Insight into the assembly of root-associated microbiome in the medicinal plant Polygonum cuspidatum

Polygonum cuspidatum (Polygonum cuspidatum Sieb. & Zucc.), a medicinal plant that is abundantly accumulating bioactive compounds in its roots, is the primary source of resveratrol in industry and has long been recognized as raw materials for traditional Chinese medicine. Plant root secondary metabolism is correlated to its surrounding microbial communities. However, the root-associated microbiomes of P. cuspidatum and the potential correlation between the bioactive compounds and microbiomes are poorly understood. To unveil the root-associated bacterial community, the microbiome compositions of P. cuspidatum roots across four cultivation years were analyzed by using 16S rRNA gene sequencing. Furthermore, the relationships among root-associated bacteria, soil properties, and four major bioactive compounds (polydatin, resveratrol, emodin, and physcion) were explored by a multivariate correlation study. The composition of the rhizosphere microbiome significantly differed from that of the endosphere microbiome. The composition of the rhizosphere microbiome significantly varied across different cultivation years and soil properties, contributing to the majority of variance. Regarding different cultivation years and soil properties, the compositions of the root endosphere microbiome remained relatively stable, indicating a strong selection effect in P. cuspidatum roots. Among root endosphere microbes, Stenotrophomonas was specifically enriched from rhizosphere with a 15 times increase of relative abundance, exhibiting no significant variation across different cultivation years. The relative abundance of rhizosphere Stenotrophomonas was positively correlated with the content of emodin. Taken together, this study demonstrated that the stability of the root endosphere microbiome with a dominance of Stenotrophomonas may maintain the growth of P. cuspidatum through the combined effect of emodin. The contents of bioactive compounds in roots exhibited distinct correlations with specific bacteria, suggesting that Bacteroides, Acinetobacter, Erysipelatoclostridium, and Achromobacter may enhance the accumulation of resveratrol. This study provides insights into the interaction networks among P. cuspidatum root-associated bacteria, cultivation years, soil properties, and bioactive compounds, giving us a new opportunity to manipulate the production of bioactive compounds, and thus improve the industrial and medicinal value of P. cuspidatum in future.