Auxin signaling activated by endophytic Cross-Kingdom synthetic microbiota improves the quality of Atractylodes chinensis

Endophytes play a vital role in improving the quality of medicinal plants. Both endophytic fungi and bacteria can confer fitness benefits to medicinal plants; however, the effects of endophytic cross-kingdom synthetic microbiota on host development remain largely unexplored. In the present study, synthetic communities (SynComs) composed of endophytic fungi and/or bacteria were constructed from the medicinal plant Atractylodes chinensis using microbial culture techniques and pot experiments. The results showed that cross-kingdom SynComs comprising endophytic fungi and bacteria were more effective than single-kingdom fungal or bacterial SynComs in promoting the growth and accumulation of secondary metabolites in A. chinensis. Transcriptomic analysis further revealed that the photosynthesis and sesquiterpenoid biosynthesis pathways were upregulated by cross-kingdom SynComs. Notably, the genes related to auxin signal transduction were markedly activated. Chemical treatments, indole-3-acetic acid flux assays, and experiments using Arabidopsis thaliana mutants collectively showed that auxin signaling plays a pivotal role in mediating the enhanced growth and metabolism induced by cross-kingdom SynComs. Field experiments validated the effectiveness of cross-kingdom SynComs for improving the yield and quality of A. chinensis. This study highlights the critical role of endophytic fungi–bacteria–plant associations in promoting host fitness through auxin signaling, providing novel insights into the application of cross-kingdom SynComs in medicinal plant research.