Rhizosphere Penicillium and phosphorus availability drive bioactive compound accumulation in Amomum villosum

Introduction Amomum villosum (A. villosum), a medicinal herb rich in bioactive metabolites (borneol, bornyl acetate), exhibits superior quality in its core production region Yangchun (YC). However, the key habitat factors influencing the quality of A. villosum, as well as the underlying mechanisms, remain unclear.Methods This study employed an integrated multi-omics approach, incorporating metabolomics, transcriptomics, soil physicochemical property analysis, and metagenomics, to systematically compare the core production region with non-core regions. By identifying potential factors influencing regional disparities and validating the functional roles of key biotic and abiotic soil components through multi-level experimental designs, this research aimed to elucidate the primary determinants of product quality and their underlying regulatory mechanisms.Results The accumulation of major bioactive components, such as borneol and bornyl acetate, was significantly enhanced in YC A. villosum. Transcriptomic analyses showed that YC A. villosum exhibited preferential gene expression patterns, and further identified a functional gene (WvBAHD3) associated with bornyl acetate synthesis. Furthermore, we analyzed the physicochemical properties of soils from the four regions and revealed that available phosphorus (AP) were more abundant in YC soils than the other three non-core regions. Metagenomic analysis revealed that Penicillium, Limnoraphis, and Alcaligenes species were the dominant rhizosphere microorganisms, showing significant enrichment in YC soils compared to other regions. Correlation analysis indicated significant associations among the three dominant microorganisms, soil AP, and the accumulation of major bioactive components in A. villosum. We further isolated a fungus strain, Penicillium citrinum, and demonstrated its role in promoting the release of soil AP by secreting organic acids. Additionally, soil AP was confirmed to enhance the accumulation of bornyl acetate in A. villosum by upregulating the expression of regulatory genes.Conclusion This study demonstrates that the recruitment of Penicillium species modulates bioactive compound accumulation in A. villosum via improved phosphorus availability, providing key guidance for high-quality cultivation of A. villosum.