Cross-niche metabolite-microbiome interactions orchestrate systemic soybean resistance to Fusarium root rot

Fusarium root rot, predominantly caused by Fusarium falciforme, poses a significant threat to soybean productivity globally. Microbiome-based strategies offer sustainable alternatives, but the mechanisms underlying multi-niche interactions remain elusive. Here, we found that a tolerant soybean cultivar (GXD2) coordinates spatially resolved metabolite signals to recruit beneficial microbes across the rhizosphere, root endosphere, and leaf endosphere. Specifically, formononetin and maltol selectively enrich Bacillus and Massilia in the rhizosphere; arctigenin and isovanillic acid recruit Bacillus and Streptomyces to the root endosphere; and flavonoids such as diosmetin attract Penicillium and Aspergillus to the leaf endosphere. Leveraging these interactions, we constructed different types of synthetic communities (SynComs) via top-down (host-selected taxa) and bottom-up (antagonist-based) strategies. Both SynComs suppressed root rot in susceptible cultivars, with foliar application of top-down SynComs significantly enhancing shoot growth. Transcriptomics revealed distinct modes of actions, that top-down SynComs activated mitogen-activated protein kinase (MAPK)-linked terpenoid and flavonoid pathways, whereas bottom-up SynComs primarily modulated host carbon-nitrogen allocation, effectively limiting pathogen resources. Our findings unveil a "metabolite-mediated, multi-niche collaborative defense" model, presenting a robust framework for microbiome-based disease management and paving the way toward sustainable crop protection strategies.