Foliar 2, 3-butanediol reprograms root exudate-driven rhizosphere microbiome assembly to modulate plant–soil feedbacks in Panax notoginseng

Abstract

Microbiomes associated with plant diversity systems can alleviate negative plant–soil feedbacks (NPSFs), yet the mechanisms responsible for establishing and maintaining protective rhizosphere microbial communities remain incompletely understood. The Panax notoginseng–pine agroforestry system provides an ecological model for investigating how plant-derived signals shape belowground microbial communities under natural NPSFs conditions. Using P. notoginseng cultivated in pine forests, we examined whether pine-derived compounds influence rhizosphere microbiome assembly. Through integration of multi-omics analyses with controlled plant experiments, we found that foliar application of 2, 3-butanediol (2, 3-BD), a key component of pine needle leachates, was associated with changes in rhizosphere microbiome assembly and reduced abundance of soil-borne pathogens. Mechanistically, foliar 2, 3-BD treatment altered root-derived amino acid profiles, including L-phenylalanine, L-leucine, L-isoleucine, and L-tyrosine, with these changes corresponding to shifts in the relative abundances of specific rhizosphere microbial taxa. Following foliar pathogen challenge, amino acid accumulation and microbiome-associated disease alleviation were further enhanced, consistent with a potential priming effect induced by foliar 2, 3-BD treatment. Together, these findings provide mechanistic insights into how foliar-derived signals alter root exudate composition and rhizosphere microbiome assembly, thereby highlighting the role of aboveground–belowground interactions in regulating plant–microbe associations. The identification of 2, 3-BD as a foliar elicitor that influences root-associated processes therefore provides a potential basis for developing microbiome-informed strategies for sustainable disease management.