Integrated multi-omics analysis reveals the response mechanisms of Trichosanthes kirilowii to root-knot nematode infection

Abstract

Background Root-knot nematodes (RKNs) pose a severe threat to Trichosanthes kirilowii production, but the molecular mechanisms of its response to RKN infection remain unclear. Methods An integrated multi-omics strategy that combined physiological trait analysis, hormone profiling, transcriptome sequencing, and untargeted metabolome analysis was used to systematically clarify the response mechanisms of T. kirilowii to Meloidogyne incognita infection. Results Comprehensive phenotypic observations combined with antioxidant enzyme activity measurements and hormone profiling identified 6 days post-inoculation (dpi) as a critical response timepoint, characterized by initial gall formation, minimum superoxide dismutase (SOD) activity, peak catalase (CAT) activity, and maximal content of auxin (IAA), abscisic acid (ABA), and salicylic acid (SA). Notably, cytokinin-type hormones were significantly upregulated after RKN infection, with zeatin increasing by 202% at 12 dpi and zeatin riboside reaching 38.5-fold that of the control at 24 dpi. Transcriptomic analysis identified 1,705 differentially expressed genes (DEGs), predominantly enriched in plant hormone signal transduction, zeatin biosynthesis, and plant-pathogen interaction pathways. Untargeted metabolomic analysis identified 658 differentially accumulated metabolites (DAMs), primarily involving carboxylic acid derivatives, amino acids, phospholipids, and isopentenyl alcohol esters; combined analysis further revealed that zeatin biosynthesis was the only significantly enriched common pathway; within this pathway, changes in 8 key genes and 5 core metabolites acted synergistically and were significantly correlated with gall number, soluble sugar content, and multiple hormones. Conclusions The results indicate that T. kirilowii responds to RKN infection through an integrated mechanism involving physiological regulation, hormonal coordination, metabolic reprogramming, and molecular defense, with the zeatin biosynthesis pathway serving as a central hub. These findings provide a basis for molecular breeding and develop green control strategies against RKNs in T. kirilowii cultivation.