Belowground pathogens rewire the phyllosphere microbiome in tomato plants

Background and aims: Plant-associated microbiomes play a critical role in host health, yet the effects of belowground pathogens on aboveground microbiomes remain poorly understood. Since systemic plant responses can alter microbial recruitment across organs, we hypothesized that plant-pathogen interactions belowground can trigger specific shifts in the phyllosphere microbiome. Methods: Here, we used a tomato microcosm system to test whether the presence of three pathogens in soil —Pseudomonas syringae pv. tomato, Fusarium oxysporum f.sp. lycopersici, and Alternaria alternata— alter the plant phyllosphere bacterial community. We characterized the phyllosphere bacterial community using 16S rRNA amplicon sequencing and inferred the effect of pathogens on microbial diversity, community structure, ecological strategies, co-occurrence network robustness, and assembly processes. Results: While overall diversity remained unchanged, we observed pathogen-specific signatures in community structure, ecological strategies, and assembly processes. In addition, exposure to belowground pathogens led to a reduction in microbial network robustness, a shift from specialist to generalist and competitor taxa, and pathogen-specific taxa enriched through selection. Conclusions: Our findings suggest that plants are able to modulate their leaf microbiome in response to different belowground pathogens, even in the absence of visible symptoms. While this helps us to better understand the interactions within the holobiont, our results contribute to the development of microbiome-based diagnostic tools, and the targeted design of beneficial microbial consortia for plant protection.