistance ( R ) genes in high‐yielding crop varieties. Advancements in our knowledge of plant genomes, structural mechanisms, innovations in bioinformatics, and improved plant transformation techniques have alleviated this bottleneck by permitting rapid gene isolation, functional studies, directed engineering of synthetic resistance and precise genome manipulation in elite crop cultivars. Most cloned cereal R genes encode canonical immune receptors which, on their own, are prone to being overcome through selection for resistance‐evading pathogenic strains. However, the increasingly large repertoire of cloned R genes permits multi‐gene stacking that, in principle, should provide longer‐lasting resistance. This review discusses how these genomics‐enabled developments are leading to new breeding and biotechnological opportunities to achieve durable rust and powdery mildew control in cereals.