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Background <p>The medicinal plant <i>Garcinia oblongifolia</i> (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.</p> Results <p>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 <i>PAL</i>, <i>C4H</i>, <i>CoA-hydratase</i> genes and their downstream metabolites. Notebly, <i>BPS</i>, <i>XS</i>, and <i>PT</i> genes were highly expressed in bark, while their corresponding metabolites accumulated in both bark and branches, suggesting inter-tissue translocation.</p> Conclusions <p>Our study analyzed xanthone distribution in <i>G. oblongifolia</i>, 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.</p>

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

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2025年12月15日

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  • Yi Zhang,
  • Ruiqi Zhang,
  • Baiyun Wang,
  • Xinyi Dai,
  • Xiaoyi Yan,
  • Xinyue Liu,
  • Lu Yang,
  • Bo Liu,
  • Honglei Jin,
  • Liya Liu,
  • Yue Liu

摘要

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.