SpringerLink
Log in

Different chilling stresses stimulated the accumulation of different types of ginsenosides in Panax ginseng cells

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Ginseng (Panax ginseng) is one of the most medically important plants in the world. Dammarane-type ginsenosides, which mainly include protopanaxatriol-type (PPT-type) and protopanaxadiol-type (PPD-type) ginsenosides, are the major pharmacologically relevant compounds that are produced by ginseng. Dammarenediol-II synthase (DDS) is the first committed enzyme in the ginsenoside biosynthetic pathway for dammarane-type ginsenosides, and PPD-type and PPT-type ginsenosides are catalyzed by protopanaxadiol synthase (PPDS) and protopanaxatriol synthase (PPTS), respectively. Ginseng cells are often used in stress studies. During their growth and development, ginseng plants are often exposed to cold stress. This study evaluated the effects of different chilling stresses on the accumulation of ginsenosides and the expressions of the DDS, PPDS and PPTS genes in ginseng cells. The results showed that continuous chilling (5 °C for 12 h) induced the PPT-type ginsenosides; whereas intermittent chilling (25 °C for 12 h and 5 °C for 12 h) stimulated the accumulation of PPD-type ginsenosides. The expression levels of DDS, PPDS and PPTS were clearly consistent with the accumulation pattern for PPT-type ginsenosides under continuous chilling stress or PPD-type ginsenosides under intermittent chilling stress, as was their order of involvement in the PPT-type or PPD-type biosynthetic pathway. These results indicate that different chilling treatments stimulated the accumulation of different types of ginsenosides, suggesting that cold stress may be one of the reasons for ginsenoside accumulation in ginseng cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Akalezi CO, Liu S, Li QS, Yu JT, Zhong JJ (1999) Combined effects of initial sucrose concentration and inoculum size on cell growth and ginseng saponin production by suspension cultures of Panax ginseng. Process Biochem 34:639–642

    Article  CAS  Google Scholar 

  • Ali MB, Hahn EJ, Paek KY (2006a) Copper-induced changes in the growth, oxidative metabolism, and saponin production in suspension culture roots of Panax ginseng in bioreactors. Plant Cell Rep 25:1122–1132

    Article  CAS  PubMed  Google Scholar 

  • Ali MB, Yu KW, Hahn EJ, Paek KY (2006b) Methyl jasmonate and salicylic acid elicitation induces ginsenosides accumulation, enzymatic and non-enzymatic antioxidant in suspension culture Panax ginseng roots in bioreactors. Plant Cell Rep 25:613–620

    Article  CAS  PubMed  Google Scholar 

  • Ali M, Hahn EJ, Paek KY (2007) Methyl jasmonate and salicylic acid induced oxidative stress and accumulation of phenolics in Panax ginseng bioreactor root suspension cultures. Molecules 12:607–621

    Article  CAS  PubMed  Google Scholar 

  • Baeg IH, So SH (2013) The world ginseng market and the ginseng (Korea). J Gins Res 37:1–7

    Article  Google Scholar 

  • Chang WC, Hsing YI (1980) Plant regeneration through somatic embryogenesis in root-derived callus of ginseng (Panax ginseng C. A. Meyer). Theor Appl Genet 57:133–135

    Article  CAS  PubMed  Google Scholar 

  • Chhotaram S, Rupali K, Pandurang D, Pallavi S (2010) Ginseng—multipurpose herb. J Biomed Sci Res 2(1):6–17

    Google Scholar 

  • Choi DW, Jung J, Ha YI, Park HW, In DS, Chung HJ, Liu JR (2005) Analysis of transcripts in methyl jasmonate-treated ginseng hairy roots to identify genes involved in the biosynthesis of ginsenosides and other secondary metabolites. Plant Cell Rep 23:557–566

    Article  CAS  PubMed  Google Scholar 

  • Cui S, Huang F, Wang J, Ma X, Cheng YS, Liu JY (2005) A proteomic analysis of cold stress responses in rice seedlings. Proteomics 5:3162–3172

    Article  CAS  PubMed  Google Scholar 

  • Dai Z, Wang B, Liu Y, Shi M, Wang D, Zhang X, Liu T, Huang L, Zhang X (2014) Producing aglycones of ginsenosides in bakers’ yeast. Sci Rep 4:3698

    PubMed  PubMed Central  Google Scholar 

  • Devi BS, Kim YJ, Selvi SK, Gayathri S, Altanzul K, Parvin S, Yang DU, Lee OR, Lee S, Yang DC (2012) Influence of potassium nitrate on antioxidant level and secondary metabolite genes under cold stress in Panax ginseng. Russ J Plant Phys 59:318–325

    Article  CAS  Google Scholar 

  • Gorpenchenko TY, Kiselev KV, Bulgakov VP, Tchernoded GK, Bragina EA, Khodakovskaya MV, Koren OG, Batygina TB, Zhuravlev YN (2006) The agrobacterium rhizogenes rolC-gene-induced somatic embryogenesis and shoot organogenesis in panax ginseng transformed calluses. Planta 223(3):457–467

  • Goulas E, Schubert M, Kieselbach T, Kleczkowski LA, Gardeström P, Schröder W, Hurry V (2006) The chloroplast lumen and stromal proteomes of Arabidopsis thaliana show differential sensitivity to short- and long-term exposure to low temperature. Plant J 47:720–734

    Article  CAS  PubMed  Google Scholar 

  • Guo Z, Ou W, Lu S, Zhong Q (2006) Differential responses of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. Plant Physiol Biochem 44:828–836

    Article  CAS  PubMed  Google Scholar 

  • Han JY, Kwon YS, Yang DC, Jung YR, Choi YE (2006) Expression and RNA interference-induced silencing of the dammarenediol synthase gene in Panax ginseng. Plant Cell Physiol 47:1653–1662

    Article  CAS  PubMed  Google Scholar 

  • Han JY, Kim HJ, Kwon YS, Choi YE (2011) The Cyt P450 enzyme CYP716A47 catalyzes the formation of protopanaxadiol from dammarenediol-II during ginsenoside biosynthesis in Panax ginseng. Plant Cell Physiol 52:2062–2073

    Article  CAS  PubMed  Google Scholar 

  • Han JY, Hwang HS, Choi SW, Kim HJ, Choi YE (2012) Cytochrome P450 CYP716A53v2 catalyzes the formation of protopanaxatriol from protopanaxadiol during ginsenoside biosynthesis in Panax ginseng. Plant Cell Physiol 53:1535–1545

    Article  CAS  PubMed  Google Scholar 

  • Han JY, Wang HY, Choi YE (2014) Production of dammarenediol-II triterpene in a cell suspension culture of transgenic tobacco. Plant Cell Rep 33:225–233

    Article  CAS  PubMed  Google Scholar 

  • Havaux M, Eymery F, Porfirova S, Rey P, Dörmann P (2005) Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. Plant Cell 17:3451–3469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu X, Neill SJ, Cai W, Tang Z (2003a) Hydrogen peroxide and jasmonic acid mediate oligogalacturonic acid-induced saponin accumulation in suspension-cultured cells of Panax ginseng. Physiol Plant 118:414–421

    Article  CAS  Google Scholar 

  • Hu X, Neill SJ, Cai W, Tang Z (2003b) Nitric oxide mediates elicitor-induced saponin synthesis in cell cultures of Panax ginseng. Funct Plant Biol 30:901–907

    Article  CAS  Google Scholar 

  • Huang C, Zhong JJ (2013) Elicitation of ginsenoside biosynthesis in cell cultures of Panax ginseng by vanadate. Process Biochem 48:1227–1234

    Article  CAS  Google Scholar 

  • Huang C, Qian ZG, Zhong JJ (2013) Enhancement of ginsenoside biosynthesis in cell cultures of Panax ginseng by N,N′-dicyclohexylcarbodiimide elicitation. J Biotechnol 165:30–36

    Article  CAS  PubMed  Google Scholar 

  • Jung SC, Kim W, Park SC, Jeong J, Park MK, Lim S, Lee Y, Im WT, Lee JH, Choi G, Kim SC (2014) Two ginseng UDP-glycosyl transferases synthesize ginsenoside Rg3 and Rd. Plant Cell Physiol 55(12):2177–2188

    Article  CAS  PubMed  Google Scholar 

  • Kim KT, Yoo KM, Lee JW, Eom SH, Hwang IK, Lee CY (2007) Protective effect of steamed American ginseng (Panax quinquefolius L.) on V79-4 cells induced by oxidative stress. J Ethnopharmacol 111:443–450

    Article  PubMed  Google Scholar 

  • Kim OT, Bang KH, Kim YC, Hyun DY, Kim MY, Cha SW (2009) Upregulation of ginsenoside and gene expression related to triterpene biosynthesis in ginseng hairy root cultures elicited by methyl jasmonate. Plant Cell Tiss Org 98:25–33

    Article  CAS  Google Scholar 

  • Kim DS, Song M, Kim SH, Jang DS, Kim JB, Ha BK, Kim SH, Lee KJ, Kang SY, Jeong IY (2013) The improvement of ginsenoside accumulation in Panax ginseng as a result of gamma-irradiation. J Gins Res 37:332–340

    Article  CAS  Google Scholar 

  • Kim YJ, Jeon JN, Jang MG, Oh JY, Kwon WS, Jung SK, Yang DC (2014) Ginsenoside profiles and related gene expression during foliation in Panax ginseng Meyer. J Gins Res 38:66–72

    Article  CAS  Google Scholar 

  • Korn M, Peterek S, Mock HP, Heyer AG, Hincha DK (2008) Heterosis in the freezing tolerance, and sugar and flavonoid contents of crosses between Arabidopsis thaliana accessions of widely varying freezing tolerance. Plant Cell Environ 31:813–827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuo YH, Ikegami F, Lambein F (2003) Neuroactive and other free amino acids in seed and young plants of Panax ginseng. Phytochemistry 62:1087–1091

    Article  CAS  PubMed  Google Scholar 

  • Lee MH, Han JY, Kim HJ, Kim YS, Huh GH, Choi YE (2012) Dammarenediol-II production confers TMV tolerance in transgenic tobacco expressing Panax ginseng dammarenediol-II synthase. Plant Cell Physiol 53:173–182

    Article  CAS  PubMed  Google Scholar 

  • Liang Y, Zhao S (2008) Progress in understanding of ginsenoside biosynthesis. Plant Biol 10:415–421

    Article  CAS  PubMed  Google Scholar 

  • Liu R, Zhang J, Liu W, Kimura Y, Zheng Y (2010) Anti-Obesity effects of protopanaxdiol types of ginsenosides isolated from the leaves of American ginseng (Panax quinquefolius L.) in mice fed with a high-fat diet. Fitoterapia 81:1079–1087

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu M, Wong H, Teng W (2001) Effects of elicitation on the production of saponin in cell culture of Panax ginseng. Plant Cell Rep 20:674–677

    CAS  Google Scholar 

  • Lukatkin AS (2010) Use of maize callus cultures for assessing chilling stress resistance. Russ Agric Sci 36:331–333

    Article  Google Scholar 

  • Oh JY, Kim YJ, Jang MG, Joo SC, Kwon WS, Kim SY, Jung SK, Yang DC (2014) Investigation of ginsenosides in different tissues after elicitor treatment in Panax ginseng. J Gins Res 38:270–277

    Article  CAS  Google Scholar 

  • Okubo K, Yoshiki Y (2000) The role of triterpenoid on reactive oxygen scavenging system: approach from the new chemiluminescence system (XYZ system). BioFactors 13:219–223

    Article  CAS  PubMed  Google Scholar 

  • Qi LW, Wang CZ, Yuan CS (2011) Ginsenosides from American ginseng: chemical and pharmacological diversity. Phytochemistry 72:689–699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruelland E, Vaultier MN, Zachowski A, Hurry V (2009) Cold signalling and cold acclimation in plants. Adv Bot Res 49:35–150

    Article  CAS  Google Scholar 

  • Shi W, Wang Y, Li J, Zhang H, Ding L (2007) Investigation of ginsenosides in different parts and ages of Panax ginseng. Food Chem 102:664–668

    Article  CAS  Google Scholar 

  • Sparg SG, Light ME, van Staden J (2004) Biological activities and distribution of plant saponins. J Ethnopharmacol 94:219–243

    Article  CAS  PubMed  Google Scholar 

  • Sun Y, Zhao SJ, Liang YL, Le W, Cao HJ (2013) Regulation and differential expression of protopanaxadiol synthase in Asian and American ginseng ginsenoside biosynthesis by RNA interferences. Plant Growth Regul 71:207–217

    Article  CAS  Google Scholar 

  • Tansakul P, Shibuya M, Kushiro T, Ebizuka Y (2006) Dammarenediol-II synthase, the first dedicated enzyme for ginsenoside biosynthesis, in Panax ginseng. FEBS Lett 580:5143–5149

    Article  CAS  PubMed  Google Scholar 

  • Thimmappa R, Geisler K, Louveau T, O’Maille P, Osbourn A (2014) Triterpene biosynthesis in plants. Annu Rev Plant Biol 65:225–257

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Gao WY, Zhang J, Zuo BM, Zhang LM, Huang LQ (2011) Advances in study of ginsenoside biosynthesis pathway in Panax ginseng C. A. Meyer. Acta Physiol Plant 34:397–403

    Article  Google Scholar 

  • Wang J, Gao W, Zuo B, Zhang L, Huang L (2012) Effect of methyl jasmonate on the ginsenoside content of Panax ginseng adventitious root cultures and on the genes involved in triterpene biosynthesis. Res Chem Intermed 39:1973–1980

    Article  Google Scholar 

  • Wu J, Lin L (2002) Elicitor-like effects of low-energy ultrasound on plant (Panax ginseng) cells: induction of plant defense responses and secondary metabolite production. Appl Microbiol Biot 59:51–57

    Article  CAS  Google Scholar 

  • Yan SP, Zhang QY, Tang ZC, Su WA, Sun WN (2006) Comparative proteomic analysis provides new insights into chilling stress responses in rice. Mol Cell Proteom 5:484–496

    Article  CAS  Google Scholar 

  • Yan X, Fan Y, Wei W, Wang P, Liu Q, Wei Y, Zhang L, Zhao G, Yue J, Zhou Z (2014) Production of bioactive ginsenoside compound K in metabolically engineered yeast. Cell Res 24:770–773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • You J, Liu X, Zhang B, **e Z, Hou Z, Yang Z (2015) Seasonal changes in soil acidity and related properties in ginseng artificial bed soils under a plastic shade. J Gins Res 39:81–88

    Article  CAS  Google Scholar 

  • Yu KW, Gao W, Hahn EJ, Paek KY (2002) Jasmonic acid improves ginsenoside accumulation in adventitious root culture of Panax ginseng C.A. Meyer. Biochem Eng J 11:211–215

    Article  CAS  Google Scholar 

  • Zhang J, Sun Y, Wang Y, Lu M, He J, Liu J, Chen Q, Zhang X, Zhou F, Wang G, Sun X (2014) Non-antibiotic agent ginsenoside 20(S)-Rh2 enhanced the antibacterial effects of ciprofloxacin in vitro and in vivo as a potential NorA inhibitor. Eur J Pharmacol 740:277–284

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was funded by the National Natural Science Foundation of China (21462044).

Author information

Authors and Affiliations

  1. Key Laboratory of Nature Resource of Changbai Mountain and Functional Molecular, Yanbian University, Ministry of Education, Park Road 977, Yanji, 133002, Jilin, China

    Mingliang Jiang, Jia Liu, Xueli Quan, Linhu Quan & Songquan Wu

Authors
  1. Mingliang Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jia Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xueli Quan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Linhu Quan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Songquan Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Linhu Quan or Songquan Wu.

Additional information

Communicated by S Renault.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiang, M., Liu, J., Quan, X. et al. Different chilling stresses stimulated the accumulation of different types of ginsenosides in Panax ginseng cells. Acta Physiol Plant 38, 210 (2016). https://doi.org/10.1007/s11738-016-2210-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-016-2210-y

Keywords

Search

Navigation