Decoupling the ‘Attract-and-Kill’ Strategy: Independent Functions for Zoospore Attraction and ROS-Executed Killing Synergize in Disease-Suppressive Intercropping

Soilborne Phytophthora diseases pose a major threat to agricultural sustainability. How non-host roots disrupt the transmission of soilborne Phytophthora pathogens without relying on classical antimicrobial exudates remains unknown. Through a decade-long field study, we demonstrate that strip intercropping achieves sustainable disease suppression (up to 46.85%) by leveraging non-host roots as ecological barriers that intercept zoospore transmission. Moving beyond the conventional focus on antimicrobial exudates, we decouple the 'attract-and-kill' strategy into two discrete functions: a broad-spectrum attraction function widespread among non-host plants (13 of 15 genera), which alone reduces disease by 9.2-24.4%; and a specialized killing function restricted to few species (e.g., garlic), where elevated root-interface concentrations of sulfur compounds induce cystospore rupture and germination inhibition, delivering 42.9-49.3% field suppression. The synergy of universal attraction and targeted killing intensifies efficacy at the rhizosphere interface. Mechanistically, killing is executed through a conserved ROS-PCD pathway, with pathogen sensitivity determined by intrinsic redox-buffering capacity. Metagenomic profiling further revealed that garlic roots and sulfur compounds enrich microbial motility genes and apoptosis pathways, adding a complementary mechanistic layer to the 'attract and kill'framework. We thus propose this two-component, ecology-based strategy for sustainable Phytophthora management in diversified cropping systems.