Environmental Response to Root Secondary Metabolite Accumulation in Paeonia lactiflora: Insights from Rhizosphere Metabolism and Root-Associated Microbial Communities

Paeonia lactiflora is a commercial crop with horticultural and medicinal value. Although interactions between plants and microbes are increasingly evident and considered to be drivers of ecosystem service, the regulatory relationship between microbial communities and the growth and root metabolites of P. lactiflora is less well known. Here, soil metabolomics indicated that carbohydrates and organic acids were enriched in the rhizosphere (RS) with higher diversity. Moreover, the variation of root-associated microbiotas between the bulk soil (BS) and the RS of P. lactiflora was investigated via 16S rRNA and internally transcribed spacer (ITS) amplicon sequencing. The RS displayed a low-diversity community dominated by copiotrophs, whereas the BS showed an oligotroph-dominated, high-diversity community. Hierarchical partitioning showed that cation exchange capacity (CEC) was the main factor affecting microbial community diversity. The null model and the dispersion niche continuum index (DNCI) suggested that stochastic processes (dispersal limitation) dominated the community assembly of both the RS and BS. The bacterial-fungal interkingdom networks illustrated that the RS possessed more complex and stable co-occurrence patterns. Meanwhile, positive link numbers and positive cohesion results revealed more cooperative relationships among microbes in the RS. Additionally, random forest model prediction and two partial least-squares path model (PLS-PM) analyses showed that the P. lactiflora root secondary metabolites were comprehensively impacted by soil water content (SWC), mean annual precipitation (MAP), pH (abiotic), and Alternaria (biotic). Collectively, this study provides a theoretical basis for screening the microbiome associated with the active components of P. lactiflora. IMPORTANCE Determining the taxonomic and functional components of the rhizosphere microbiome, as well as how they differ from those of the bulk soil microbiome, is critical for manipulating them to improve plant growth performance and increase agricultural yields. Soil metabolic profiles can help enhance the understanding of rhizosphere exudates. Here, we explored the regulatory relationship across environmental variables (root-associated microbial communities and soil metabolism) in the accumulation of secondary metabolites of P. lactiflora. Overall, this work improves our knowledge of how the rhizosphere affects soil and microbial communities. These observations improve the understanding of plant-microbiome interactions and introduce new horizons for synthetic community investigations as well as the creation of microbiome technologies for agricultural sustainability.