Decline in rhizosphere VOC diversity drives microbiome restructuring inducing Fritillaria pallidiflora replant disease

Replantation disorder poses a significant challenge in medicinal plant production, primarily due to soil-borne diseases and yield reduction. This phenomenon arises from complex interactions between root exudates and rhizosphere microbes, though the underlying mechanisms remain poorly understood. We compared rhizosphere soils from first-crop and consecutively replanted (2–4 years old) Fritillaria pallidiflora plants. Using GC-MS, we analyzed soil volatile organic compounds (VOCs), while high-throughput sequencing characterized microbial community structure, diversity, and soil properties to elucidate root exudate-microbiome interactions. Continuous monoculture led to the accumulation of phthalates and alkanes (e.g., dodecane, 2,6,10-trimethyl-) while reducing VOC diversity. This directly suppressed bacterial and fungal α-diversity and elevated levels of available potassium, phosphorus, and organic carbon. Notably, the allelochemical phthalates exhibited a strong correlation with Fusarium (a root rot pathogen) abundance, driving the co-enrichment of both pathogenic and beneficial fungi. Monoculture intensified stochastic microbial community assembly, shifting bacterial functions toward chemoheterotrophy and enhancing fungal saprotrophic activity. Bacterial functional profiles and fungal composition were strongly influenced by soil physicochemical properties. VOCs-microbe cross-kingdom network analysis revealed the strongest correlations between metabolites and rhizosphere bacteria. By reducing VOC diversity, monoculture impaired soil nutrient cycling, leading to specific nutrient accumulation and increased VOCs-microbe network complexity. These changes indirectly suppressed plant growth and elevated disease incidence. Our study elucidates how rhizosphere VOCs drive microbiome restructuring under monoculture, providing a theoretical basis for mitigating F. pallidiflora replanting challenges.