Yang Gao, Hainuo Hong, Qiulin Chen, Zheyi Shi, Xiao Liang, Mingkai Jiang, Muhammud Musa Khan, Zeng-Rong Zhu, Lingfei Hu, Ying Zhou
How organisms convert short-term stress into long-term defense is a key ecological question. Classic herbivore-induced plant volatiles recruit natural enemies but act briefly only in damaged tissues. Here, we report that leaf herbivory establishes a persistent soil defensive legacy to help uninfested subsequent plants attract parasitoids. During the conditioning phase, herbivory systemically activates jasmonate signaling, which reprograms root metabolism and promotes the exudation of specific flavonoids, notably daidzein and genistein. These compounds selectively restructure the rhizosphere microbiome, enriching functionally specialized bacterial taxa that constitute the soil-borne legacy. During the feedback phase, these enriched rhizosphere bacteria, in turn, increase jasmonate signaling in succeeding plants, boosting emission of the key parasitoid-attracting volatile (Z)-3-hexenyl acetate in the absence of herbivory. Together, our findings reveal plant-soil feedback as an active ecological process that extends the spatial and temporal reach of plant defenses, with broad implications for plant-enemy interactions and sustainable pest management.