Polyesters of 14-Hydroxylated Taxoids Found for the First Time in  Taxus canadensis  Intact Plants

D. V. Kochkin; Кочкин Д. В.; E. V. Demidova; Демидова Е. В.; E. B. Globa; Глоба Е. Б.; E. S. Glagoleva; Глаголева Е. С.; B. A. Galishev; Галишев Б. А.; A. M. Nosov; Носов А. М.

doi:10.31857/S0015330322600401

Polyesters of 14-Hydroxylated Taxoids Found for the First Time in Taxus canadensis Intact Plants

Authors: Kochkin D.V.¹^,2, Demidova E.V.¹, Globa E.B.¹, Glagoleva E.S.², Galishev B.A.³, Nosov A.M.¹^,2
Affiliations:
1. Federal State Budgetary Institution of Science Timiryazev Institute of Plant Physiology, Russian Academy of Sciences
2. Federal State Budgetary Educational Institution of Higher Education Lomonosov Moscow State University
3. Federal State Autonomous Educational Institution of Higher Education Yeltsin Ural Federal University
Issue: Vol 70, No 1 (2023)
Pages: 71-79
Section: ЭКСПЕРИМЕНТАЛЬНЫЕ СТАТЬИ
URL: https://journals.rcsi.science/0015-3303/article/view/130209
DOI: https://doi.org/10.31857/S0015330322600401
EDN: https://elibrary.ru/AMIVWU
ID: 130209

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Abstract

Taxane diterpenoids (taxoids) are found only in representatives of the Taxaceae family (different yew species); however, the unique structure and therapeutic properties of taxoids, which are in demand in medicine, have made these compounds one of the most studied secondary metabolites of higher plants. In this work, for the first time, a detailed study is performed into the structural diversity of polyesters of 14-hydroxylated taxoids in Taxus canadensis a yew species, for intact plants of which nonpolar 14-hydroxylated taxoids have not been previously described. At the first stage of the work, it was shown using chromato-mass spectrometry that polyesters of 14-hydroxylated taxoids (yunnanxan, taxuyunnanin C, sinenxan B, sinenxan C) are the dominant diterpenoid secondary metabolites in T. canadensis callus cell culture. Based on these results, as well as the similarity of the metabolism of cultivated in vitro plant cells and root cells in planta, it was suggested that polyesters of 14-hydroxylated taxoids will preferentially accumulate in the roots in intact T. canadensis plants. The validity of this hypothesis was confirmed using liquid chromatography-mass spectrometry and nuclear magnetic resonance spectroscopy (NMR). According to chromato-mass-spectrometric screening in T. canadensis needles, polyesters of 14-hydroxylated taxoids are actually found only in trace amounts, while they are one of the major (quantitatively) diterpenoids in the roots. One of the main 14-hydroxylated taxoids of T. canadensis roots, yunnanxan, was isolated preparatively and uniquely identified using NMR spectroscopy and high-resolution mass spectrometry. This work is the first report on the presence of polyesters of 14-hydroxylated taxoids in intact Canadian yew plants.

Keywords

Taxus, Taxus canadensis, diterpenoids, taxoids, 14-hydroxylated taxoids, yunnanxan, plant cell culture

References

Wang Y.-F., Shi Q.-W., Dong M., Kiyota H., Gu Y.-C., Cong B. Natural taxanes: Developments since 1828 // Chem. Rev. 2011. V. 111. P. 7652. https://doi.org/10.1021/cr100147u
Lange B.M., Conner C.F. Taxanes and taxoids of the genus Taxus – A comprehensive inventory of chemical diversity // Phytochemistry. 2021. V. 190. P. 112829. https://doi.org/10.1016/j.phytochem.2021.112829
Johnson S.R., Bhat W.W., Bibik J., Turmo A., Hamberger B., Evolutionary Mint Genomics Consortium, Hamberger B. A database-driven approach identifies additional diterpene synthase activities in the mint family (Lamiaceae) // J. Biol. Chem. 2019. V. 294. P. 1349. https://doi.org/10.1074/jbc.RA118.006025
Baloglu E., Kingston D.G.I. The taxane diterpenoids // J. Nat. Prod. 1999. V. 62. P. 1448. https://doi.org/10.1021/np990176i
Kochkin D.V., Globa E.B., Demidova E.V., Gaisinsky V.V., Kuznetsov V.V., Nosov A.M. Detection of taxuyunnanin C in suspension cell culture of Taxus canadensis // Dokl. Biochem. Biophys. 2019. V. 485. P. 129. https://doi.org/10.1134/S1607672919020145
Shin J., Seo P.J. Varying auxin levels induce distinct pluripotent states in callus cells // Front. Plant Sci. 2018. V. 9. P. 1563. https://doi.org/10.3389/fpls.2018.01653
Wink M. Physiology of the accumulation of secondary metabolites with special reference to alkaloids // Cell Culture in Phytochemistry / Eds. F. Constabel, I. Vasil. K. Academic Press, 1987. P. 17.
Глоба Е.Б., Демидова Е.В., Туркин В.В., Макарова С.С., Носов А.М. Каллусогенез и получение суспензионных культур клеток четырех видов тисса: Taxus canadensis, T. baccata, T. cuspidata и T. media // Биотехнология. 2009. Т. 3. С. 54.
Elpe C., Knopf P., Stützel T., Schulz C. Diversity and evolution of leaf anatomical characters in Taxaceae s.l. – fluorescence microscopy reveals new delimitating characters // J. Plant Res. 2018. V. 131. P. 125. https://doi.org/10.1007/s10265-017-0973-x
Глоба Е.Б., Демидова Е.В., Гайсинский В.В., Кочкин Д.В. Получение и характеристика каллусной и суспензионной культур клеток тиса Валлиха (Taxus wallichiana Zucc.) // Вестник Северо-Восточного федерального университета имени М.К. Аммосова. 2018. Т. 2. С. 18. https://doi.org/10.25587/SVFU.2018.64.12127
Kochkin D.V., Globa E.B., Demidova E.V., Gaisinsky V.V., Galishev B.A., Kolotyrkina N.G., Kuznetsov V.V., Nosov A.M. Occurrence of 14-hydroxylated taxoids in the plant in vitro cell cultures of different yew species (Taxus spp.) // Dokl. Biochem. Biophys. 2017. V. 476. P. 337. https://doi.org/10.1134/S1607672917050131
Madhusudanan K. P., Chattopadhyay S. K., Tripathi V., Sashidhara K. V., Kumar S. MS/MS profiling of taxoids from the needles of Taxus wallichiana // Phytochem. Anal. 2002. V. 13. P. 18. https://doi.org/10.1002/pca.610
Madhusudanan K.P., Chattopadhyay S.K., Tripathi V.K., Sashidhara K.V., Kukreja A.K., Jain S.P. LC-ESI-MS analysis of taxoids from the bark of Taxus wallichiana // Biomed. Chromatogr. 2002. V.16. P. 343. https://doi.org/10.1002/bmc.163
Zhao C. F., Yu L. J., Li L. Q., Xiang F. Simultaneous identification and determination of major taxoids from extracts of Taxus chinensis cell cultures // Z. Naturforsch. C, J. Biosci. 2007. V. 62. P. 1. https://doi.org/10.1515/znc-2007-1-201
Morikawa K., Tanaka K., Li F., Awale S., Tezuka Y., Nobukawa T., Kadota S. Analysis of MS/MS fragmentation of taxoids // Nat. Prod. Commun. 2010. V. 5. P. 1551. https://doi.org/10.1177/1934578x1000501007
Sanchez-Muñoz R., Perez-Mata E., Almagro L., Cusido R.M., Bonfill M., Palazon J., Moyano E. A Novel Hydroxylation Step in the Taxane Biosynthetic Pathway: A New Approach to Paclitaxel Production by Synthetic Biology // Front. Bioeng. Biotechnol. 2020. V. 8. P. 410. https://doi.org/10.3389/fbioe.2020.00410
Ma W., Stahlhut R.W., Adams T.L., Park G.L., Evans W.A., Blumenthal S.G., Gomez G.A., Nieder M.H., Hylands P.J. Yunnanxane and its homologous esters from cell cultures of Taxus chinensis var. mairei // J. Nat. Prod. 1994. V. 57. P. 1320. https://doi.org/10.1021/np50111a027
Shi Q.-W., Sauriol F., Mamer O., Zamir L. O. New minor taxane derivatives from the needles of Taxus canadensis // J. Nat. Prod. 2003. V. 66. P. 1480. https://doi.org/10.1021/np000053u
Topcu G., Sultana N., Akhtar F., Habib ur r., Hussain T., Choudhary M. I., Atta-ur R. Taxane diterpenes from Taxus baccata // Nat. Prod. Let. 1994. V. 4. P. 93. https://doi.org/10.1080/10575639408044919
Banskota A.H., Usia T., Tezuka Y., Kouda K., Nguyen N.T., Kadota S. Three new C-14 oxygenated taxanes from the wood of Taxus yunnanensis // J. Nat. Prod. 2002. V. 65. P. 1700. https://doi.org/10.1021/np020235j
Zhang H., Takeda Y., Minami Y., Yoshida K., Matsumoto T., Xiang W., Mu O., Sun H. Three new taxanes from the roots of Taxus yunnanensis // Chem. Let. 1994. V. 23. P.957. https://doi.org/10.1246/cl.1994.957
Gabetta B., Peterlongo F., Zini G., Barboni L., Rafaiani G., Ranzuglia P., Torregiani E., Appendino G., Cravotto G. Taxanes from Taxus x media // Phytochemistry. 1995. V. 40. P. 1825. https://doi.org/10.1016/0031-9422(95)00474-L
Chen W. M., Zhang P. L., Wu B., Zheng Q. T. Studies on the chemical constituents of Taxus yunnanensis // Yao Xue Xue Bao. 1991. V. 26. P. 747. [In Chinese].
Shi Q.-W., Dong M., Huo C.-H., Su X.-H., Li C.-F., Zhang X.-P., Wang Y.-F., Kiyota H. New 14-Hydroxy-taxane and 2α,20-Epoxy-11(15→1)abeotaxane from the needles of Taxus canadensis // Biosci. Biotechnol. Biochem. 2007. V. 71. P. 1777. https://doi.org/10.1271/bbb.70063
Li N., Wang J., Yan H.-M., Zhang M.-l., Shi Q.-W., Sauriol F., Kiyota H., Dong M. Two new taxane-glycosides from the needles of Taxus canadensis // Z. Naturforsch. B. 2015. V. 70 P. 829. https://doi.org/10.1515/znb-2015-0074
Allison T. Self-fertility in Canada yew (Taxus canadensis Marsh.) // J. Torrey Bot. Soc. 1993. V. 120. P. 115. https://doi.org/10.2307/2996940
Wilson P., Buonopane M., Allison T. Reproductive biology of the monoecious clonal shrub Taxus canadensis // Bull. Torrey Bot. Club. 1996. V. 123. P. 7. https://doi.org/10.2307/2996301
Collins D., Mill R.R., Möller M. Species separation of Taxus baccata, T. canadensis, and T. cuspidata (Taxaceae) and origins of their reputed hybrids inferred from RAPD and cpDNA data // Am. J. Bot. 2003. V. 90. P. 175. https://doi.org/10.3732/ajb.90.2.175
Windels S.K.W.K., Flaspohler D.J.F.J. The ecology of Canada yew (Taxus canadensis Marsh.): A review // Botany. 2011. V. 89. P. 1. https://doi.org/10.1139/B10-084
van Rozendaal E.L.M., Kurstjens S.J.L., van Beek T.A., van den Berg R. G. Chemotaxonomy of Taxus // Phytochemistry. 1999. V. 52. P. 427. https://doi.org/10.1016/S0031-9422(99)00229-0
Möller M., Liu J., Li Y., Li J.-H., Ye L.-J., Mill R., Thomas P., Li D.-Z., Gao L.-M. Repeated intercontinental migrations and recurring hybridizations characterise the evolutionary history of yew (Taxus L.) // Mol. Phylogenet. Evol. 2020. V. 153. P. 106952. https://doi.org/10.1016/j.ympev.2020.106952
Butenko R.G. Some features of cultured plant cell // Plant cell culture. Advances in science and technology in the USSR / Ed. R.G. Butenko. Mir Publishers. 1985. P. 11.
Fan M., Xu C., Xu K., Hu Y. LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation in Arabidopsis regeneration // Cell Res. 2012. V. 22. P. 1169. https://doi.org/10.1038/cr.2012.63
Ikeuchi M., Sugimoto K., Iwase A. Plant callus: Mechanisms of induction and repression // Plant Cell. 2013. V. 25. P. 3159. https://doi.org/10.1105/tpc.113.116053