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Roles of reactive oxygen species in methyl jasmonate and nitric oxide-induced tanshinone production in Salvia miltiorrhiza hairy roots

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Abstract

Salvia miltiorrhiza is one of the most popular traditional Chinese medicinal plants for treatment of coronary heart disease. Tanshinones are the main biological active compounds in S. miltiorrhiza. In this study, effects of exogenous methyl jasmonate (MJ) and nitric oxide (NO) on tanshinone production in S. miltiorrhiza hairy roots were investigated and the roles of reactive oxygen species (ROS) in MJ and NO-induced tanshinone production were elucidated further. The results showed that contents of four tanshinone compounds were significantly increased by 100 μM MJ when compared to the control. Application of 100 μM sodium nitroprusside (SNP), a donor of NO, also resulted in a significant increase of tanshinone production. Expression of two key genes encoding 3-hydroxy-3-methylglutaryl coenzyme A reductase (HMGR) and 1-deoxy-d-xylulose 5-phosphate reductoisomerase (DXR) was up-regulated by MJ and SNP. Generations of O2 − and H2O2 were triggered by MJ, but not by SNP. The increase of tanshinone production and up-regulation of HMGR and DXR expression induced by MJ were significantly inhibited by ROS scavengers, superoxide dismutase (SOD) and catalase (CAT). However, neither SOD nor CAT was able to suppress the SNP-induced increase of tanshinone production and expression of HMGR and DXR gene. In conclusion, tanshinone production was significantly stimulated by MJ and SNP. Of four tanshinone compounds, cryptotanshinone accumulation was most affected by MJ elicitation, while cryptotanshinone and tanshinone IIA accumulation was more affected by SNP elicitation. ROS mediated MJ-induced tanshinone production, but SNP-induced tanshinone production was ROS independent.

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References

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  PubMed  CAS  Google Scholar 

  • Bach TJ, Lichtenthaler HK (1982) Mevinolin: a highly specific inhibitor of microsomal 3-hydroxy-3-methylglutaryl-coenzyme A reductase of radish plants. Z Naturforsch [C] 37:46–50

    CAS  Google Scholar 

  • Chen H, Chen F (1999) Effects of methyl jasmonate and salicylic acid on cell growth and cryptotanshinone formation in Ti transformed Salvia miltiorrhiza cell suspension cultures. Biotechnol Lett 21:803–807

    Article  CAS  Google Scholar 

  • Dai Z, Cui G, Zhou SF, Zhang X, Huang L (2011) Cloning and characterization of a novel 3-hydroxy-3-methylglutaryl coenzyme A reductase gene from Salvia miltiorrhiza involved in diterpenoid tanshinone accumulation. J Plant Physiol 168:148–157

    Article  PubMed  CAS  Google Scholar 

  • Exposito O, Syklowska-Baranek K, Moyano E, Onrubia M, Bonfill M, Palazon J, Cusido RM (2010) Metabolic responses of Taxus media transformed cell cultures to the addition of methyl jasmonate. Biotechnol Prog 26:1145–1153

    PubMed  CAS  Google Scholar 

  • Ge XC, Wu JY (2005) Tanshinone production and isoprenoid pathways in Salvia miltiorrhiza hairy roots induced by Ag+ and yeast elicitor. Plant Sci 168:487–491

    Article  CAS  Google Scholar 

  • Han JY, Fan JY, Horie Y, Miura S, Cui DH, Ishii H, Hibi T, Tsuneki H, Kimura I (2008) Ameliorating effects of compounds derived from Salvia miltiorrhiza root extract on microcirculatory disturbance and target organ injury by ischemia and reperfusion. Pharmacol Ther 117:280–295

    Article  PubMed  CAS  Google Scholar 

  • Hu ZB, Alfermann AW (1993) Diterpenoid production in hairy root cultures of Salvia miltiorrhiza. Phytochemistry 32:699–703

    Article  CAS  Google Scholar 

  • Jomaa H, Wiesner J, Sanderbrand S, Altincicek B, Weidemeyer C, Hintz M, Turbachova I, Eberl M, Zeidler J, Lichtenthaler HK, Soldati D, Beck E (1999) Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 285:1573–1576

    Article  PubMed  CAS  Google Scholar 

  • Kai G, Xu H, Zhou C, Liao P, Xiao J, Luo X, You L, Zhang L (2011) Metabolic engineering tanshinone biosynthetic pathway in Salvia miltiorrhiza hairy root cultures. Metab Eng 13:319–327

    Article  PubMed  CAS  Google Scholar 

  • Liao P, Zhou W, Zhang L, Wang J, Yan XM, Zhang Y, Zhang R, Li L, Zhou GY, Kai GY (2009) Molecular cloning, characterization and expression analysis of a new gene encoding 3-hydroxy-3-methylglutaryl coenzyme A reductase from Salvia miltiorrhiza. Acta Physiol Plant 31:565–572

    Article  CAS  Google Scholar 

  • Liu Z, Yu LJ, Li CY, Zhao CF (2005) Effects of fosmidomycin and lovastatin treatment on taxol biosynthesis in suspension culture cells of Taxus chinensis. Zhi Wu Sheng Li Yu Fen Zi Sheng Wu Xue Xue Bao 31:199–204

    PubMed  CAS  Google Scholar 

  • Memelink J, Verpoorte R, Kijne JW (2001) ORCAnization of jasmonate—responsive gene expression in alkaloid metabolism. Trends Plant Sci 6:212–219

    Article  PubMed  CAS  Google Scholar 

  • Perassolo M, Quevedo CV, Busto VD, Giulietti AM, Talou JR (2011) Role of reactive oxygen species and proline cycle in anthraquinone accumulation in Rubia tinctorum cell suspension cultures subjected to methyl jasmonate elicitation. Plant Physiol Biochem 49:758–763

    Article  PubMed  CAS  Google Scholar 

  • Perrone ST, McDonald KL, Sutherland MW, Guest DI (2003) Superoxide release is necessary for phytoalexin accumulation in Nicotiana tabacum cells during the expression of cultivar-race and non-host resistance towards Phytophthora spp. Physiol Mol Plant Pathol 62:127–135

    Article  CAS  Google Scholar 

  • Preston TJ, Muller WJ, Singh G (2001) Scavenging of extracellular H2O2 by catalase inhibits the proliferation of HER-2/Neu-transformed rat-1 fibroblasts through the induction of a stress response. J Biol Chem 276:9558–9564

    Article  PubMed  CAS  Google Scholar 

  • Ren A, Qin L, Shi L, Dong X, Mu da S, Li YX, Zhao MW (2010) Methyl jasmonate induces ganoderic acid biosynthesis in the basidiomycetous fungus Ganoderma lucidum. Bioresour Technol 101:6785–6790

    Article  PubMed  CAS  Google Scholar 

  • Sarath G, Bethke PC, Jones R, Baird LM, Hou GC, Mitchell RB (2006) Nitric oxide accelerates seed germination in warm-season grasses. Planta 223:1154–1164

    Article  PubMed  CAS  Google Scholar 

  • Shao JR, Zhou ML, Zhu XM, Wu YM, Tang YX (2010) Transcriptional response of the catharanthine biosynthesis pathway to methyl jasmonate/nitric oxide elicitation in Catharanthus roseus hairy root culture. Appl Microbiol Biotechnol 88:737–750

    Article  PubMed  Google Scholar 

  • Song LL, Ding W, Shen J, Zhang ZG, Bi YR, Zhang LX (2008) Nitric oxide mediates abscisic acid induced thermotolerance in the calluses from two ecotypes of reed under heat stress. Plant Sci 175:826–832

    Article  CAS  Google Scholar 

  • Srivastava N, Gonugunta VK, Puli MR, Raghavendra AS (2009) Nitric oxide production occurs downstream of reactive oxygen species in guard cells during stomatal closure induced by chitosan in abaxial epidermis of Pisum sativum. Planta 229:757–765

    Article  PubMed  CAS  Google Scholar 

  • Suhita D, Raghavendra AS, Kwak JM, Vavasseur A (2004) Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure. Plant Physiol 134:1536–1545

    Article  PubMed  CAS  Google Scholar 

  • Sun Q, Hu JJ (2006) Research technology of plant physiology. Northwest A&F University Press, Yangling

    Google Scholar 

  • Tewari RK, Hahn EJ, Paek KY (2008) Function of nitric oxide and superoxide anion in the adventitious root development and antioxidant defence in Panax ginseng. Plant Cell Rep 27:563–573

    Article  PubMed  CAS  Google Scholar 

  • Wang JW, Wu JY (2004) Involvement of nitric oxide in elicitor-induced defense responses and secondary metabolism of Taxus chinensis cells. Nitric Oxide Biol Chem 11:298–306

    Article  CAS  Google Scholar 

  • Wang JW, Wu JY (2005) Nitric oxide is involved in methyl jasmonate-induced defense responses and secondary metabolism activities of Taxus cells. Plant Cell Physiol 46:923–930

    Article  PubMed  CAS  Google Scholar 

  • Wang JW, Zheng LP, Zhang B, Zou T (2009) Stimulation of artemisinin synthesis by combined cerebroside and nitric oxide elicitation in Artemisia annua hairy roots. Appl Microbiol Biotechnol 85:285–292

    Article  PubMed  CAS  Google Scholar 

  • Wu JY, Wu SJ, Shi M (2009a) Cloning and characterization of the 1-deoxy-d-xylulose 5-phosphate reductoisomerase gene for diterpenoid tanshinone biosynthesis in Salvia miltiorrhiza (Chinese sage) hairy roots. Biotechnol Appl Biochem 52:89–95

    Article  PubMed  CAS  Google Scholar 

  • Wu SJ, Qi JL, Zhang WJ, Liu SH, Xiao FH, Zhang MS, Xu GH, Zhao WG, Shi MW, Pang YJ, Shen HG, Yang YH (2009b) Nitric oxide regulates shikonin formation in suspension-cultured Onosma paniculatum cells. Plant Cell Physiol 50:118–128

    Article  PubMed  CAS  Google Scholar 

  • Xiao Y, Gao S, Di P, Chen J, Chen W, Zhang L (2009) Methyl jasmonate dramatically enhances the accumulation of phenolic acids in Salvia miltiorrhiza hairy root cultures. Physiol Plant 137:1–9

    Article  CAS  Google Scholar 

  • Xu MJ, Dong JF (2005a) Nitric oxide stimulates indole alkaloid production in Catharanthus roseus cell suspension cultures through a protein kinase-dependent signal pathway. Enzyme Microb Technol 37:49–53

    Article  CAS  Google Scholar 

  • Xu MJ, Dong JF (2005b) O-2- from elicitor-induced oxidative burst is necessary for triggering phenylalanine ammonia-lyase activation and catharanthine synthesis in Catharanthus roseus cell cultures. Enzyme Microb Technol 36:280–284

    Article  CAS  Google Scholar 

  • Yang D, Yang S, Zhang Y, Liu Y, Meng X, Liang Z (2009a) Metabolic profiles of three related Salvia species. Fitoterapia 80:274–278

    Article  PubMed  CAS  Google Scholar 

  • Yang DF, Liang ZS, Liu JL (2009b) LC fingerprinting for assessment of the quality of the lipophilic components of Salvia miltiorrhiza. Chromatographia 69:555–560

    Article  CAS  Google Scholar 

  • Zhang L, Xing D (2008) Methyl jasmonate induces production of reactive oxygen species and alterations in mitochondrial dynamics that precede photosynthetic dysfunction and subsequent cell death. Plant Cell Physiol 49:1092–1111

    Article  PubMed  CAS  Google Scholar 

  • Zhao J, Hu Q, Guo Y-Q, Zhu W-H (2001) Elicitor-induced indole alkaloid biosynthesis in Catharanthus roseus cell cultures is related to Ca2+ influx and the oxidative burst. Plant Sci 161:423–431

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Zhao JL, Zhou LG, Wu JY (2010) Effects of biotic and abiotic elicitors on cell growth and tanshinone accumulation in Salvia miltiorrhiza cell cultures. Appl Microbiol Biotechnol 87:137–144

    Article  PubMed  CAS  Google Scholar 

  • Zheng LP, Zhang B, Zou T, Chen ZH, Wang JW (2010) Nitric oxide interacts with reactive oxygen species to regulate oligosaccharide-induced artemisinin biosynthesis in Artemisia annua hairy roots. J Med Plants Res 4:758–766

    CAS  Google Scholar 

  • Zhu Z, Liang Z, Han R (2009) Saikosaponin accumulation and antioxidative protection in drought-stressed Bupleurum chinense DC. plants. Environ Exp Bot 66:326–333

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by Knowledge Innovation Project of Chinese Academy of Science (KZCX2-YW-443).

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Authors and Affiliations

  1. College of Life Science of Zhejiang Sci-Tech University, Hangzhou, 310018, People’s Republic of China

    Zong-Suo Liang

  2. College of Life Science of Northwest A&F University, Yangling, 712100, People’s Republic of China

    Zong-Suo Liang, Dong-Feng Yang, Xiao Liang & Yue-Jin Zhang

  3. Tianjin Tasly Modern TCM Resources Co., Ltd, Tianjin, 300402, People’s Republic of China

    Yan Liu & Feng-Hua Liu

Authors
  1. Zong-Suo Liang
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  2. Dong-Feng Yang
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  3. Xiao Liang
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  4. Yue-Jin Zhang
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  5. Yan Liu
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  6. Feng-Hua Liu
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Correspondence to Zong-Suo Liang.

Additional information

Communicated by M. Petersen.

D.-F. Yang is the co-first author.

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Liang, ZS., Yang, DF., Liang, X. et al. Roles of reactive oxygen species in methyl jasmonate and nitric oxide-induced tanshinone production in Salvia miltiorrhiza hairy roots. Plant Cell Rep 31, 873–883 (2012). https://doi.org/10.1007/s00299-011-1208-6

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  • DOI: https://doi.org/10.1007/s00299-011-1208-6

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