Integrated omics identifies phenylpropanoid biosynthesis as a key defense mechanism against Meloidogyne incognita in Cucumis metuliferus

The southern root-knot nematode (Meloidogyne incognita) severely threatens Cucurbitaceae crop. However, no M. incognita-resistant resources exist in cultivated cucurbits. Though Cucumis metuli-ferus (a wild Cucurbitaceae relative) show resistance to M.incognita, the resistance molecular mechanisms remains largely unknown. Here, we employed integrated transcriptomic and metabolomic analyses to compare resistant (CM064) and susceptible (CM083) C. metuliferus responses to M. incognita at early (7 dpi) and late (14 dpi) infection stages. The resistant CM064 exhibited a biphasic defense strategy: early-stage upregulation of defense pathways (hormone signaling, chitin response) and downregulation of cell wall biogenesis, suggesting inhibition of feeding site establishment; and late-stage upregulation of cell wall reinforcement, redox homeostasis, and restriction of phloem transport, indicating suppression of M. incognita development. In contrast, the susceptible CM083 showed progressive susceptibility traits, including early-stage cytoskeletal hijacking and defense suppression, followed by late-stage upregulation of heterocycle biosynthesis and downregulation of serine/threonine kinase signaling that may facilitate parasitism. Critically, multi-omics integration identified sustained activation of phenylpropanoid biosynthesis pathway in resistant CM064. Functional validation through Agrobacterium rhizogenes-mediated hairy root transformation system demonstrated that ectopic overexpression of C4H (a key enzyme in phenylpropanoid pathway) in cucumber conferred significant resistance to M.incognita. Our study systematically elucidate the dynamic molecular basis of C.metuliferus resistance to M. incognita and provide a potential theoretical foundation for breeding root-knot nematode-resistant Cucurbitaceae crops.