Tissue-specific biosynthesis and spatial distribution of xanthones in Garcinia oblongifolia revealed by integrated metabolomic and full-length transcriptomic analyses

BACKGROUND: The medicinal plant Garcinia oblongifolia (Clusiaceae), widely used in the Lingnan area of southern China, exhibits notable anti-inflammatory, analgesic, antimyatrophy, antibacterial, and antitumor properties. Traditional applications, particularly the use of its bark, were extensive and largely attributed to bioactive xanthones. However, the tissue-specific distribution and biosynthesis of these compounds remained poorly understood. RESULTS: Metabolite profiling identified 402 metabolites, including 215 that accumulated differentially across four tissues. Notably, 16 xanthones were predominantly localized in the bark and branches, with prenyl-substituted derivatives exhibiting the highest accumulation in branches. To elucidate xanthones biosynthesis, we integrated Illumina and single-molecule real-time (SMRT) sequencing, which yielded 70,401 full-length transcripts. Transcriptomic analysis revealed 8,842 differentially expressed transcripts, with xanthone-related genes showing bark-specific expression a pattern confirmed by qRT-PCR. We reconstructed a putative xanthone biosynthetic pathway involving 32 full-length transcripts encoding seven key enzymes. Phylogenetic and motif analyses revealed that four benzophenone synthase (BPS) homologs catalyze the conversion of benzoyl-CoA into 2,4,6-trihydroxybenzophenone. As a pivotal enzyme, BPS plays a central role in this biosynthetic pathway. Transcription factor analysis indicated that the bHLH family was closely associated with the regulation of BPS. Correlation and WGCNA analyses demonstrated a positive regulatory relationship between PAL, C4H, CoA-hydratase genes and their downstream metabolites. Notebly, BPS, XS, and PT genes were highly expressed in bark, while their corresponding metabolites accumulated in both bark and branches, suggesting inter-tissue translocation. CONCLUSIONS: Our study analyzed xanthone distribution in G. oblongifolia, supporting its medicinal uses, and provided its first full-length transcriptome. We proposed a xanthone biosynthetic pathway, aiding in vitro synthesis and sustainable production, advancing pharmacological and biotechnological applications.