Skip to main content

Advertisement

SpringerLink
Log in

Studies on the glyphosate-induced amino acid starvation and addition of precursors on caffeic acid accumulation and profiles in adventitious roots of Echinacea purpurea (L.) Moench

  • Original Paper
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

Shikimate pathway leads to the production of several secondary metabolites including caffeic acid derivatives (CADs), phenols and flavonoids and its regulation is assumed to respond to the requirements for both the synthesis of protein and secondary metabolites. We tested the response of growth, accumulation of phenols, flavonoids, caffeic acid, CADs profiles and activities of shikimate dehydrogenase (SKDH; EC. 1.1.1.25), chorismate mutase (CM; EC. 5.4.99.5), phenylalanine ammonia lyase (PAL; EC. 4.3.1.5) to glyphosate-induced starvation and feeding of aromatic amino acids (l-phenylalanine and l-tryptophan) in adventitious root cultures of Echinacea purpurea. Feeding of l-phenylalanine enhanced the growth but the accumulation of phenols, flavanoids and caffeic acid was lower in comparison to the l-tryptophan fed cultures. The addition of l-tryptophan (0.5, 1 and 5 mM) resulted in an increase up to 56, 61, 84 % in phenol, 24, 12, 3 % in flavonoids and 86, 63, 39 % in total caffeic acid. When glyphosate was added, the growth and accumulation of secondary metabolites were suppressed massively. The addition of l-tryptophan to the media not only countered the deleterious impact of glyphosate but enhanced the growth and accumulation of secondary metabolites in root cultures. The activity of SKDH, CM and PAL induced in presence of l-tryptophan. However, l-phenylalanine addition resulted in increase and decrease of PAL and CM activity, respectively. The presence of glyphosate maximally induced the PAL activity but that could not be translated into higher accumulation of secondary metabolites as it suppresses the accumulation of its substrates i.e. aromatic amino acids. Among CADs, highest cichoric acid and chlorogenic acid was found in l-tryptophan (0.5 mM) which was 2.0 and 1.62 times more than the control treatments. We concluded that addition of l-tryptophan (indolic pathway precursor) and not the l-phenylalanine (phenylpropanoid pathway precursor) stimulate the growth and accumulation of secondary metabolites in adventitious root cultures of E. purpurea (L.) Moench.

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

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

Similar content being viewed by others

References

  • Abbasi BH, Tian C, Murch SJ, Saxena PK, Liu C (2007) Light-enhanced caffeic acid derivatives biosynthesis in hairy root cultures of Echinacea purpurea. Plant Cell Rep 26:1367–1372

    Article  CAS  PubMed  Google Scholar 

  • Abbasi BH, Stiles AR, Saxena PK, Liu C-Z (2012) Gibberellic acid increases secondary metabolite production in Echinacea purpurea hairy roots. Appl Biochem Biotechnol 168:2057–2066

    Article  CAS  PubMed  Google Scholar 

  • Akashi T, Ishizaki M, Aoki T, Ayabe S (2005) Isoflavonoid production by adventitious root cultures of Iris germanica (Iridaceae). Plant Biotechnol 22:207–215

    Article  CAS  Google Scholar 

  • Amrhein N, Deus B, Gehrke P, Steinrucken HC (1980) The site of the inhibition of the shikimate pathway by glyphosate II. Interference of glyphosate with chorismate formation in vivo and in vitro. Plant Physiol 66:830–834

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bauer R (1998) Echinacea: biological effects and active principals. Phytomedicines of Europe. In: Lawson LD, Bauer R (eds) Chemistry and biological activity. ACS Symposium Series 691 American Chemical Society, Washington, pp 140–157

  • Cheminat A, Zawatzky R, Becker H, Brouillard R (1988) Caffeoyl conjugates from Echinacea species: structures and biological activity. Phytochemistry 27:2787–2794

    Article  CAS  Google Scholar 

  • Choi O, Wu C-Z, Kang SY, Ahn JS, Uhm T-B, Hong Y-S (2011) Biosynthesis of plant-speciWc phenylpropanoids by construction of an artificial biosynthetic pathway in Escherichia coli. J Ind Microbiol Biotechnol 38:1657–1665

    Article  CAS  PubMed  Google Scholar 

  • Cui L, Wang ZY, Zhou XH (2012) Optimization of elicitors and precursors to enhance valtrate production in adventitious roots of Valeriana amurensis Smir. ex Kom. Plant Cell Tissue Organ Cult 108:411–420

    Article  CAS  Google Scholar 

  • D’Cunha GB, Satyanarayan V, Nair PM (1996) Purification of phenylalanine ammonia-lyase from Rhodotorula glutinis. Phytochemistry 42:17–20

    Article  Google Scholar 

  • Diaz J, Barcelo AR, De Caceres FM (1997) Changes in shikimate dehydrogenase and the end products of the shikimate pathway, chlorogenic acid and lignins, during the early development of seedlings of Capsicum annuum. New Phytol 136:183–188

    Article  CAS  Google Scholar 

  • Ding L, Hofius D, Hajirezaei MR, Fernie AR, Bornke F, Sonnewald U (2007) Functional analysis of the essential bifunctional tobacco enzyme 3-dehydroquinate dehydratase/shikimate dehydrogenase in transgenic tobacco plants. J Exp Bot 58:2053–2067

    Article  CAS  PubMed  Google Scholar 

  • Edhahiro J-I, Nakamura M, Seki M, Furusaki S (2005) Enhanced accumulation of anthocyanin in cultured strawberry cells by repetitive feeding of l-phenylalanine into the medium. J Biosci Bioeng 99:43–47

    Article  Google Scholar 

  • Facino RM, Carini M, Aldini G, Marinello C, Arlandini E, Franzo L, Colombo M, Pietta P, Mauri P (1993) Direct characterization of caffeoyl esters with antihyaluronidase activity in crude extracts from Echinacea angustifolia roots by fast atom bombardment tandem mass spectrometry. Farmaco 48:1447–1456

    CAS  PubMed  Google Scholar 

  • Facino RM, Carini M, Aldini G, Saibene L, Pietta P, Mauri P (1995) Echinacoside and caffeoyl conjugates protect collagen from free radical-induced degradation: a potential use of Echinacea extracts in the prevention of skin photodamage. Planta Med 61:510–514

    Article  CAS  PubMed  Google Scholar 

  • Fett-Neto AG, Melanson SJ, Sakata K, DiCosmo F (1993) Improved growth and taxol yield in developing callus of Taxus cuspidata by medium composition modification. Biotech 11:731–734

    Article  CAS  Google Scholar 

  • Fett-Neto AG, Melanson SJ, Nicholson SA, Pennington JJ, DiCosmo F (1994) Improved taxol yield by aromatic carboxylic and amino acid feeding to cell cultures of Taxus cuspidata. Biotechnol Bioeng 44:967–971

    Article  CAS  PubMed  Google Scholar 

  • Folin O, Ciocalteu V (1927) On tyrosine and tryptophane determination in proteins. J Biol Chem 27:627–650

    Google Scholar 

  • Goers SK, Jensen RA (1984) Separation and characterization of two chorismate-mutase isoenzymes from Nicotiana silvestris. Planta 162:109–116

    Article  CAS  PubMed  Google Scholar 

  • Guyer D, Patton D, Ward E (1995) Evidence for cross-pathway regulation of metabolic gene-expression in plants. Proc Natl Acad Sci USA 92:4997–5000

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Herrmann KM (1995) The shikimate pathway as an entry to aromatic secondary metabolism. Plant Physiol 107:7–12

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ibrahim RK (1987) Regulation of synthesis of phenolics. In: Constabel F, Vasil I (eds) Cell culture and somatic cell genetics of plants. Academic Press, San Diego, vol 4, pp 77–95

  • Johal GS, Rahe JE (1988) Glyphosate, hypersensitivity and phytoalexin accumulation in the incompatible bean anthracnose host-parasite interaction. Physiol Mol Plant Pathol 32:267–281

    Article  CAS  Google Scholar 

  • Karppinen K, Hokkanen J, Tolonen A, Maltila S, Hohtola A (2007) Biosynthesis of hyperforin and adhyperforin from amino acid precursors in shoot cultures of Hypericum perforatum. Phytochemistry 68:1038–1045

    Article  CAS  PubMed  Google Scholar 

  • King PJ, Ma G, Miao W, Jia Q, McDougall BR, Reinecke MG, Cornell C, Kuan J, Kim TR, Robinson WE (1999) Structure– activity relationships: analogues of the dicaffeoylquinic and dicaffeoyltartaric acids as potent inhibitors of human immunodeficiency virus type 1 integrase and replication. J Med Chem 42:497–509

    Article  CAS  PubMed  Google Scholar 

  • Kiong LP, Mahmood M, Fadzillah NM, Daud SK (2005) Effects of precursor supplementation on the production of triterpenes by Centella asiatica callus cultures. Pak J Biol Sci 8:1160–1169

    Article  CAS  Google Scholar 

  • Leonard E, Koffas MA (2007) Engineering of artificial plant cytochrome P450 enzymes for synthesis of isoflavones by Escherichia coli. Appl Environ Microbiol 73:7246–7251

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lin Z, Neamati N, Zhao H, Kiryu Y, Turpin JA, Aberham C, Strebel K, Kohn K, Wityrouw M, Pannecouque C, Debyser Z, De Clercq E, Rice WG, Pommier Y, Burke RT (1999) Cichoric acid analogues as HIV-1 integrase inhibitors. J Med Chem 42:1401–1414

    Article  CAS  PubMed  Google Scholar 

  • Lindsey K, Yeoman MM (1984) The synthetic potential of immobilized cells of Capsicum frutescens Mill. cv. annuum. Planta 162:495–501

    Article  CAS  PubMed  Google Scholar 

  • Liu XN, Zhang XQ, Zhang SX, Sun JS (2007) Regulation of metabolite production by precursors and elicitors in liquid cultures of Hypericum perforatum. Plant Cell Tissue Organ Cult 91:1–7

    Article  CAS  Google Scholar 

  • Liu R, Li W, Sun LY, Liu CZ (2012) Improving root growth and cichoric acid derivatives production in hairy root culture of Echinacea purpurea by ultrasound treatment. Biochem Eng J 60:62–66

    Article  CAS  Google Scholar 

  • Matsukawa T, Ishihara A, Iwamura H (2002) Differential induction of chorismate mutase isoforms by elicitors in oat leaves. Plant Physiol Biochem 40:795–802

    Article  CAS  Google Scholar 

  • McCue KF, Conn EE (1990) Induction of shikimic acid pathway enzymes by light in suspension cultured cells of parsley (Petroselinum crispum). Plant Physiol 94:507–510

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Min JY, Jung HY, Kang SM, Kim YD, Kang YM, Park DJ, Prasad DT, Choi MS (2007) Production of tropane alkaloids by small-scale bubble column bioreactor cultures of Scopolia parviflora adventitious roots. Bioresour Technol 98:1748–1753

    Article  CAS  PubMed  Google Scholar 

  • Morgan JA, Shanks JV (2000) Determination of metabolic rate-limitations by precursor feeding in Catharanthus roseus hairy root cultures. J Biotechnol 79:137–145

    Article  CAS  PubMed  Google Scholar 

  • Mulder-Krieger T, Verpoorte R, Svendse A, Scheffer J (1988) Production of essential oils and flavours in plant cell and tissue cultures: a review. Plant Cell Tissue Organ Cult 13:85–114

    Article  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Murthy HN, Lee EJ, Paek KY (2014) Production of secondary metabolites from cell and organ cultures: strategies and approaches for biomass improvement and metabolite accumulation. Plant Cell Tissue Organ Cult 118:1–16

    Article  CAS  Google Scholar 

  • Paek KY, Murthy HN, Hahn EJ (2009) Establishment of adventitious root cultures of Echinacea purpurea for the production of caffeic acid derivatives. Methods Mol Biol 547:3–16

    Article  CAS  PubMed  Google Scholar 

  • Palacio L, Cantero JJ, Cusido R, Goleniowski M (2011) Phenolic compound production by Larrea divaricata Cav. plant cell cultures and effect of precursor feeding. Process Biochem 46:418–422

    Article  Google Scholar 

  • Pellati F, Benvenuti S, Magro L, Melegari M, Soragni F (2004) Analysis of phenolic compounds and radical scavenging activity of Echinacea spp. J Pharm Biomed Anal 35:289–301

    Article  CAS  PubMed  Google Scholar 

  • Perassolo M, Quevedo CV, Giuletti AM, Talou JR (2011) Stimulation of the proline cycle and anthraquinone accumulation in Rubia tinctorum cell suspension cultures in the presence of glutamate and two proline analogs. Plant Cell Tissue Organ Cult 106:153–159

    Article  CAS  Google Scholar 

  • Pinto JEBP, Dyer WE, Weller SC, Herrmann KM (1988) Glyphosate induces 3-Deoxy-D-arabino-heptulosonate 7pPhosphate synthase in potato (Solanum tuberosum L.) cells grown in suspension culture. Plant Physiol 87:891–893

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sabra A, Adam L, Daayf F, Renault S (2012) Salinity-induced changes in caffeic acid derivatives, alkamides and ketones in three Echinacea species. Environ Exp Bot 77:234–241

    Article  CAS  Google Scholar 

  • Sakanaka S, Tachibana Y, Okada Y (2005) Preparation and antioxidant properties of extracts of Japanese persimmon leaf tea (kakinoha-cha). Food Chem 89:569–575

    Article  CAS  Google Scholar 

  • Sharon A, Amsellem Z, Gressel J (1992) Glyphosate suppression of an elicited defense response. Plant Physiol 98:654–659

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Singh BK, Lonergan SG, Conn EE (1986) Chorismate mutase isoenzymes from selected plants and their immunological comparison with the isoenzymes from Sorghum bicolor. Plant Physiol 81:717–722

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vats S, Kamal R (2014) Cassia occidentalis L. (a new source of rotenoids): its in vitro regulation by feeding precursors and larvicidal efficacy. Plant Cell Tissue Organ Cult 116:403–409

    Article  CAS  Google Scholar 

  • Wielanek M, Urbanek H (2006) Enhanced glucotropaeolin production in hairy root cultures of Tropaeolum majus L. by combining elicitation and precursor feeding. Plant Cell Tissue Organ Cult 86:177–186

    Article  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 of Echinacea angustifolia. J Plant Biol 49:193–199

    Article  CAS  Google Scholar 

  • Wu CH, Murthy HN, Hahn EJ, Paek KY (2007) Large-scale cultivation of adventitious roots of Echinacea purpurea in air-lift bioreactors for the production of chichoric acid, chlorogenic acid and caftaric acid. Biotechnol Lett 29:1179–1182

    Article  CAS  PubMed  Google Scholar 

  • Xu CG, Tang TX, Chen R, Liang CH, Liu XY, Wu CL, Yang Y-S, Yang D-P, Wu H (2014) A comparative study of bioactive secondary metabolite production in diploid and tetraploid Echinacea purpurea (L.) Moench. Plant Cell Tissue Organ Cult 116:323–332

    Article  CAS  Google Scholar 

  • Zenk MH (1991) Chasing the enzymes of secondary metabolism: plant cultures as a pot of gold. Phytochemistry 30:3861–3863

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work is financially supported by the Ministry of Education and Human Resources Development (MOE), the Ministry of Commerce, Industry and Energy (MOCIE) and the Ministry of Labor (MOLAB) through the fostering project of the Lab. of Excellency, Korea.

Author information

Authors and Affiliations

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

    Mohammad Mobin, Chun-Hua Wu, Rajesh Kumar Tewari & Kee-Yoeup Paek

  2. Department of Biology, Faculty of Science, University of Tabuk, Tabuk, 71491, Saudi Arabia

    Mohammad Mobin

  3. Department of Terrestrial Ecosystem Research, University of Vienna, Vienna, Austria

    Rajesh Kumar Tewari

Authors
  1. Mohammad Mobin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chun-Hua Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rajesh Kumar Tewari
    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 author

Correspondence to Mohammad Mobin.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mobin, M., Wu, CH., Tewari, R.K. et al. Studies on the glyphosate-induced amino acid starvation and addition of precursors on caffeic acid accumulation and profiles in adventitious roots of Echinacea purpurea (L.) Moench. Plant Cell Tiss Organ Cult 120, 291–301 (2015). https://doi.org/10.1007/s11240-014-0606-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-014-0606-1

Keywords

Search

Navigation