Skip to main content
SpringerLink
Log in

Nitric Oxide Elicitation Induces the Accumulation of Secondary Metabolites and Antioxidant Defense in Adventitious Roots ofEchinacea purpurea

  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Nitric oxide and reactive oxygen species are important signal molecules that play key roles in plant defense responses. We investigated the involvement of nitric oxide elicitation in the synthesis of secondary metabolites within the adventitious roots ofEchinacea purpurea. When roots were treated with 100 μM sodium nitroprusside (SNP), an exogenous nitric oxide producer, the accumulation of phenolics, flavonoids, and caffeic acid derivatives was enhanced. This level of SNP also induced an antioxidant defense, as indicated by increases in Superoxide dismutase, ascorbate peroxidase, and ascorbic acid, along with decreases in hydrogen peroxide, lipid peroxidation, and dehydroascorbate/ascorbic acid. However, a higher concentration (250 μM SNP) acted as a pro-oxidant, thereby raising the levels of hydrogen peroxide, lipid peroxidation, and dehydroascorbate/ascorbic acid while diminishing ascorbic acid, ascorbate peroxidase, and the accumulation of secondary metabolites compared with our observations at 100 μM SNP. Therefore, we conclude that elicitingE. purpurea adventitious roots with a concentration of 100 μM SNP is beneficial to their accumulation of secondary metabolites.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Literature Cited

  • Ali MB, Hahn EJ, Paek KY (2006) Antioxidative responses of Echinaceaangustifolia cultured roots to different levels of CO2 in bioreactor liquid cultures. Enzyme Microb Technol39: 982–990

    Article  CAS  Google Scholar 

  • Baker CJ, Orlandi EW (1995) Active oxygen in plant pathogenesis. Annu Rev Phytopathol33: 299–321

    Article  PubMed  CAS  Google Scholar 

  • Barrett B (2003) Medicinal properties ofEchinacea: A critical review. Phytomedicine10: 66–86.

    Article  PubMed  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: Improved assays and assays applicable to acrylamide gels. Anal Biochem44: 276–287

    Article  PubMed  CAS  Google Scholar 

  • Beligni MV, Lamattina L (2000) Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light inducible responses in plants. Planta210: 215–222

    Article  PubMed  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem72: 248–254

    Article  PubMed  CAS  Google Scholar 

  • Brennan T, Frenkel C (1977) Involvement of hydrogen peroxide in regulation of senescence in pear. Plant Physiol59: 411–416

    Article  PubMed  CAS  Google Scholar 

  • Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a secondary signal in plant disease resistance.Nature394: 585–588

    Article  PubMed  CAS  Google Scholar 

  • Delledonne M, Zeier J, Marocco A (2001) Signal interaction between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci USA98: 13454–13459

    Article  PubMed  CAS  Google Scholar 

  • Dietrich A, Mayer JE, Hahlbrock K (1990) Fungal elicitor triggers rapid, transient, and specific protein phosphorylation in parsley cell suspension cultures. J Biol Chem265: 6360–6368

    PubMed  CAS  Google Scholar 

  • Durner J, Wendehenne D, Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic CMP and cyclic ADP-ribose. Proc Natl Acad Sci USA95: 10328–10333

    Article  PubMed  CAS  Google Scholar 

  • Capper C, Dolan L (2006) Control of plant development by reactive oxygen species. Plant Physiol141: 341–345

    Article  Google Scholar 

  • Couvêa CMCP, Souza JF, Magalhães CAN, Martins IS (1997) NO-releasing substances that induce growth elongation in maize root segments. Plant Growth Reg21: 183–187

    Article  Google Scholar 

  • Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol141: 312–322

    Article  PubMed  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplast, I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys125: 180–198

    Google Scholar 

  • Heldt HW (1997) Plant Biochemistry and Molecular Biology. Oxford University Press Inc., New York

    Google Scholar 

  • Hung KT, Chang CJ, Kao CH (2002) Paraquat toxicity is reduced by nitric oxide in rice leaves. J Plant Physiol159: 159–166

    Article  CAS  Google Scholar 

  • Liszkay A, van der Zalm E, Schopfer P (2004) Production of reactive oxygen intermediates O2, H2O2, and OH by maize roots and their role in wall loosening and elongation growth. Plant Physiol136: 3114–3123

    Article  PubMed  CAS  Google Scholar 

  • Lombardo MC, Graziano M, Palacco JC, Lamattina L (2006) Nitric oxide functions as a positive regulator of root hair development. Plant Signal Behav1: 28–33

    Google Scholar 

  • Morot-Gaudry-Talarmain Y, Rockel P, Moureaux T (2002) Nitrite accumulation and nitric oxide emission in relation to cellular signaling in nitrite reductase antisense plants. Planta215: 708–715

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant15: 473–497

    Article  CAS  Google Scholar 

  • Murgia I, Tarantino D, Vannini C, Bracale M, Carravieri S, Soave C (2004)Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to paraquat induced photooxidative stress and to nitric oxide-induced cell death. Plant J38: 940–953

    Article  PubMed  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplast. Plant Cell Physiol22: 867–880

    CAS  Google Scholar 

  • Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signaling in plants. New Phytol159: 11–22

    Article  CAS  Google Scholar 

  • Nürnberger T, Colling C, Hahlbrock K (1994) Perception and transduction of an elicitor signal in cultured parsley cells. Biochem Soc Symp60: 173–182

    PubMed  Google Scholar 

  • Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L (2002) Nitric oxide is required for root organogenesis. Plant Physiol129: 954–956

    Article  PubMed  CAS  Google Scholar 

  • Pagnussat GC, Lanteri ML, Lamattina L (2003) Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol132: 1241–1248

    Article  PubMed  CAS  Google Scholar 

  • Pedroso MC, Magalhaes JR, Durzan D (2000) Nitric oxide induces cell death in Taxus cells. Plant Sci157: 173–180

    Article  PubMed  CAS  Google Scholar 

  • Pellati F, Benvenuti S, Magro L, Melegari M, Soragni F (2004) Analysis of phenolic compounds and radical scavenging activity ofEchinacea spp. J Pharm Biomed Anal35: 289–301

    Article  PubMed  CAS  Google Scholar 

  • Pütter J (1974) Peroxidases.In Bergmeyer HU, ed, Methods of Enzymatic Analysis, Vol 2. Academic Press, New York, pp 685–690

    Google Scholar 

  • Rao MV, Hale BA, Ormrod DP (1995) Amelioration of ozone-induced oxidative damage in wheat plants grown under high carbon dioxide. Plant Physiol109: 421–432

    PubMed  CAS  Google Scholar 

  • Roberts SC, Shuler ML (1997) Large-scale plant cell culture. Curr Opin Biotechnol8: 154–159

    Article  PubMed  CAS  Google Scholar 

  • Romero-Puertas MC, Perazzolli M, Zago ED, Delledonne M (2004) Nitric oxide signaling functions in plant-pathogen interactions. Cell Microbiol6: 795–803

    Article  PubMed  CAS  Google Scholar 

  • Rubbo H, Radi R, Anselmi D, Kirk M, Barnes S, Butler J, Eiserich JP, Freeman BA (2000) Nitric oxide reaction with lipid peroxyl radicals spares alpha-tocopherol during lipid peroxidation. Greater oxidant protection from the pair nitric oxide/alphatocopherol than alpha-tocopherol/ascorbate. J Biol Chem275: 10812–10818

    Article  PubMed  CAS  Google Scholar 

  • Sagi M, Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol141: 336–340

    Article  PubMed  CAS  Google Scholar 

  • Sakanaka S, Tachibana Y, Okada Y (2005) Preparation and antioxidant properties of extracts of Japanese persimmon leaf tea (Kakinoha-cha). Food Chem89: 569–575

    Article  CAS  Google Scholar 

  • Sarath G, Bethke PC, Jones R, Baird LM, Hou G, Mitchell RB (2006) Nitric oxide accelerates seed germination in warm-season grasses. Planta223: 1154–1164

    Article  PubMed  CAS  Google Scholar 

  • Takahama U, Oniki T (1992) Regulation of peroxidase-dependent oxidation of phenolics in the apoplast of spinach leaves by ascorbate. Plant Cell Physiol33: 379–387

    CAS  Google Scholar 

  • Tewari RK, Hahn EJ, Paek KY (2007) Function of nitric oxide and Superoxide anion in the adventitious root development and antioxidant defence in Panax ginseng. Plant Cell Rep DOI 10.1007/s00299-007-0448-y

  • Uchida A, Jagendorf AT, Hibino T, Takabe T, Takabe T (2002) Effect of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci163: 515–523

    Article  CAS  Google Scholar 

  • Wach MJ, Kers JA, Krasnoff SB, Loria R, Gibson DM (2005) Nitric oxide synthase inhibitors and nitric oxide donors modulate the biosynthesis of thaxtomin A, a nitrated phytotoxin produced byStreptomyces spp. Nitric Oxide12: 46–53

    Article  PubMed  CAS  Google Scholar 

  • Wang JW, Wu JY (2004) Involvement of nitric oxide in elicitor- induced defense responses and secondary metabolism ofTaxus chinensis cells. Nitric Oxide11: 298–306

    Article  PubMed  CAS  Google Scholar 

  • Wang JW, Wu JY (2005) Nitric oxide is involved in methyl jas-monate-induced defense responses and secondary metabolism activities of Taxus cells. Plant Cell Physiol46: 923–930

    Article  PubMed  CAS  Google Scholar 

  • Wang JW, Zheng LP, Wu JY, Tan RX (2006) Involvement of nitric oxide in oxidative burst, phenylalanine ammonia-lyase activation and taxol production induced by low-energy ultrasound inTaxus yunnanensis cell suspension cultures. Nitric Oxide15: 351–358

    Article  PubMed  CAS  Google Scholar 

  • Wink DA, Cook JA, Pacelli R, Liebmann J, Krishne MC, Mitchell JB (1995) Nitric oxide (NO) protects against cellular damage by reactive oxygen species. Toxicol Lett82-83: 221–226

    Article  PubMed  CAS  Google Scholar 

  • Wu CH, Dewir YH, Hahn EJ, Paek KY (2006) Optimization of culturing conditions for the production of biomass and phenolics from adventitious roots ofEchinacea angustifolia. J Plant Biol49: 193–199

    Article  CAS  Google Scholar 

  • Wu J, Lin L (2003) Enhancement of taxol production and release in Taxuschinensis cell cultures by ultrasound, methyl jasmonate and in situ solvent extraction. Appl Microbiol Biotechnol62: 151–155

    Article  PubMed  CAS  Google Scholar 

  • Xu M-J, Dong JF, Zhu MY (2005) Nitric oxide mediates the fungal elicitor-induced hypericin production ofHypericum perforatum cell suspension cultures through a jasmonic-acid-dependent signal pathway. Plant Physiol139: 991–998

    Article  PubMed  CAS  Google Scholar 

  • Yuan YJ, Li C, Hu ZD, Wu JC (2001) Signal transduction pathway for oxidative burst and taxol production in suspension cultures of Taxuschinensis var. mairei induced by oligosaccharide fromFusarium oxysporum. Enzyme Microb Technol29: 372–379

    Article  CAS  Google Scholar 

  • Zhou B, Guo Z, Xing J, Huang B (2005) Nitric oxide is involved in abscisic acid-induced antioxidant activities inStylosanthes guianensis. J Exp Bot56: 3223–3228

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Research Center for the Development of Advanced Horticultural Technology, Chungbuk National University, 361-763, Cheongju, Republic of Korea

    Chun-Hua Wu, Rajesh Kumar Tewari, Eun-Joo Hahn & Kee-Yoeup Paek

Authors
  1. Chun-Hua Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rajesh Kumar Tewari
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eun-Joo Hahn
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kee-Yoeup Paek
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Rajesh Kumar Tewari or Kee-Yoeup Paek.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wu, CH., Tewari, R.K., Hahn, EJ. et al. Nitric Oxide Elicitation Induces the Accumulation of Secondary Metabolites and Antioxidant Defense in Adventitious Roots ofEchinacea purpurea . J. Plant Biol. 50, 636–643 (2007). https://doi.org/10.1007/BF03030607

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03030607

Keywords

Search

Navigation