Pseudomonas simiae-induced resistance in barley is associated with compromised JA signaling and phyllosphere microbiome responses

Interactions of plant growth-promoting rhizobacteria with plant roots can trigger induced resistance (IR) protecting above-ground tissues from disease, a process that is increasingly recognized for its potential to support sustainable crop protection strategies. Here, we show that Pseudomonas simae WCS417r triggers IR in barley (Hordeum vulgare) and reduces the propagation of a Blumeria graminis f. sp. hordei challenge inoculum, the causative agent of barley powdery mildew. RNA-sequencing of IR-induced plants before and after the challenge infection revealed only few differentially expressed genes (DEGs) in response to the IR trigger, while the powdery mildew infection induced pronounced transcriptional reprogramming of barley. Notably, WCS417r-IR reduced the extent of transcriptional reprogramming in response to infection and further led to the differential regulation of a unique set of transcripts after infection, indicative of priming. Further, RNA-sequencing of barley leaves after their treatment with different phytohormones, allowed the identification of barley-specific marker genes for abscisic acid, jasmonate, and salicylate responses. The jasmonate-responsive markers were downregulated by a powdery mildew infection and this effect appeared exacerbated in response to WCS417r, associating early reactions of barley to powdery mildew with compromised JA responses. Finally, 16S rRNA gene amplicon sequencing of the phyllosphere microbiome revealed a moderate enrichment of certain beneficial microbes in the phyllosphere of WCS417r-treated barley. Together, the data disclose new aspects of barley defense against powdery mildew and reveal that WCS417r induces resistance through priming while potentially increasing overall fitness promoting beneficial microbes in the barley phyllosphere.