Integrated omics reveal phenylpropanoid biosynthesis as a key defense pathway against Meloidogyne incognita in Cucumis metuliferus.

The southern root-knot nematode (Meloidogyne incognita, M. incognita) poses a severe threat to cucurbit production, yet no resistant germplasm exists among cultivated species. Although Cucumis metuliferus (C. metuliferus), a wild Cucurbitaceae species, exhibits resistance to M. incognita and prior transcriptomic studies have identified key responsive genes and signaling pathways, an integrated understanding of the dynamic transcriptional and metabolic reprogramming is still lacking. Here, an integrated transcriptomic and metabolomic analysis was performed on resistant (CM064) and susceptible (CM083) C. metuliferus accessions during M. incognita infection. The resistant CM064 exhibited distinct temporal shifts in defense strategy: early-stage activation of defense pathways (hormone signaling and chitin response) coupled with repression of cell wall biogenesis, and late-stage upregulation of cell wall reinforcement, redox homeostasis, and restriction of phloem transport. In contrast, the susceptible CM083 showed progressive susceptibility, characterized by early-stage modulation of cytoskeletal activity and defense suppression, followed by late-stage upregulation of amino acid biosynthesis and downregulation of serine/threonine kinase signaling. Multi-omics integration revealed a sustained activation of the phenylpropanoid biosynthesis pathway during infection. Ectopic overexpression of Cinnamate 4-hydroxylase (C4H) was associated with significant resistance to M. incognita in cucumber. Collectively, this study provides insights into the multi-layered defense mechanism of C. metuliferus against M. incognita and supports the important role of phenylpropanoid pathway activation in nematode resistance, suggesting a potential strategy for crop improvement.