Comparative Transcriptomic and Microscopic Analyses of a Wild Wheat Relative Reveal Novel Mechanisms of Immune Suppression by the Pathogen Zymoseptoria tritici.

The plant pathogenic fungus Zymoseptoria tritici is the causal agent of the devasting Septoria tritici blotch, a major wheat disease, with limited resistance genes identified. Aegilops cylindrica, a wild relative of wheat, is resistant to Z. tritici isolates originating from cultivated wheat but susceptible to Z. tritici isolates derived from Aegilops species. Therefore, A. cylindrica provides an intriguing model system to identify novel resistance genes against Z. tritici. We here integrated plant infection experiments, advanced microscopy and comparative transcriptome analyses to identify new putative resistance mechanisms against Z. tritici. We therefore constructed a de novo transcriptome assembly of A. cylindrica during compatible and incompatible plant-pathogen interactions across different infection stages using the two Z. tritici isolates Zt469 and IPO323. Our microscope analyses identify the substomatal cavity as a crucial checkpoint for Z. tritici infection where infection by incompatible isolates is aborted. In the compatible interaction, based on the transcriptome analyses, we reveal suppression of several key resistance-associated genes, including homologues of known resistance genes (e.g., RPM1- and RPP13-like) and certain pathogenesis related (PR) genes encoding various lipid transfer proteins (PR-14) and an apoplastic subtilisin-like protease SBT3.6-like (PR-7), none so far known to be involved in resistance towards Z. tritici. In the incompatible interaction we find a different set of upregulated genes compared to genes up-regulated in the immune response in resistant wheat cultivars. The de novo transcriptome assembly presented here provides a new valuable resource for wheat genetics and points novel immune pathways which may determine resistance against Z. tritici.