Metabolomic approach reveals the mechanism of synthetic communities to promote high quality and high yield of medicinal plants—danshen (Salvia miltiorrhiza Bge.)

Abstract Background Salvia miltiorrhiza Bunge, a significant and widely used medicinal herb, is also recognized in the US Pharmacopoeia as a dietary supplement. However, the decline in yield and quality limits its further development as a traditional herbal medicine. Therefore, a deeper understanding of how synthetic communities (SynCom) affect the quality and yield of S. miltiorrhiza and the underlying mechanisms is necessary. Results In this study, we selected S. miltiorrhiza as the research subject and designed two synthetic communities (SynCom 1 and SynCom 2) using five endophytic fungi without significantly growth-promoting effect. We conducted both greenhouse and field experiments to investigate their impact on the yield and quality of the herbal plants. Greenhouse experiments confirmed that SynCom 1 significantly increased the biomass of S. miltiorrhiza, whereas SynCom 2 had the opposite effect. Field experiments further demonstrated that the application of SynCom 1 promoted photosynthesis and enhanced carbon and nitrogen metabolism, steady and markedly promoted plant growth, and thus increased S. miltiorrhiza yield compared to the uninoculated. In contrast, SynCom 2 inhibited yield but increased the content of the main active components. Un-targeted metabolomics analysis showed that SynCom 1 mainly promoted tricarboxylic acid cycle and nitrogen assimilation process to increase yield, and SynCom 2 mainly increase substrate content in the salvianolic acid and tanshinone synthesis pathways to improve quality. Conclusion These beneficial qualities exhibited by SynComs composed of fungi without apparent growth-promoting abilities represent an untapped resource that can be leveraged to enhance crop productivity. This opens up new research avenues for precision manipulation of plant microbiomes. Graphical abstract