Multi-omics dissection of metabolic and transcriptional regulation underlying fruit maturation in Panax ginseng

Abstract

Background: Panax ginseng is a perennial plant valued for its medicinal and nutritional properties. Its fruit contains a variety of bioactive compounds such as ginsenosides, flavonoids, phenolic acids, and anthocyanins. However, the regulatory mechanisms underlying the accumulation of these compounds during fruit development remain largely unexplored.

Results: We performed integrated metabolomic and transcriptomic analyses across four developmental stages of ginseng fruit. Metabolite profiling revealed stage-specific accumulation patterns of ginsenosides and phenolics with biphasic trends, and increasing levels of flavonoids and anthocyanins during maturation. We constructed a metabolic and gene expression atlas covering primary metabolism (carbon, amino acids, nitrogen), secondary metabolism (flavonoids, terpenoids), and hormone signaling pathways (abscisic acid, gibberellin, brassinosteroids). Key structural genes and transcription factors, including MYB, bHLH, and ERF families, were found to coordinate stage-specific metabolic shifts. Weighted gene co-expression network analysis revealed metabolite-linked gene modules that delineate regulatory relationships.

Conclusions: This study provides a comprehensive molecular framework of fruit development in P. ginseng, highlighting coordinated transcriptional regulation and metabolic reprogramming. These insights contribute to our understanding of developmental regulation in medicinal plants and lay the groundwork for metabolic engineering strategies aimed at enhancing nutritional quality and bioactive compound production.

Keywords: Panax ginseng; Fruit development; Multi-omics integration; Primary metabolism; Secondary metabolism; Transcription factors.

Fig. 1

Dynamic accumulation of bioactive compounds during ginseng fruit development. A Four representative developmental stages of ginseng fruits. B Contents of nine ginsenosides across developmental stages. C Total phenolic content. D Total flavonoid content. E Total anthocyanin content. Different lowercase letters above bars indicate statistically significant differences between stages (one-way ANOVA, P < 0.05)

Fig. 2

Metabolomic profiling reveals dynamic changes during ginseng fruit development. A Classification of detected metabolites. B Principal component analysis (PCA) of metabolic profiles across developmental stages. C Statistics of differentially accumulated metabolites (DAMs) in pairwise comparisons. D–F KEGG enrichment analysis of DAMs in specific comparisons: D FG vs. WG, E GR vs. FG, F FR vs. GR. G Temporal trajectory analysis of metabolic profiles

Fig. 3

Transcriptomic analysis identifies key regulatory pathways during ginseng fruit development. A Principal component analysis (PCA) of transcriptome profiles across developmental stages. B Statistics of differentially expressed genes (DEGs) in pairwise comparisons. C Venn diagram illustrating overlaps of DEGs between comparison groups. D–F KEGG enrichment analysis of DEGs in specific comparisons: D FG vs. WG, E GR vs. FG, F FR vs. GR

Fig. 4

Transcription factor (TF) dynamics reveal differential regulation during ginseng fruit development. A Distribution of TFs identified in the FG vs. WG comparison. B Distribution of TFs in the GR vs. FG comparison. C Expression profiles of the top 50 highly expressed TFs in FG vs. WG. D Expression profiles of the top 50 highly expressed TFs in GR vs. FG. E Expression profiles of TFs in FR vs. GR. F Venn diagram showing overlapping TFs across pairwise comparisons. The red boxes highlight the TFs that are significantly differentially expressed across multiple pairwise comparisons

Fig. 5

Integrated regulatory network of key primary metabolic pathways during ginseng fruit development. A Carbon metabolism. B Amino acid metabolism. C Fatty acid metabolism. D Nitrogen metabolism. The pathway maps were simplified, and some intermediate metabolites and bypasses of the metabolic pathway were not shown to emphasize the DAMs and DEGs detected

Fig. 6

Coordinated regulation of key secondary metabolic pathways during ginseng fruit development. A Flavonoid-related biosynthesis. B Terpenoid-related metabolism. The pathway maps were simplified, and some intermediate metabolites and bypasses of the metabolic pathway were not shown to emphasize the DAMs and DEGs detected

Fig. 7

Hormonal coordination regulates ginseng fruit developmental transitions. A Hormone signal transduction pathways. B Biosynthesis of gibberellins (GAs). C Biosynthesis of brassinosteroids (BRs).The pathway maps were simplified, and some intermediate metabolites and bypasses of the metabolic pathway were not shown to emphasize the DEGs detected

Fig. 8

Integrative WGCNA (weighted gene co-expression network analysis) uncovers stage-specific metabolic and transcriptional modules during ginseng fruit development. A Hierarchical clustering dendrogram of metabolite-level modules. B Expression patterns of module eigengenes across developmental stages (metabolite-level). C–E KEGG pathway analysis and eigengene trends of key modules: C green, D grey, E yellow. F Hierarchical clustering dendrogram of gene-level modules. G Stage-dependent expression dynamics of gene modules. H KEGG enrichment and eigengene profile of the red module