Downy mildew disease-suppressive soils transmit a protective core microbiome to the phyllosphere
Plants can respond to pathogen attack by assembling disease-suppressive soil 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, termed the 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. However, the relationship between rhizosphere and phyllosphere microbiota in generating the SBL and assembling protective HAM remained unclear. Here, 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 the core-HAM member Sphingobium ASV ed6be was recapitulated, showing de novo and progressive accumulation under sustained disease pressure. Although HAM transmission in SBL occurred via soil, these bacteria were shown to be phyllosphere specialists, accumulating more abundantly on aboveground than belowground tissues. Moreover, leaf wash-offs from plant populations that inherited SBL, effectively suppressed 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 central hub for the accumulation of disease-suppressive soil microbiomes.