From insect control to plant resilience: Unraveling the entomopathogenic nematode-driven quadripartite network for sustainable agriculture

Global agriculture faces mounting pressure from insect pests, resulting in significant yield losses and unsustainable reliance on chemical pesticides. Entomopathogenic nematodes (EPNs) have long been valued as biocontrol agents for their host-specificity and environmental safety. However, emerging evidence reveals that EPNs function not merely as insect killers but as central components within a dynamic quadripartite network—encompassing the insect pest, rhizosphere microbiome, and host plant. This review synthesizes contemporary research to decode this interconnected system, highlighting how EPNs, along with their symbiotic bacteria, directly suppress insect immunity through a suite of toxins and the disruption of critical host metabolic processes. Beyond pest mortality, EPNs activity reshapes soil microbial communities, enriching beneficial organisms while suppressing pathogens, and primes systemic plant defenses via induced volatile signaling and key signaling pathways. We further explore how EPNs enhance plant resilience to abiotic and biotic stresses, improve nutrient availability, and integrate into synergistic microbial consortia. By connecting these multilayered interactions, this review reframes EPNs as multifunctional bioagents essential for ecosystem health. Consequently, we provide a translational roadmap for deploying EPNs as keystone organisms in sustainable agriculture, advocating for management strategies that actively cultivate the beneficial quadripartite network they anchor to achieve resilient pest suppression, enhanced soil vitality, and optimized plant health.