Green manure enhances ecological pest management by triggering systemic resistance in rice through reshaped rhizosphere microbiome

Ecological pest management (EPM) is gaining increased attention with concerns regarding human health and the environment. Planting green manure (GM) represents a significant practice in EPM; meanwhile, GM enhances crop production and reduces environmental footprints via its effect on the soil microbiome. GM’s direct inhibitory effect on pests and its protective effect on natural enemies have been widely reported. However, the impact of GM's soil legacy effect on pests and the underlying molecular mechanisms remains poorly characterized. In this study, three-year field trials, greenhouse experiments, and multi-omics integration were conducted to address the gap. Compared to winter fallow treatment, GM significantly reduced the occurrence of rice major pests by 43.8-94.2%, including Mythimna separata, Cnaphalocrocis medinalis, Chilo suppressalis, and rice planthoppers. The infestation rate of C. suppressalis , consumption by M. separata , and oviposition by Nilaparvata lugens were reduced by 64.3-87.4%, 38.7-39.9% and 45.3%, respectively. Mechanistically, GM upregulated key defense-related genes and stimulated biosynthesis of flavonoids and alkaloids, alongside the accumulation of jasmonic acid and salicylic acid, indicating synergistic activation of induced systemic resistance in rice plants. Rhizosphere soil analysis revealed GM-driven enrichment of plant-beneficial taxa ( Rhizophagus irregularis , Bradyrhizobium erythrophlei , Pseudolabrys sp.), alongside enhanced soil multifunctionality (N/C cycling) and nutrient mobilization. Our PLS-PM results supported a scenario in which GM-induced pest suppression is potentially mediated by microbiome-driven defense priming. Our findings provide fundamental insights into EPM and highlight how GM modulates the rhizosphere ecosystem and further enhances aboveground systemic resistance in rice. This study offers a potential solution for reducing synthetic inputs in crop production, which contributes to agroecosystem sustainability. • GM reduces subsequent rice pest populations, damage and host preference. • Expression of insect-resistant genes in subsequent rice is up-regulated, and resistant metabolites are enhanced. • Subsequent rice rhizosphere soil nutrients, microbial diversity and multifunctionality are increased. • GM mitigates pests depending on soil-rice-pest interaction cascades. • GM has powerful practical significance in EPM, offering a practical solution for reducing synthetic inputs.