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Functional characterization of genes related to triterpene and flavonoid biosynthesis in Cyclocarya paliurus

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Abstract

Main conclusion

The oxidosqualene cyclases (OSCs) generating triterpenoid skeletons in Cyclocarya paliurus were identified for the first time, and two uridine diphosphate (UDP)-glycosyltransferases (UGTs) catalyzing the glycosylation of flavonoids were characterized.

Abstract

Cyclocarya paliurus, a native rare dicotyledonous plant in China, contains an abundance of triterpenoid saponins and flavonoid glycosides that exhibit valuable pharmaceutical effects in preventing hypertension, hyperlipidemia, and diabetes. However, the molecular mechanism explaining the biosynthesis of triterpenoid saponin and flavonoid glycoside in C. paliurus remains unclear. In this study, the triterpene content in different tissues and the expression pattern of genes encoding the key enzymes associated with triterpenoid saponin and flavonoid glycoside biosynthesis were studied using transcriptome and metabolome analysis. The eight upstream oxidosqualene cyclases (OSCs) involved in triterpenoid saponin biosynthesis were functionally characterized, among them CpalOSC6 catalyzed 2,3;22,23-dioxidosqualene to form 3-epicabraleadiol; CpalOSC8 cyclized 2,3-oxidosqualene to generate dammarenediol-II; CpalOSC2 and CpalOSC3 produced β-amyrin and CpalOSC4 produced cycloartenol, while CpalOSC2–CpalOSC5, CpalOSC7, and CpalOSC8 all produced lanosterol. However, no catalytic product was detected for CpalOSC1. Moreover, two downstream flavonoid uridine diphosphate (UDP)-glycosyltransferases (UGTs) (CpalUGT015 and CpalUGT100) that catalyze the last step of flavonoid glycoside biosynthesis were functionally elucidated. These results uncovered the key genes involved in the biosynthesis of triterpenoid saponins and flavonoid glycosides in C. paliurus that could be applied to produce flavonoid glycosides and key triterpenoid saponins in the future via a synthetic strategy.

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Availability of data and materials

The plant specimens of the materials used in the experiment are stored in the Southwest Biodiversity Laboratory (No: XINAN202004201). All data supporting the findings were contained in the manuscript and its supplementary files except the RNA-seq raw data. And all original transcriptome data were submitted to NCBI and available for download after six months (Accession Number: PRJNA894718, https://dataview.ncbi.nlm.nih.gov/object/PRJNA894718?reviewer=hjonor6i3ve0j7ffabpos98ba9).

Abbreviations

OSC:

Oxidosqualene cyclase

UGT:

Uridine diphosphate-dependent glycosyltransferases

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Acknowledgements

This work was supported by Major Science and Technology Projects in Yunnan Province (2019ZF011-1), the independent research fund of Yunnan Characteristic Plant Extraction Laboratory (2022YKZY001), Natural Science Foundation of Yunnan Province (Grant No. 202201AU070236) and the Project of Young and Middle-aged Talent of Yunnan Province (Grant No. 2019HB019). We thank the Dr. Yunheng Ji (Kunming Institute of Botany) for identifying plant materials. We thank the Dr. Huifeng Jiang (Tianjin Institute of Industrial Biotechnology) for the gift of S. cerevisiae GIL77.

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Authors

Contributions

SYZ: Conceptualization, Methodology, Validation, Writing—original draft, Visualization. YQP: Conceptualization, Methodology, Validation, Visualization. GSX: Data Curation, Software, Visualization. WLS: Project administration. LF: Methodology. XYJ: Validation. XJL: Resources. SMH: Resources. SCY: Resources. YZ: Writing—review and editing. GHZ: Conceptualization, Supervision, Writing—review and editing. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Yan Zhao or Guang-hui Zhang.

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The authors declare no conflict of interest.

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Communicated by Dorothea Bartels.

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Zhang, Sy., Peng, Yq., Xiang, Gs. et al. Functional characterization of genes related to triterpene and flavonoid biosynthesis in Cyclocarya paliurus. Planta 259, 50 (2024). https://doi.org/10.1007/s00425-023-04282-1

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  • DOI: https://doi.org/10.1007/s00425-023-04282-1

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