Decoupling the "attract-and-kill" strategy: Independent zoospore attraction and ROS-executed killing synergistically drive disease-suppressive intercropping.

Soilborne Phytophthora diseases pose a major threat to agricultural sustainability. However, how nonhost roots disrupt the transmission of soilborne Phytophthora pathogens without relying solely on classical antimicrobial exudates remains poorly understood. Through a decade-long field study, we demonstrate that strip intercropping can sustainably suppress disease incidence by up to 46.85% by leveraging nonhost roots as ecological barriers that intercept zoospore transmission. Moving beyond the conventional focus on antimicrobial exudates, we resolve the "attract-and-kill" strategy into two discrete functions: a broad-spectrum attraction function widespread among nonhost plants (13 of 15 genera), which alone reduces disease incidence by 9.2%-24.4%, and a specialized killing function restricted to a few species, such as garlic, in which elevated concentrations of sulfur compounds at the root interface induce cystospore rupture and inhibit germination, delivering 42.9%-49.3% field suppression. The synergy between universal attraction and targeted killing enhances disease suppression at the rhizosphere interface. Mechanistically, killing is executed through a conserved reactive oxygen species-programmed cell death (ROS-PCD) pathway, with pathogen sensitivity determined by intrinsic redox-buffering capacity. Metagenomic profiling further revealed that garlic roots and sulfur compounds are associated with the enrichment of genes involved in microbial motility and apoptosis-related pathways, adding a complementary mechanistic layer to the attract-and-kill framework. We thus propose this ecology-based, two-component strategy for sustainable Phytophthora management in diversified cropping systems.