Plant–metabolite–microbe interactions play essential roles in disease suppression. Most studies focus on the root exudates and rhizosphere microbiota to fight soil-borne pathogens, but it is poorly understood whether the changes in phyllosphere metabolites can actively recruit beneficial microbes to enhance disease resistance. In this study, the differences of phyllosphere microbial communities and key leaf metabolites were systematically explored in resistant and susceptible black currant cultivars related to powdery mildew (PM) by integrating microbiome and metabolomic analyses. The results showed that the diversity and composition of microbiome changed, as highlighted by a reduction in microbial alpha-diversity and beta-diversity of susceptible cultivars. An increasing fungal network complexity and a decreasing bacterial network complexity occurred in resistant cultivar. Bacillus, Burkholderia (bacteria), and Penicillium (fungi) were identified as keystone microorganisms and resistance effectors in resistant cultivar. Metabolites such as salicylic acid, trans-zeatin, and griseofulvin were more abundant in resistant cultivar, which had a positive regulatory effect on the abundance of bacterial and fungal keystones. These findings unravel that resistant cultivar can enrich beneficial microorganisms by adjusting leaf metabolites, thus showing the external disease-resistant response. Moreover, the reduced stomatal number and increased tissue thickness were observed in resistant cultivar, suggesting inherent physical structure also provides a basic defense against PM pathogens. Therefore, resistant black currant cultivar displayed multilevel defense responses of physical structures, metabolites, and microorganisms to PM pathogens. Collectively, our study highlights the potential for utilizing phyllosphere microbiome dynamics and metabolomic adjustments in agricultural practices, plant breeding, and microbiome engineering to develop disease-resistant crops.

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