Pseudomonas simiae-induced resistance in barley is subject to pathogen-dependent gene expression regulation and not associated with major changes in the phyllosphere microbiome

Abstract

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. Although the molecular basis of IR has been extensively studied in Arabidopsis thaliana, considerably less is known about the underlying mechanisms in cereal crops. Here, we show that Pseudomonas simae WCS417r triggers IR in barley (Hordeum vulgare), reducing the propagation of Blumeria graminis f. sp. hordei, the causative agent of barley powdery mildew. Analysis of defense-associated marker genes revealed pathogen-dependent transcriptional responses during IR: HvPATHOGENESIS-RELATED1 (HvPR1) was induced by powdery mildew but not by the bacterial pathogen Xanthomonas translucens pathovar cerealis, whereas HvPR5 responded to both pathogens, with its induction by X. translucens depending on WCS417r-IR. To improve our molecular understanding of IR, transcriptomic responses to methyl jasmonate, salicylic acid and abscisic acid were characterized and used to identify hormone-responsive genes. Notably, several jasmonate-responsive genes were suppressed during powdery mildew infection, and this suppression was more pronounced in plants undergoing IR, indicative of priming. Finally, metabarcoding of the phyllosphere microbiome demonstrated that IR was not associated with major shifts in bacterial community composition. Alpha and beta diversity remained largely unchanged, while a limited number of amplicon sequence variants differed in abundance between treatments. Together, these results show that P. simiae WCS417r induces resistance against powdery mildew in barley through priming pathogen-dependent transcriptional changes while leaving the overall phyllosphere microbiome structure largely intact.