The <i>Zymoseptoria tritici</i> Avirulence Factor AvrStb6 Accumulates in Hyphae Close to Stomata and Triggers a Wheat Defense Response Hindering Fungal Penetration

Background Septoria tritici blotch (STB), caused by the foliar fungus Zymoseptoria tritici, is one of the most damaging disease of wheat in Europe. Genetic resistance against this fungus relies on different types of resistance from non-host resistance (NHR) and host species specific resistance (HSSR) to host resistance mediated by quantitative trait loci (QTLs) or major resistance genes (Stb). Characterizing the diversity of theses resistances is of great importance for breeding wheat cultivars with efficient and durable resistance. While the functional mechanisms underlying these resistance types are not well understood, increasing piece of evidence suggest that fungus stomatal penetration and early establishment in the apoplast are both crucial for the outcome of some interactions between Z. tritici and plants. To validate and extend these previous observations, we conducted quantitative comparative phenotypical and cytological analyses of the infection process corresponding to 22 different interactions between plant species and Z. tritici isolates. These interactions included four major bread wheat Stb genes, four bread wheat accessions with contrasting quantitative resistance, two species resistant to Z. tritici isolates from bread wheat (HSSR) and four plant species resistant to all Z. tritici isolates (NHR). Results Infiltration of Z. tritici spores into plant leaves allowed the partial bypass of all bread wheat resistances and durum wheat resistance, but not resistances from other plants species. Quantitative comparative cytological analysis showed that in the non-grass plant Nicotiana benthamiana, Z. tritici was stopped before stomatal penetration. By contrast, in all resistant grass plants, Z. tritici was stopped, at least partly, during stomatal penetration. The intensity of this early plant control process varied depending on resistance types, quantitative resistances being the least effective. These analyses also demonstrated that Stb-mediated resistances, HSSR and NHR, but not quantitative resistances, relied on the strong growth inhibition of the few Z. tritici penetrating hyphae at their entry point in the sub-stomatal cavity. Conclusions In addition to furnishing a robust quantitative cytological assessment system, our study uncovered three stopping patterns of Z. tritici by plant resistances. Stomatal resistance was found important for most resistances to Z. tritici, independently of its type (Stb, HSSR, NHR). These results provided a basis for the functional analysis of wheat resistance to Z. tritici and its improvement.

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A novel genome-wide association approach reveals wheat pathogen genes involved in host specialization

Lorrain,

Feurtey,

Alassimone

et al. 2024

Preprint

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Plant-pathogenic microbes, including the wheat fungal pathogen Zymoseptoria tritici, adapt to their host environment. In plants, genome-wide association studies (GWAS) have been extensively used to uncover the complexity of local adaptation and disease resistance. However, the application of GWAS to decipher the mechanisms underlying fungal pathogenicity and host adaptation trails far behind. Here, we established a genome-host association (GHA) approach to infer statistical associations between pathogen allele frequencies and host of origin for 832 fungal strains isolated from twelve different host cultivars during a natural field epidemic. We identified from two to twenty genes associated with specialization to the different wheat cultivars, including one known effector gene that provided a proof-of-concept for our GHA approach, as well as two new virulence-related genes that we validated with targeted gene knockouts. Our study highlights the polygenic genetic architecture of host adaptation and provides a novel application of GWAS in plant pathogens that transcends the limitations imposed by traditional phenotyping methods.

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The Zymoseptoria tritici Avirulence Factor AvrStb6 Accumulates in Hyphae Close to Stomata and Triggers a Wheat Defense Response Hindering Fungal Penetration

Cited by 3 publications

References 69 publications

Entrance Denied: Deciphering the Transcriptional Circuitry of Wheat Resistance to Zymoseptoria tritici

Entrance Denied: Deciphering the Transcriptional Circuitry of Wheat Resistance to Zymoseptoria tritici

Stomatal penetration: the cornerstone of plant resistance to the fungal pathogen Zymoseptoria tritici

A novel genome-wide association approach reveals wheat pathogen genes involved in host specialization

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