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.

Footnotes

* In this revision, we changed the description of the group of genes under study. Instead of "homologs of common symbiosis genes" (HCSGs), we have now used an acronym that represents a neutral list of the products of these genes. There are also numerous smaller text changes to improve the clarity of the discussion. Former Figure 3 - Figure Supplement 3 is now part of Figure 2. Data concerning the reproductive success of E. cruciferarum can now be found in Figures 3 and S9. PR1 expression in a cpr5 mutant has been added to Figure 4. Data showing that the cell death response is unaltered in the analysed mutants can now be found in Figure 5 instead of the supplemental information. Alignments of the Lotus common symbiosis genes and closely related Arabidopsis genes have been added to sthe supplemental information. To allow for a continuous documentation of haustoria shape by life cell imaging during development, we changed the marker used in fluorescence microscopy from YFP-AtREM1.2 to RPW8.2-YFP. As a consequence Figure 2 - S4 was replaced with Figure 2 e.