Arbuscular mycorrhizal symbiosis decouples arsenic risk from saponin biosynthesis in Panax notoginseng (Araliaceae) by reprogramming rhizosphere and root processes.

Abstract

Arsenic (As) contamination poses a serious threat to the safety and medicinal quality of Panax notoginseng, a high-value medicinal herb rich in triterpenoid saponins. Arbuscular mycorrhizal fungi (AMF) can improve plant tolerance to metal(loid) stress, but how AMF coordinate rhizosphere processes with host metabolic regulation to reduce As accumulation while maintaining medicinal quality remains poorly understood. Here, we integrated physiological assays, As partitioning and subcellular fractionation, rhizosphere microbiome profiling, root exudate metabolomics, phytohormone quantification, transcriptomics, proteomics, and partial least squares path modelling (PLS-PM) to investigate the effects of Entrophospora etunicatum inoculation on P. notoginseng under As stress. AMF colonization alleviated As-induced toxicity by improving plant growth, photosynthetic performance, and antioxidant capacity. Notably, AMF reduced As accumulation in medicinal taproot, while promoting As retention in fibrous roots and immobilization in cell wall-associated fractions. AMF also reshaped the rhizosphere bacterial community, enhanced glomalin-related soil protein (GRSP) accumulation and soil enzyme activities, and altered root exudate and endogenous hormone profiles. Transcriptomic and proteomic analyses indicated coordinated regulation of detoxification, transport, carbon metabolism, phenylpropanoid biosynthesis, and secondary metabolism. In parallel, AMF promoted the accumulation of major notoginseng saponins, suggesting that As detoxification was coupled with preservation of medicinal quality rather than a growth-defense trade-off. PLS-PM supported linkages among AMF colonization, rhizosphere reassembly, As sequestration, host metabolic reprogramming, and saponin accumulation. Overall, our results reveal a multiscale mechanism by which AMF reduce As risk in medicinal tissues while sustaining bioactive compound biosynthesis, providing promising biological strategy for safe production of medicinal plants in As-contaminated soils.