Root exudates drive plant-microbiome interactions influencing the quality of cultivated Rheum tanguticum during different growth development stages

Root exudate composition serves as a crucial determinant in shaping the structural assembly and functional dynamics of rhizosphere microbial communities. Despite the critical role of plant-microbe interactions at the rhizosphere interface in mediating plant health and productivity, the mechanistic understanding of how root exudation dynamics regulate microbial community construction throughout the development of perennial plants remains insufficiently characterized. This study focused on Rheum tanguticum Maxim. ex Regel, from which we collected root exudates and microbial samples from the plant-soil continuum during the growth, maturity, and senescence periods. We investigated the feedback regulatory mechanisms of rhizosphere microorganisms mediated by the spatiotemporal dynamics of root exudates and their impact on the contents of bioactive compounds. Our results indicated that the growth development stages significantly altered the composition of root exudates, shifting from primary to secondary metabolites. During the growth and maturity periods, root exudates were primarily composed of organic acids and amino acids, while during the senescence phase, they consisted of amines, benzene, phenolics, and so on. These changes in root exudates significantly impacted the composition and function of the rhizosphere microbial community. Beneficial microbial groups such as Beijerinckiaceae, Propionibacteriaceae, Sphingomonadaceae, and Didymellaceae were inhibited by secondary metabolites like amines and benzene, whereas pathogenic microorganisms, such as TRA3–20 and Pseudeurotiaceae, were promoted. The content of active compounds in the roots significantly decreased during the senescence period, which was closely associated with changes in the abundance of beneficial microbial groups in the rhizosphere. This finding provides novel evidence for elucidating the “root exudates-microbiome-bioactive compounds” cascade regulatory network and offers a theoretical foundation for the precise cultivation of medicinal plants and targeted microbial regulation, which facilitates the transition of herb cultivation from an empirical model to a scientific paradigm. • The bioactive compounds of roots are significantly different across growth stages. • Growth stages shift the root exudates from primary to secondary metabolites. • Primary metabolites recruit probiotics, promoting the bioactive components. • Secondary metabolites recruit pathogens, diminishing the bioactive components.