An altruistic rhizo-microbiome strategy in crop rotation systems for sustainable management of soil-borne diseases.

Crops leave a soil legacy with altruistic effects for other subsequent crops but not for themselves. While research has focused on improvements in soil physicochemical properties and the suppression of non-host pathogens, the altruistic microbiome and its assembly mechanism driven by root exudates remain largely unknown. Here, we identified the altruistic but self-detrimental phenomena when garlic rotated with other crops based on meta-analysis and in vivo experiments. Studies utilizing a globally adopted garlic-pepper rotation system demonstrated density-dependent enrichment of key microbial taxa, especially the Penicillium genus, which benefits the healthy growth of non-Allium plants but exhibits pathogenicity toward garlic. Furtherly, we found that garlic root stably secretes diallyl disulfide (DADS) into soil to impose a ROS stress to rhizosphere then reshape the rhizosphere microbial community, especially suppressing ROS-sensitive pathogen but enriching ROS-tolerant beneficial microorganisms. As a result, Penicillium allii with strong oxidative stress tolerance has the ability to survive and accumulate in the highly stressful garlic rhizosphere environment, which plays an 'altruistic but self-detrimental' role in rotation system. In addition, preliminary field experiments showed that co-applying DADS with P. allii could enhance the stable colonization of P. allii, thereby promoting sustainable management of soil-borne diseases and improving yield. In summary, this study reveals that garlic root exudate DADS triggers ROS-mediated selection pressure, enriching stress-tolerant Penicillium allii and establishing an 'altruistic' microbiome succession mechanism in crop rotation systems. This mechanism enables targeted soil-borne disease management through plant-driven microbial community engineering.