Mutagenesis of wheat powdery mildew reveals a single gene controlling both NLR and tandem kinase-mediated immunity

Article


Bernasconi, Zoe, Stirnemann, Ursin, Heuberger, Matthias, Sotiropoulos, Alexandros, Graf, Johannes, Wicker, Thomas, Keller, Beat and Sánchez-Martín, Javier. 2023. "Mutagenesis of wheat powdery mildew reveals a single gene controlling both NLR and tandem kinase-mediated immunity." Molecular Plant-Microbe Interactions. https://doi.org/10.1094/MPMI-09-23-0136-FI
Article Title

Mutagenesis of wheat powdery mildew reveals a single gene controlling both NLR and tandem kinase-mediated immunity

ERA Journal ID2766
Article CategoryArticle
AuthorsBernasconi, Zoe, Stirnemann, Ursin, Heuberger, Matthias, Sotiropoulos, Alexandros, Graf, Johannes, Wicker, Thomas, Keller, Beat and Sánchez-Martín, Javier
Journal TitleMolecular Plant-Microbe Interactions
Year2023
PublisherAmerican Phytopathological Society
Place of PublicationUnited States
ISSN0894-0282
1943-7706
Digital Object Identifier (DOI)https://doi.org/10.1094/MPMI-09-23-0136-FI
Web Address (URL)https://apsjournals.apsnet.org/doi/abs/10.1094/MPMI-09-23-0136-FI
Abstract

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 effectors proteins, then defined as avirulence (Avr) factors. Identifying Avr factors is vital for understanding the mechanisms, function, 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 AvrPm3b2/c2 gene or its promoter region. We further selected six mutants on Pm3a, aiming to identify the yet unknown AvrPm3a3 recognized by Pm3a, in addition to the previously described AvrPm3a2/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 towards 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, non-secreted 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 NLR 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.

KeywordsAvrXpose; transposable elements; avirulence factors; effectors; mutagenesis; Blumeria graminis; tandem kinase proteins; NLR; race-specific resistance; wheat
ANZSRC Field of Research 2020310599. Genetics not elsewhere classified
310704. Microbial genetics
310407. Host-parasite interactions
Byline AffiliationsUniversity of Zurich, Switzerland
Centre for Crop Health
University of Salamanca, Spain
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