A novel strategy to enhance terpenoids production using cambial meristematic cells of Tripterygium wilfordii Hook. f.

Abstract Background Tripterygium wilfordii Hook. f. (T. wilfordii) is an important medicinal plant with anti-inflammatory, immunosuppressive and anti-tumor activities. The main bioactive ingredients are diterpenoids and triterpenoids, such as triptolide, triptophenolide and celastrol. However, the p...

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Main Authors: Yadi Song, Shang Chen, Xiujuan Wang, Rui Zhang, Lichan Tu, Tianyuan Hu, Xihong Liu, Yifeng Zhang, Luqi Huang, Wei Gao
Format: Article
Language:English
Published: BMC 2019-11-01
Series:Plant Methods
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13007-019-0513-x
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author Yadi Song
Shang Chen
Xiujuan Wang
Rui Zhang
Lichan Tu
Tianyuan Hu
Xihong Liu
Yifeng Zhang
Luqi Huang
Wei Gao
author_facet Yadi Song
Shang Chen
Xiujuan Wang
Rui Zhang
Lichan Tu
Tianyuan Hu
Xihong Liu
Yifeng Zhang
Luqi Huang
Wei Gao
author_sort Yadi Song
collection DOAJ
description Abstract Background Tripterygium wilfordii Hook. f. (T. wilfordii) is an important medicinal plant with anti-inflammatory, immunosuppressive and anti-tumor activities. The main bioactive ingredients are diterpenoids and triterpenoids, such as triptolide, triptophenolide and celastrol. However, the production of terpenoids from original plants, hairy roots and dedifferentiated cells (DDCs) are not satisfactory for clinical applications. To find a new way to further improve the production of terpenoids, we established a new culture system of cambial meristematic cells (CMCs) with stem cell-like properties, which had strong vigor and high efficiency to produce large amounts of terpenoids of T. wilfordii. Results CMCs of T. wilfordii were isolated and cultured for the first time. CMCs were characterized consistent with stem cell identities based on their physiological and molecular analysis, including morphology of CMCs, hypersensitivity to zeocin, thin cell wall and orthogonal partial least square-discriminant analysis, combination of transcriptional data analysis. After induction with methyl jasmonate (MJ), the maximal production of triptolide, celastrol and triptophenolide in CMCs was 312%, 400% and 327% higher than that of control group, respectively. As for medium, MJ-induced CMCs secreted 231% triptolide and 130% triptophenolide at the maximum level into medium higher than that of control group. Maximal celastrol production of induced CMCs medium was 48% lower than that of control group. Long-term induction significantly enhanced the production of terpenoids both in cells and medium. The reason for increasing the yield of terpenoids was that expression levels of 1-deoxy-d-xylulose-5-phosphate synthase (DXS), 1-deoxy-d-xylulose-5-phosphate reductoisomerase (DXR) and hydroxymethylglutaryl-CoA synthase (HMGS) were upregulated in CMCs after induction. Conclusions For the first time, CMCs of T. wilfordii were isolated, cultured, characterized and applied. Considering the significant enrichment of terpenoids in CMCs of T. wilfordii, CMCs could provide an efficient and controllable platform for sustainable production of terpenoids, which can be a better choice than DDCs.
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spelling doaj.art-f3cc5591805c4c668e5c0111f1a663652022-12-22T01:20:57ZengBMCPlant Methods1746-48112019-11-0115111310.1186/s13007-019-0513-xA novel strategy to enhance terpenoids production using cambial meristematic cells of Tripterygium wilfordii Hook. f.Yadi Song0Shang Chen1Xiujuan Wang2Rui Zhang3Lichan Tu4Tianyuan Hu5Xihong Liu6Yifeng Zhang7Luqi Huang8Wei Gao9School of Traditional Chinese Medicine, Capital Medical UniversitySchool of Traditional Chinese Medicine, Capital Medical UniversitySchool of Traditional Chinese Medicine, Capital Medical UniversitySchool of Traditional Chinese Medicine, Capital Medical UniversitySchool of Traditional Chinese Medicine, Capital Medical UniversitySchool of Traditional Chinese Medicine, Capital Medical UniversitySchool of Traditional Chinese Medicine, Capital Medical UniversitySchool of Traditional Chinese Medicine, Capital Medical UniversityState Key Laboratory of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical SciencesSchool of Traditional Chinese Medicine, Capital Medical UniversityAbstract Background Tripterygium wilfordii Hook. f. (T. wilfordii) is an important medicinal plant with anti-inflammatory, immunosuppressive and anti-tumor activities. The main bioactive ingredients are diterpenoids and triterpenoids, such as triptolide, triptophenolide and celastrol. However, the production of terpenoids from original plants, hairy roots and dedifferentiated cells (DDCs) are not satisfactory for clinical applications. To find a new way to further improve the production of terpenoids, we established a new culture system of cambial meristematic cells (CMCs) with stem cell-like properties, which had strong vigor and high efficiency to produce large amounts of terpenoids of T. wilfordii. Results CMCs of T. wilfordii were isolated and cultured for the first time. CMCs were characterized consistent with stem cell identities based on their physiological and molecular analysis, including morphology of CMCs, hypersensitivity to zeocin, thin cell wall and orthogonal partial least square-discriminant analysis, combination of transcriptional data analysis. After induction with methyl jasmonate (MJ), the maximal production of triptolide, celastrol and triptophenolide in CMCs was 312%, 400% and 327% higher than that of control group, respectively. As for medium, MJ-induced CMCs secreted 231% triptolide and 130% triptophenolide at the maximum level into medium higher than that of control group. Maximal celastrol production of induced CMCs medium was 48% lower than that of control group. Long-term induction significantly enhanced the production of terpenoids both in cells and medium. The reason for increasing the yield of terpenoids was that expression levels of 1-deoxy-d-xylulose-5-phosphate synthase (DXS), 1-deoxy-d-xylulose-5-phosphate reductoisomerase (DXR) and hydroxymethylglutaryl-CoA synthase (HMGS) were upregulated in CMCs after induction. Conclusions For the first time, CMCs of T. wilfordii were isolated, cultured, characterized and applied. Considering the significant enrichment of terpenoids in CMCs of T. wilfordii, CMCs could provide an efficient and controllable platform for sustainable production of terpenoids, which can be a better choice than DDCs.http://link.springer.com/article/10.1186/s13007-019-0513-xCambial meristematic cellsTripterygium wilfordii Hook. fTriptolideCelastrolTriptophenolide
spellingShingle Yadi Song
Shang Chen
Xiujuan Wang
Rui Zhang
Lichan Tu
Tianyuan Hu
Xihong Liu
Yifeng Zhang
Luqi Huang
Wei Gao
A novel strategy to enhance terpenoids production using cambial meristematic cells of Tripterygium wilfordii Hook. f.
Plant Methods
Cambial meristematic cells
Tripterygium wilfordii Hook. f
Triptolide
Celastrol
Triptophenolide
title A novel strategy to enhance terpenoids production using cambial meristematic cells of Tripterygium wilfordii Hook. f.
title_full A novel strategy to enhance terpenoids production using cambial meristematic cells of Tripterygium wilfordii Hook. f.
title_fullStr A novel strategy to enhance terpenoids production using cambial meristematic cells of Tripterygium wilfordii Hook. f.
title_full_unstemmed A novel strategy to enhance terpenoids production using cambial meristematic cells of Tripterygium wilfordii Hook. f.
title_short A novel strategy to enhance terpenoids production using cambial meristematic cells of Tripterygium wilfordii Hook. f.
title_sort novel strategy to enhance terpenoids production using cambial meristematic cells of tripterygium wilfordii hook f
topic Cambial meristematic cells
Tripterygium wilfordii Hook. f
Triptolide
Celastrol
Triptophenolide
url http://link.springer.com/article/10.1186/s13007-019-0513-x
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