Tobacco intercropping with Allium crops reshapes soil microbiome–metabolome interactions and improves plant health and tobacco leaf quality

Abstract Background Intercropping systems play important roles in improving soil conditions, enhancing crop performance and suppressing soil-borne diseases. However, the mechanisms by which tobacco–Allium intercropping regulates soil microecology, tobacco growth and leaf quality remain insufficiently understood. In this study, tobacco monoculture and tobacco intercropping systems with onion, garlic or Chinese chive were established to evaluate tobacco agronomic traits, disease occurrence, cured leaf chemical composition and defence-related enzyme activities. Soil physicochemical properties, microbial community structure and metabolomic profiles were further analysed and integrated using a multi-omics approach. Results Compared with tobacco monoculture, the tobacco–garlic intercropping treatment (CG) showed the most pronounced effects. CG alleviated soil acidification and increased the contents of available phosphorus and available potassium. The incidence and disease index of tobacco mosaic disease were significantly reduced by 27.91% and 31.77%, respectively. CG also significantly improved tobacco agronomic traits and enhanced the activities of phenylalanine ammonia-lyase (PAL), polyphenol oxidase (PPO) and superoxide dismutase (SOD) by 146.50%, 162.65% and 248.87%, respectively. In cured tobacco leaves, total nitrogen, nicotine and reducing sugar contents increased by 20.57%, 28.22% and 10.49%, respectively. In addition, CG significantly increased potassium content and improved the potassium-to-chloride ratio by 55.46%. Correlation analysis showed that intercropping promoted the enrichment of beneficial bacterial genera, including Gemmatimonas and Sphingomonas, and enhanced functional pathways associated with linoleic acid metabolism, nucleotide metabolism, purine metabolism, pyrimidine metabolism, and the biosynthesis of antibiotics and other secondary metabolites. These changes were closely associated with increased SOD, PPO and PAL activities. In the fungal community, increases in soil pH, available potassium and available phosphorus were associated with reduced Penicillium abundance, jointly contributing to the establishment of a disease-suppressive rhizosphere microenvironment. Conclusions Tobacco–Allium intercropping, particularly tobacco–garlic intercropping, promotes tobacco growth, improves cured leaf quality and enhances disease resistance by modifying soil physicochemical properties, reshaping microbial community structure and regulating key metabolic pathways, especially linoleic acid metabolism, nucleotide metabolism and secondary metabolite biosynthesis. These findings provide a theoretical basis for ecological tobacco cultivation and integrated disease management.