Rhizosphere Microbiomes Respond to Plant‐Parasitic Nematode Cues and Contribute to Host Defence

ABSTRACT Plant‐parasitic nematodes (PPNs) cause major crop losses, while current nematicides face increasing regulatory restrictions and often show inconsistent efficacy. We tested whether nematode‐associated cues activate rhizosphere microbiomes and cuticle‐associated fungi to produce suppressive metabolites that impair nematodes and stimulate host defence. Maize rhizosphere microbiomes from different soils and fungal isolates recovered from nematode cuticles were exposed to Meloidogyne hapla , after which cell‐free filtrates were assessed for juvenile mortality, root invasion, gall formation, egg production and reactive oxygen species (ROS) accumulation in tomato. Nematode‐conditioned microbiome filtrates increased M. hapla juvenile mortality relative to nonconditioned controls across soils, although the magnitude of this effect varied with soil origin. Several fungal isolates also showed suppressive activity against Pratylenchus penetrans in maize and M. hapla in tomato, with distinct outcomes across biological assays. Among them, Akanthomyces sp. F20/JKI73389 was selected for mechanistic follow‐up: stimulation by M. hapla , or by nematode‐derived molecules, induced F20 to release a filtrate that reduced nematode root invasion and triggered a strong ROS response in host tissue. UHPLC‐MS analysis further revealed a distinct nematode‐induced metabolite profile in F20, including six candidate features that were absent from non‐stimulated controls and were provisionally associated with enhanced nematode mortality. These results support a model in which nematode‐derived cues alter the metabolite output of indigenous rhizosphere microbes and associated fungi in ways linked to nematode suppression and host defence, highlighting their potential as environmentally compatible tools for PPN management.