Interaction-Dependent Gene Expression in Mla-Specified Response to Barley Powdery Mildew

Abstract

<p>Plant recognition of pathogen-derived molecules influences attack and counterattack strategies that affect the outcome of host–microbe interactions. To ascertain the global framework of host gene expression during biotrophic pathogen invasion, we analyzed in parallel the mRNA abundance of 22,792 host genes throughout 36 (genotype × pathogen × time) interactions between barley (<em>Hordeum vulgare</em>) and <em>Blumeria graminis</em> f. sp <em>hordei</em> (<em>Bgh</em>), the causal agent of powdery mildew disease. A split-split-plot design was used to investigate near-isogenic barley lines with introgressed <em>Mla6</em>, <em>Mla13</em>, and <em>Mla1</em> coiled-coil, nucleotide binding site, Leu-rich repeat resistance alleles challenged with <em>Bgh</em> isolates 5874 (<em>AvrMla6</em> and <em>AvrMla1</em>) and K1 (<em>AvrMla13</em> and <em>AvrMla1</em>). A linear mixed model analysis was employed to identify genes with significant differential expression (P value < 0.0001) in incompatible and compatible barley-<em>Bgh</em> interactions across six time points after pathogen challenge. Twenty-two host genes, of which five were of unknown function, exhibited highly similar patterns of upregulation among all incompatible and compatible interactions up to 16 h after inoculation (hai), coinciding with germination of <em>Bgh</em> conidiospores and formation of appressoria. By contrast, significant divergent expression was observed from 16 to 32 hai, during membrane-to-membrane contact between fungal haustoria and host epidermal cells, with notable suppression of most transcripts identified as differentially expressed in compatible interactions. These findings provide a link between the recognition of general and specific pathogen-associated molecules in gene-for-gene specified resistance and support the hypothesis that host-specific resistance evolved from the recognition and prevention of the pathogen's suppression of plant basal defense.</p>