Production of ginseng saponins: elicitation strategy and signal transductions

Applied Microbiology and Biotechnology

Volumn 99, Issue 17, 2015, Pages 6987-6996

  Rahimi, Shadi ^a   Kim, Yu Jin ^a   Yang, Deok Chun ^a  

^a Kyung Hee University   (South Korea)

Author keywords

Elicitation; Ginseng; Ginsenoside; Jasmonic acid; Signal transduction

Indexed keywords

BACTERIOPHAGES; ETHYLENE; METABOLITES; MOLECULES; NITRIC OXIDE; PHARMACODYNAMICS; PLANTS (BOTANY); TISSUE CULTURE;

ELICITATION; GINSENG; GINSENOSIDE ACCUMULATION; GINSENOSIDES; JASMONIC ACIDS; PHARMACOLOGICAL EFFECTS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION PATHWAYS;

SIGNAL TRANSDUCTION;

CALCIUM; ETHYLENE; GINSENOSIDE; JASMONIC ACID; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; SAPONIN; SAPONIN DERIVATIVE; TRITERPENE; CYCLOPENTANE DERIVATIVE; OXYLIPIN;

BIOACCUMULATION; BIOACTIVITY; BIOLOGICAL PRODUCTION; CULTIVATION; DRUG; ETHYLENE; FATTY ACID; GENE EXPRESSION; HERB; HETEROGENEITY; NITRIC OXIDE; ORGANIC COMPOUND; OXYGEN; PERENNIAL PLANT; SECONDARY METABOLITE; STEROID;

CALCIUM SIGNALING; GINSENG; METABOLITE; NONHUMAN; ORIENTAL MEDICINE; PLANT ROOT; REVIEW; SIGNAL TRANSDUCTION; TISSUE CULTURE; CHEMISTRY; DRUG EFFECTS; GENE EXPRESSION REGULATION; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; PANAX; TRANSCRIPTION INITIATION;

PANAX GINSENG;

CALCIUM; CYCLOPENTANES; GENE EXPRESSION REGULATION, PLANT; HUMANS; NITRIC OXIDE; OXYLIPINS; PANAX; REACTIVE OXYGEN SPECIES; SAPONINS; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION;

EID: 84939263311     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-015-6806-8     Document Type: Review

References (59)

1. Ali MB, Yu KW, Hahn EJ, Paek KY (2005) Differential responses of anti-oxidants enzymes, lipoxygenase activity, ascorbate content and the production of saponins in tissue cultured root of mountain Panax ginseng CA Mayer and Panax quinquefolium L. in bioreactor subjected to methyl jasmonate stress. Plant Sci 169(1):83–92
2. 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(10):1122–1132
3. 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(6):613–620
4. Bae KH, Choi YE, Shin CG, Kim YY, Kim YS (2006) Enhanced ginsenoside productivity by combination of ethephon and methyl jasmoante in ginseng (Panax ginseng CA Meyer) adventitious root cultures. Biotechnol Lett 28(15):1163–1166
5. Choudhury S, Panda P, Sahoo L, Panda SK (2013) Reactive oxygen species signaling in plants under abiotic stress. Plant Signal Behav 8(4):e23681
6. Devi BSR, Kim YJ, Sathiyamoorthy S, Khorolragchaa A, Gayathri S, Parvin S, Yang DU, Selvi SK, Lee OR, Lee S, Yang DC (2011) Classification and characterization of putative cytochrome P450 genes from Panax ginseng CA Meyer. Biochem Mosc 76(12):1347–1359
7. Dewir YH, Chakrabarty D, Wu CH, Hahn EJ, Jeon WK, Paek KY (2010) Influences of polyunsaturated fatty acids (PUFAs) on growth and secondary metabolite accumulation in Panax ginseng CA Meyer adventitious roots cultured in air-lift bioreactors. S Afr J Bot 76(2):354–358
8. Ferrari S (2010) Biological elicitors of plant secondary metabolites: mode of action and use in the production of nutraceutics. In Bio-farms for nutraceuticals, Springer US, p. 152-166
9. Fuzzati N (2004) Analysis methods of ginsenosides. J Chromatogr B Anal Technol Biomed Life Sci 812(1-2):119–133
10. Halliwell B, Gutteridge JMC (2006) Free radicals in biology and medicine, 4th edn. Oxford University Press, New York, p 968
11. 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(12):1653–1662
12. Hu FX, Zhong JJ (2007) Role of jasmonic acid in alteration of ginsenoside heterogeneity in elicited cell cultures of Panax notoginseng. J Biosci Bioeng 104(6):513–516
13. Hu FX, Zhong JJ (2008) Jasmonic acid mediates gene transcription of ginsenoside biosynthesis in cell cultures of Panax notoginseng treated with chemically synthesized 2-hydroxyethyl jasmonate. Process Biochem 43(1):113–118
14. Hu X, Neill S, 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(3):414–421
15. 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(8):901–907
16. Huang C, Zhong JJ (2013) Elicitation of ginsenoside biosynthesis in cell cultures of Panax ginseng by vanadate. Process Biochem 48(8):1227–1234
17. 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(1):30–36
18. Khorolragchaa A, Kim YJ, Rahimi S, Sukweenadhi J, Jang MG, Yang DC (2014) Grouping and characterization of putative glycosyltransferase genes from Panax ginseng Meyer. Gene 536(1):186–192
19. Kim YS, Hahn EJ, Murthy HN, Paek KY (2004) Adventitious root growth and ginsenoside accumulation in Panax ginseng cultures as affected by methyl jasmonate. Biotechnol Lett 26(21):1619–1622
20. Kim YS, Yeung EC, Hahn EJ, Paek KY (2007) Combined effects of phytohormone, indole-3-butyric acid, and methyl jasmonate on root growth and ginsenoside production in adventitious root cultures of Panax ginseng CA Meyer. Biotechnol Lett 29(11):1789–1792
21. 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 Tissue Organ Cult 98(1):25–33
22. Kim YS, Han JY, Lim S, Kim HJ, Lee MH, Choi YE (2012) Overexpressing Arabidopsis jasmonic acid carboxyl methyltransferase (AtJMT) results in stimulation of root growth and ginsenoside heterogeneity in ‘Panax ginseng’. Plant Omics 5(1):28
23. Kim OT, Yoo NH, Kim GS, Kim YC, Bang KH, Hyun DY, Kim SH, Kim MY (2013) Stimulation of Rg3 ginsenoside biosynthesis in ginseng hairy roots elicited by methyl jasmonate. Plant Cell Tissue Organ Cult 112(1):87–93
24. Kim YJ, Lee OR, Oh JY, Jang MG, Yang DC (2014) Functional analysis of 3-hydroxy-3-methylglutaryl coenzyme A reductase encoding genes in triterpene saponin-producing ginseng. Plant Physiol 165(1):373–387
25. Kim YJ, Zhang D, Yang DC (2015) Biosynthesis and biotechnological production of ginsenosides. Biotechnol Adv
26. Lapous D, Mathieu Y, Guern J, Lauriere C (1998) Increase of defense gene transcripts by cytoplasmic acidification in tobacco cell suspensions. Planta 205(3):452–458
27. Liang Y, Wu J, Li Y, Li J, Ouyang Y, He Z, Zhao S (2014) Enhancement of ginsenoside biosynthesis and secretion by Tween 80 in Panax ginseng hairy roots. Biotechnol Appl Biochem 62(2):193–199
28. Lipinski M, Scholz M, Pieper K, Fischer R, Prüfer D, Müller KJ (2009) A squalene epoxidase from Nigella sativa participates in saponin biosynthesis and mediates terbinafine resistance in yeast. Cent Eur J Biol 4(2):163–169
29. Lu MB, Wong HL, Teng WL (2001) Effects of elicitation on the production of saponin in cell culture of Panax ginseng. Plant Cell Rep 20:647–677
30. Murthy HN, Georgiev MI, Kim YS, Jeong CS, Kim SJ, Park SY, Paek KY (2014) Ginsenosides: prospective for sustainable biotechnological production. Appl Microbiol Biotechnol 98(14):6243–6254
31. 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 Ginseng Res 38(4):270–277
32. Parmenter G, Littlejohn R (2000) Effect of shade on growth and photosynthesis of Panax ginseng. N Z J Crop Hortic Sci 28:255–269
33. 2 in abscisic acid-induced antioxidant defense in the seedlings of Panax ginseng. Mol Biol Rep 39(7):7327–7338
34. Radad K, Gille G, Liu L, Rausch WD (2006) Use of ginseng in medicine with emphasis on neurodegenerative disorders. J Pharmacol Sci 100:175–186
35. Rahimi S, Devi BSR, Khorolragchaa A, Kim YJ, Kim JH, Jung SK, Yang DC (2014) Effect of salicylic acid and yeast extract on the accumulation of jasmonic acid and sesquiterpenoids in Panax ginseng adventitious roots. Russ J Plant Physiol 61(6):811–817
36. Sathiyaraj G, Lee OR, Parvin S, Khorolragchaa A, Kim YJ, Yang DC (2011) Transcript profiling of antioxidant genes during biotic and abiotic stresses in Panax ginseng CA Meyer. Mol Biol Rep 38(4):2761–2769
37. Subramaniyam S, Mathiyalagan R, Natarajan S, Kim YJ, Jang MG, Park JH, Yang DC (2014) Transcript expression profiling for adventitious roots of Panax ginseng Meyer. Gene 546(1):89–96
38. Sun Y, Niu Y, Xu J, Li Y, Luo H, Zhu Y, Liu M, Wu Q, Song J, Sun C, Chen S (2013) Discovery of WRKY transcription factors through transcriptome analysis and characterization of a novel methyl jasmonate-inducible PqWRKY1 gene from Panax quinquefolius. Plant Cell Tissue Organ Cult 114(2):269–277
39. Suzuki H, Reddy MSS, Naoumkina M, Aziz N, May GD, Huhman DV, Sumner LW, Blount JW, Mendes P, Dixon RA (2005) Methyl jasmonate and yeast elicitor induce differential transcriptional and metabolic re-programming in cell suspension cultures of the model legume Medicago truncatula. Planta 220:696–707
40. Tewari RK, Paek KY (2011) Salicylic acid-induced nitric oxide and ROS generation stimulate ginsenoside accumulation in Panax ginseng roots. J Plant Growth Regul 30(4):396–404
41. Tewari RK, Lee SY, Hahn EJ, Paek KY (2007) Temporal changes in the growth, saponin content and antioxidant defense in the adventitious roots of Panax ginseng subjected to nitric oxide elicitation. Plant Biotechnol Rep 1(4):227–235
42. Tewari RK, Hahn EJ, Paek KY (2008) Function of nitric oxide and superoxide anion in the adventitious root development and antioxidant defense in Panax ginseng. Plant Cell Rep 27:563–573
43. Thanh NT, Murthy HN, Yu KW, Jeong CS, Hahn EJ, Paek KY (2006) Effect of oxygen supply on cell growth and saponin production in bioreactor cultures of Panax ginseng. J Plant Physiol 163(12):1337–1341
44. Thanh NT, Murthy HN, Paek KY (2014) Ginseng cell culture for production of ginsenosides. In: Paek KY, Murthy HN, Zhong JJ (eds) Production of biomass and bioactive compounds using bioreactor Technology. Springer, Dordrecht
45. Wang W, Zhong JJ (2002) Manipulation of ginsenoside heterogeneity in cell cultures of Panax notoginseng by addition of jasmonates. J Biosci Bioeng 93(1):48–53
46. Wang W, Zhao ZJ, Xu Y, Qian X, Zhong JJ (2006) Efficient induction of ginsenoside biosynthesis and alteration of ginsenoside heterogeneity in cell cultures of Panax notoginseng by using chemically synthesized 2-hydroxyethyl jasmonate. Appl Microbiol Biotechnol 70(3):298–307
47. Wang J, Gao WY, Zhang J, Huang T, Wen TT, Huang LQ (2011) Combination effect of lactoalbumin hydrolysate and methyl jasmonate on ginsenoside and polysaccharide production in Panax quinquefolium L. cells cultures. Acta Physiol Plant 33(3):861–866
48. Wang J, Gao WY, Zhang J, Zuo BM, Zhang LM, Huang LQ (2012) Advances in study of ginsenoside biosynthesis pathway in Panax ginseng CA Meyer. Acta Physiol Plant 34(2):397–403
49. Wang J, Gao W, Zuo B, Zhang L, Huang L (2013) 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(5):1973–1980
50. Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100(4):681–697
51. Wu JY, Wong K, Ho KP, Zhou LG (2005) Enhancement of saponin production in Panax ginseng cell culture by osmotic stress and nutrient feeding. Enzym Microb Technol 36(1):133–138
52. Wu CH, Popova EV, Hahn EJ, Paek KY (2009) Linoleic and α-linolenic fatty acids affect biomass and secondary metabolite production and nutritive properties of Panax ginseng adventitious roots cultured in bioreactors. Biochem Eng J 47(1):109–115
53. Xu X, Hu X, Neill SJ, Fang J, Cai W (2005) Fungal elicitor induces singlet oxygen generation, ethylene release and saponin synthesis in cultured cells of Panax ginseng CA Meyer. Plant Cell Physiol 46(6):947–954
54. Yu KW, Gao W, Hahn EJ, Paek KY (2002) Jasmonic acid improves ginsenoside accumulation in adventitious root culture of Panax ginseng CA Meyer. Biochem Eng J 11(2):211–215
55. Yu KW, Murthy HN, Hahn EJ, Paek KY (2005) Ginsenoside production by hairy root cultures of Panax ginseng: influence of temperature and light quality. Biochem Eng J 23(1):53–56
56. Yue CJ, Zhong JJ (2004) Impact of external calcium and calcium sensors on ginsenoside Rb1 biosynthesis by Panax notoginseng cells. Biotechnol Bioeng 89(4):444–452
57. Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23(4):283–333
58. Zhong JJ, Wang DJ (1996) Improvement of cell growth and production of ginseng saponin and polysaccharide in suspension cultures of Panax notoginseng: Cu 2+ effect. J Biotechnol 46(1):69–72
59. Zhou L, Cao X, Zhang R, Peng Y, Zhao S, Wu J (2007) Stimulation of saponin production in Panax ginseng hairy roots by two oligosaccharides from Paris polyphylla var. yunnanensis. Biotechnol Lett 29(4):631–634G