Induced systemic resistance impacts the phyllosphere microbiome through plant-microbe-microbe interactions

Both above- and below-ground parts of plants are constantly confronted with microbes, which are main drivers for the development of plant-microbe interactions. Plant growth-promoting rhizobacteria enhance the immunity of above-ground tissues, which is known as induced systemic resistance (ISR). We show here that ISR also influences the leaf microbiome. We compared ISR triggered by the model strain Pseudomonas simiae WCS417r (WCS417) to that triggered by Bacillus thuringiensis israelensis (Bti) in Arabidopsis thaliana. In contrast to earlier findings, immunity elicited by both strains depended on salicylic acid. Both strains further relied on MYC2 for signal transduction in the plant, while WCS417-elicited ISR additionally depended on SAR-associated metabolites, including pipecolic acid. A metabarcoding approach applied to the leaf microbiome revealed a significant ISR-associated enrichment of amplicon sequence variants with predicted plant growth-promoting properties. WCS417 caused a particularly dramatic shift in the leaf microbiota with more than 50% of amplicon reads representing two bacterial species: WCS417 and Flavobacterium sp.. Co-inoculation experiments using WCS417 and At-LSPHERE Flavobacterium sp. Leaf82, suggest that the proliferation of these bacteria is influenced by both microbial and plant-derived factors. Together, our data connect systemic immunity with leaf microbiome dynamics and highlight the importance of plant- microbe-microbe interactions for plant health.