Integrated multiomics profiling elucidates the spatiotemporal metabolic dynamics and regulatory networks of the bioactive components of Trichosanthes kirilowii

Introduction Trichosanthes kirilowii Maxim. is an important medicinal and edible plant, with its roots, fruits, pericarp, and seeds extensively utilized in traditional medicine and increasingly incorporated into functional foods and health products due to their distinct bioactive constituents. However, a comprehensive understanding of the spatiotemporal dynamics and regulatory mechanisms underlying the biosynthesis of these valuable compounds is lacking, limiting the scientific basis for traditional use, targeted quality improvement, and value-added utilization of this plant. Methods An integrated multiomics strategy (LC–MS/MS metabolomics and Illumina transcriptomics) was employed to elucidate the metabolic and transcriptional landscapes across three pivotal fruit ripening stages (initial, color-changing, and mature) and four tissues (roots, pericarp, fruits, and seeds). Weighted gene coexpression network analysis (WGCNA) was used to identify core modules associated with medicinal compound biosynthesis and hub transcription factors. Results A total of 1,558 metabolites were identified via metabolomic profiling, which revealed pronounced tissue-specific accumulation: fruits and pericarps were enriched in amino acids, flavonoids, and organic acids, seeds accumulated terpenoids, flavonoids, and fatty acids, roots served as the predominant reservoir for pharmacologically active terpenoids, such as the antitumor cucurbitacin B. Transcriptome analysis revealed tissue- and stage-specific expression patterns of genes involved in terpenoid, phenylpropanoid, and flavonoid biosynthetic pathways, which were strongly correlated with metabolite abundance. WGCNA identified three core modules (MEturquoise, MEblack, and MEbrown) and pinpointed the transcription factor Tk_ERF4 as a putative regulator orchestrating cross-talk between these metabolic pathways—supported by consistent co-expression patterns with key pathway genes and conservation of Tk_ERF4 function in medicinal plants. Discussion Collectively, our findings provide a comprehensive molecular blueprint for the spatiotemporal biosynthesis of medicinal compounds in T. kirilowii , deciphering the scientific basis for traditional organ-specific use, establishing foundations for genetic enhancement and quality control, and offering scientific guidance for precision horticultural practices. Beyond T. kirilowii , this work provides a valuable multiomics reference for medicinal-edible plant research and serves as a methodological paradigm for bridging traditional knowledge with modern bioscience.