Regional variations and plant compartments shape the community structures of the endophytic microbiome and secondary metabolites of Astragalus mongholicus

Increasing evidence has proven that spatial distance has stronger effects on root-associated microbiomes. However, the effect of spatial distance on the composition of plant endophytic microbiomes has been poorly understood. Meanwhile, whether aboveground endophytes can regulate the accumulation of secondary metabolites in the roots of medicinal plants remains unclear. To explore the effect of the endophytic microbiome of the medicinal plant Astragalus membranaceus (Fisch.) Bunge var.mongholicus (A. mongholicus) on secondary metabolites, we investigated the endophytic community structure of A. mongholicus from Tanchang county in Gansu province, Hunyuan county in Shanxi province and Zizhou county in Shaanxi province in China using the high-throughput sequencing. The results demonstrated that regional variation had a greater effect on the endophytic community than plant compartments, especially on leaf endophytic bacteria and root endophytic fungi. The endophytic network patterns showed distinct co-occurrence patterns and niche differentiation, especially the root network. In addition, the contents of secondary metabolites in endophytic compartments were also affected by regional variation. Correlation analysis and random forest model (RF) showed that endophytic bacteria of A. mongholicus grew in three regions exhibited a stronger correlation with secondary metabolite accumulation in plants. Interestingly, the keystone species in the pivotal modules were significantly related to secondary metabolites. Importantly, pot experiments verified that the aboveground microbiota were associated with the accumulation of secondary metabolites in roots. Taken together, our findings illustrate the importance and functionalities of plant microbiomes, highlight the role of key microbiota constituents in regulating plant secondary metabolites, and provide a basis for the application of prospective endophytic taxa to improve the quality and pharmaceutical value of A. mongholicus.