Interspecific Allelopathic Interaction Primes Direct and Indirect Resistance of Neighbor Plant in Agroforestry System

Agroforestry system with high biodiversity augments ecosystem stability and minimizes its vulnerability to environmental disturbances and disease. Deciphering the underlying mechanisms of interspecies allelopathic interactions in disease suppression in agroforestry offer a sustainable strategy for plant disease management. Here, we utilized Panax ginseng cultivated under Pinus koraiensis forests, where the occurrences of Alternaria leaf spot are low, as a research model to investigate the role of allelochemicals in disease suppression. Our findings demonstrate that foliar application of leachates from the needles of P. koraiensis effectively enhanced the resistance of P. ginseng against Alternaria leaf spot. Through GC-MS analysis, we identified and quantified endo-borneol as a key compound in the leachates of P. koraiensis, and validated its capacity to prime resistance in its neighbor P. ginseng. We discovered that endo-borneol not only directly activates defense-related pathways of P. ginseng to induce resistance, but also indirectly recruits its rhizospheric beneficial microbiota by enhancing the secretion of ginsenosides, thereby triggering induced systemic resistance (ISR). Importantly, the higher concentrations of endo-borneol from 10 to 100 mg/L demonstrated a stronger capacity to induce plant resistance and enhance root secretion to recruit more microbiota compared with the lower concentrations from 0.01 to 1 mg/L. Moreover, endo-borneol exhibited antifungal activity against the growth of the pathogen Alternaria panax when its concentrations exceeding 10 mg/L. These results reveal the multifaceted functions of allelochemical endo-borneol in disease suppression in agroforestry system and highlight its potential as an environmental-friendly compound for sustainable agriculture.