Plant-driven assembly and maintenance of disease-suppressive soil microbiomes in a changing climate

Disease-suppressive soils are a fundamental aspect of sustainable agriculture, where native microbiomes help control soilborne pathogens through antagonistic interactions, protecting plant health even in favorable environmental conditions. This review synthesizes the current understanding of how plants actively assemble and maintain protective root microbiomes, a process that initiates and sustains this suppressiveness. The mechanistic depth of this synthesis is anchored primarily in annual cereal and vegetable crop systems, where the genetic, chemical, and ecological bases of plant-driven suppression have been most extensively characterized. While illustrative examples from perennial and woody systems are included to highlight specific principles, a comprehensive treatment of their distinct assembly dynamics, shaped by root persistence and long-term legacy accumulation, lies beyond the scope of this review. We detail how plants recruit beneficial microbes through a dynamic dialogue involving root exudates and immune system modulation, creating rhizosphere hotspots that enrich for protective consortia. This assembly is governed by host genetics, which shapes microbial recruitment and the plant's responsiveness to beneficial feedback. Critically, these interactions foster self-reinforcing legacies, where pathogen-induced stress reprograms exudate profiles to recruit suppressors, establishing durable microbiome shifts that confer intergenerational protection. However, escalating climate change threatens this equilibrium by perturbing microbial community structure, reducing beneficial diversity, favoring opportunistic pathogens, and eroding suppression efficacy. By integrating plant-microbe communication with soil-borne disease ecology, this perspective illuminates strategies for breeding crops and engineering soils to harness protective feedbacks for sustainable, microbiome-mediated disease management.