Downy mildew disease-suppressive soils transmit a protective core microbiome to the phyllosphere

Plants can respond to pathogen attack by assembling disease-suppressive microbiomes. In Arabidopsis thaliana, infection by the obligate foliar downy mildew pathogen Hyaloperonospora arabidopsidis (Hpa) consistently led to the formation of a soil microbial community, referred to as "soilborne legacy" (SBL), that enhanced resistance in subsequent plant populations grown in the same soil. Previous work identified an enrichment of specific "Hpa-associated microbiota" (HAM) in the phyllospheres of infected plants, which suppressed pathogen proliferation. Here, we demonstrate how the assembly of protective HAM in the phyllosphere contributes to a disease-suppressive SBL. We identified a community of 25 core-HAM that consistently dominated the phyllospheres of 14 sets of distinct Hpa-infected plant populations across six independent experiments. Using HAM-free, gnotobiotic Hpa spores, the infection-driven assembly of a core-HAM representative was recapitulated, showing de novo and progressive enrichment under sustained disease pressure. Despite being transmitted via soil as SBL, HAM are phyllosphere specialists with infected leaves as their primary niche. Disease-induced HAM assembly is initiated in the phyllosphere rather than the rhizosphere, and once transmitted, they particularly accumulate on aboveground tissues. Leaf wash-offs from plant populations that inherited SBL were shown to effectively suppress downy mildew disease when applied to leaves of plants grown in unconditioned soil. These findings reveal that downy mildew disease-suppressive soils transmit a protective core microbiome to the phyllosphere, highlighting a crucial link between belowground and aboveground plant-driven microbiome assembly processes. Paradoxically, the phyllosphere thus emerges as a key assembly hub for disease-suppressive soil microbiomes.