A set of Arabidopsis genes involved in the accommodation of the downy mildew pathogen Hyaloperonospora arabidopsidis

Abstract The intracellular accommodation structures formed by plant cells to host arbuscular mycorrhiza fungi and biotrophic hyphal pathogens are cytologically similar but it remains unclear whether these interactions build on an overlapping genetic framework. In legumes, the malectin-like domain leucine-rich repeat receptor kinase SYMRK, the cation channel POLLUX and members of the nuclear pore NUP107-160 subcomplex are essential for symbiotic signal transduction and arbuscular mycorrhiza development. Here we identified members of these three groups in Arabidopsis thaliana and explored their impact on the interaction with the oomycete downy mildew pathogen Hyaloperonospora arabidopsidis (Hpa). We report that mutations in the corresponding genes reduced the reproductive success of Hpa as determined by sporangiophore and spore counts. We discovered that a developmental transition of haustorial shape occurred significantly earlier and at higher frequency in the mutants. Analysis of the multiplication of extracellular bacterial pathogens, Hpa-induced cell death or callose accumulation, as well as Hpa- or flg22-induced defence marker gene expression, did not reveal any traces of constitutive or exacerbated defence responses. These findings point towards an overlap between the plant genetic toolboxes involved in the interaction with biotrophic intracellular hyphal symbionts and pathogens in terms of the gene families involved. Author Summary Our work reveals genetic commonalities between biotrophic intracellular interactions with symbiotic and pathogenic hyphal microbes. The majority of land plants engages in arbuscular mycorrhiza (AM) symbiosis with phosphate-acquiring arbuscular mycorrhizal fungi to avoid phosphate starvation. Nutrient exchange in this interaction occurs via arbuscules, tree-shaped fungal structures, hosted within plant root cells. A series of plant genes including the Symbiosis Receptor-like kinase (SYMRK), members of the NUP107-160 subcomplex and nuclear envelope localised cation channels are required for a signalling process leading to the development of AM. The model plant Arabidopsis thaliana lost the ability to form AM. Although the ortholog of SYMRK was deleted during evolution, members of the malectin-like domain leucine-rich repeat receptor kinases (MLD-LRR-RKs) gene family, components of the NUP107-160 subcomplex, and an ortholog of the nuclear envelope-localized cation channel POLLUX, are still present in the Arabidopsis genome, and Arabidopsis leaf cells retained the ability to accommodate haustoria, presumed feeding structures of the obligate biotrophic downy mildew pathogen Hyaloperonospora arabidopsidis. We discovered that both of these plant-microbe interactions utilize a corresponding set of genes including the ortholog of POLLUX, members of the NUP107-160 subcomplex and members of the MLD-LRR-RK gene family, thus revealing similarities in the plant program for the intracellular accommodation of biotrophic organisms in symbiosis and disease.