Metabolic Reprogramming in Cucumis metuliferus Roots and Rhizosphere Identifies Candidate Metabolites That Reduce Meloidogyne incognita Infection.

Root-knot nematode causes severe yield losses in cucumber and other cucurbits. The wild relative Cucumis metuliferus exhibits strong resistance, but the metabolic basis of this resistance and the potential of resistance-associated metabolites to protect susceptible crops remains poorly understood. Here, we compared host status, phenolic content, and untargeted metabolomes of roots and rhizosphere soils of C. metuliferus and C. sativus upon Meloidogyne incognita infection. C. metuliferus showed delayed nematode development, fewer galls, and a lower reproduction factor compared with C. sativus, accompanied by higher constitutive phenolic levels in mock-inoculated plants and phenolic levels at 7, 14, 21, and 28 days after inoculation. Untargeted metabolomics revealed that C. metuliferus underwent more extensive metabolic reprogramming than C. sativus, with 72 root-specific and 45 rhizosphere-specific differential metabolites enriched mainly in linolenic acid metabolism and dominated by lipids and organic acids. Six C. metuliferus-specific up-regulated metabolites (arginine, phenylacetic acid, proline, hydroxyproline, malic acid, maleic acid) were selected for functional validation. When exogenously applied to C. sativus seedlings under nematode stress, these metabolites were associated with enhanced shoot growth and biomass accumulation. Among them, arginine, hydroxyproline, and maleic acid were consistently associated with reduced root gall formation. Our findings demonstrate that C. metuliferus mounts a resistance phenotype through extensive root and rhizosphere metabolic reprogramming, and that specific up-regulated metabolites from this resistant species can both promote cucumber growth and reduce M. incognita infection. These metabolites represent promising candidates but require further field validation and formulation studies before being developed into sustainable nematode management strategies.