Log in

Copper-Induced Modulation of Biomass Growth, Physiological Parameters, Bioactive Centellosides, and Expression of Biosynthetic Pathway Genes in an Important Medicinal Herb, Centella asiatica

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Hydroponically established Centella asiatica plants were studied under different concentrations of copper (0, 0.32,1.6, and 3.2 µM) for their morphological, physiological, and biochemical characteristics. The plants grown in the medium without any exogenous supply of copper showed improved biomass accumulation with maximum fresh weight (FW = 24.7 g plant−1) and dry weight (DW = 2.35 g plant−1). The total chlorophyll content, leaf number, and the leaf area were higher (0.27 mg g−1 DW, 20 and 100.54 cm2) in the plants grown under copper-deficient conditions. The toxic effects of increased levels of copper were evident by significant inhibition in growth and other morphological parameters. Copper treatment showed an increase in malondialdehyde (MDA) content and SOD activity. Bioactive phytochemical profiling using HPLC analysis revealed that higher levels of copper (1.6 and 3.2 µM) inhibit the accumulation of total centelloside content. The differential accumulation of centelloside content was further validated by the consistent pattern of expression of key pathway genes related to centelloside production in copper-treated C. asiatica plants. The study unveiled some of the important facts associated with the mechanism of copper tolerance in this important medicinal herb C. asiatica. The findings of the present study can be further used to provide better production of high value, in demand centellosides.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abdel-Ghany SE, Pilon M (2008) Micro RNA-mediated systemic down regulation of copper protein expression in response to low copper availability in Arabidopsis. J Biol Chem 283:15932–15945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Agarwala SC, Sharma CP (1961) The standardization of sand culture technique for the study of macro and micro (trace) element deficiencies under Indian conditions. Curr Sci 11:427

    Google Scholar 

  • Alaoui-Soss´e B, Genet P, Vinit-Dunand F, Toussaint ML, Epron D, Badot PM (2004) Effect of copper on growth in cucumber plants (Cucumissativus) and its relationships with carbohydrate accumulation and changes in ion contents. Plant Sci 166:1213–1218

    Article  Google Scholar 

  • Ali MB, Hahn EJ, Paek KY (2006) 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 

  • Arnon DJ (1949) Copper enzymes in isolated chloroplasts polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Augustin JM, Kuzina V, Andersen SB, Bak S (2011) Molecular activities, biosynthesis and evolution of triterpenoid saponins. Phytochemistry 72:435–457

    Article  CAS  PubMed  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  PubMed  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 Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • De Vos CHR, Schat H, Vooijs R, Ernst WHO (1989) Copper-induced damage to the permeability barrier in roots of Silenecuiubalus. J Plant Physiol 135:164–179

    Article  Google Scholar 

  • Emamverdian A, Ding Y, Mokhberdoran F, **e Y (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World J. doi:10.1155/2015/756120

    Google Scholar 

  • Fendt SM, Buescher JM, Rudroff F, Picotti P, Zamboni N, Sauer U (2010) Tradeoff between enzyme and metabolite efficiency maintains metabolic homeostasis upon perturbations in enzyme capacity. Mol Syst Biol 6:356

    PubMed  PubMed Central  Google Scholar 

  • Fernandes JC, Henriques FS (1991) Biochemical, physiological and structural effects of excess copper in plants. Bot Rev 57:246–273

    Article  Google Scholar 

  • Gohil KJ, Patil JA, Gajjar AK (2010) Pharmacological review on Centella asiatica: a potential herbal cure-all. Ind J Pharm Sci 72:546–556

    Article  Google Scholar 

  • Hodenberg A, Fink A (1975) Ermittlung von Toxizitats-Grenzwerten fur Zink, Kupfer und Blei in Hafer und Rotklee. Z PlanzenernahrBodenk 138:489–503

    Google Scholar 

  • Hogland DR, Arnon DI (1938) The water culture method for growing plants without soil. Circ Calif Agric Exp Stat 347:1–15

    Google Scholar 

  • Ivanov YV, Kartashov AV, Ivanova AI, Savochkin YV, Kuznetsov VV (2016) Effects of copper deficiency and copper toxicity on organogenesis and some physiological and biochemical responses of Scots pine (Pinus sylvestris L.) seedlings grown in hydroculture. Environ Sci Pollut Res. doi:10.1007/s11356-016-6929-1

    Google Scholar 

  • James J, Dubery I (2009) Pentacyclic triterpenoids from the medicinal herb Centella asiatica (L.) Urban. Molecules 14:3922–3941

    Article  CAS  PubMed  Google Scholar 

  • Keunen E, Truyens S, Bruckers L, Remans T, Vangronsveld J, Cuypers A (2011) Survival of Cd-exposed Arabidopsis thaliana: are these plants reproductively challenged? Plant Physiol Biochem 49:1084–1091

    Article  CAS  PubMed  Google Scholar 

  • Kim OT, Kim MY, Hong MH, Ahn JC, Hwang B (2004) Stimulation of asiaticoside accumulation in the whole plant cultures of Centella asiatica (L.) Urban by elicitors. Plant Cell Rep 23:339–344

    Article  CAS  PubMed  Google Scholar 

  • Kupper H, Andresen E (2016) Mechanisms of metal toxicity in plants. Metallomics 8:269–285

    Article  PubMed  Google Scholar 

  • Kwon TW, Menzel DB, Olcott HS (1965) Reactivity of malondialdehyde with food constituents. J Food Sci 30:808–813

    Article  CAS  Google Scholar 

  • Lequeux H, Hermans C, Lutts S, Verbruggen N (2010) Response to copper excess in Arabidopsis thaliana: Impact on the root system architecture, hormone distribution, lignin accumulation and mineral profile. Plant Physiol Biochem 48:673–682

    Article  CAS  PubMed  Google Scholar 

  • Mangas S, Moyano E, Osuna L, Cusido RM, Bonfill M, Palazon J (2008) Triterpenoid saponin content and the expression level of some related genes in calli of Centella asiatica. Biotechnol Lett 30:1853–1859

    Article  CAS  PubMed  Google Scholar 

  • Mantovi P, Bonazzi G, Maestri E, Marmiroli N (2003) Accumulation of copper and zinc from liquid manure in agricultural soils and crop plants. Plant Soil 250:249–257

    Article  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, vol II. Academic Press, London, pp 337–347

    Google Scholar 

  • Meng Q, Zou J, Zou J, Jiang W, Liu D (2007) Effect of Cu2+ concentration on growth, antioxidant activitity and malondialdehyde content in garlic (Allium sativum). Acta Biol Cracov Ser Bot 49:95–101

    Google Scholar 

  • Mithofer A, Schulze B, Boland W (2004) Biotic and heavy metal stress response in plants: evidence for common signals. FEBS Lett 566:1–5

    Article  CAS  PubMed  Google Scholar 

  • Mourato MP, Martins LL, Campos-Andrada MP (2009) Physiological responses of Lupinus luteus to different copper concentrations. Biol Plant 53:105–111

    Article  CAS  Google Scholar 

  • Prasad A, Pragadheesh VS, Mathur A, Srivastava NK, Singh M, Mathur AK (2012) Growth and centelloside production in hydroponically established medicinal plant-Centella asiatica (L). Ind Crops Prod 35:309–312

    Article  CAS  Google Scholar 

  • Rahman MM, Chongling Y, Rahman MDM, Islam KS (2012) Effects of copper on growth, accumulation, antioxidant activity and malondialdehyde content in young seedlings of the mangrove species Kandelia candel (L.). Plant Biosyst 146:47–57

    Article  Google Scholar 

  • Robson AD, Reuter DJ (1981) Diagnosis of copper deficiency and toxicity. In: Loneragan JF, Robson AD, Graham RD (eds) Copper in soils and plants. Academic Press, London, pp 287–312

    Google Scholar 

  • Roy DC, Barman SK, Shaik MM (2013) Current updates on Centella asiatica: phytochemistry, pharmacology and traditional uses. Med Plant Res 3:20–36

    Google Scholar 

  • Satheesan J, Narayanan AK, Sakunthala M (2012) Induction of root colonization by Piriformospora indica leads to enhanced asiaticoside production in Centella asiatica. Mycorrhiza 22:195–202

    Article  CAS  PubMed  Google Scholar 

  • Shahid M, Pourrut B, Dumat C, Nadeem M, Aslam M, Pinelli E (2014) Heavy-metal-induced reactive oxygen species: phytotoxicity and physicochemical changes in plants. In: Whitacre DM (ed) Review of environmental contamination and toxicology, Vol 232. Springer, Cham, pp 1-44

    Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 26. doi:10.1155/2012/217037

  • Shaw AK, Ghosh S (2014) Nano-CuO stress induced modulation of antioxidative defense and photosynthetic performance of Syrian barley (Hordeum vulgare L.). Env Exp Bot 102:37–47

    Article  CAS  Google Scholar 

  • Slooten L, Carpiau K, Van CW, Van MM, Sybesma C, Jnze D (1995) Factors affecting the enhancement of oxidative stress tolerance in transgenic tobacco overexpressing manganese superoxide dismutase in the chloroplasts. Plant Physiol 107:737–750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song WY, Yang HCH, Shao HB, Zheng AZ, Brestic M (2014) The alleviative effects of salicylic acid on the activities of catalase and superoxide dismutase in malting barley (Hordeum uhulgare L.) seedling leaves stressed by heavy metals. Clean—Soil Air Water 42:88–97

    Article  CAS  Google Scholar 

  • Štolfa I, Pfeiffer TŽ, Špoljarić D, Teklić T, Lončarić Z (2015) Heavy metal-induced oxidative stress in plants: response of the antioxidative system. In: Gupta DK et al (eds) Reactive oxygen species and oxidative damage in plants under stress. Springer, Cham, pp 127–163

    Google Scholar 

  • Sytar O, Kumar A, Latowski D, Kuczynska P, Strzałka K, Prasad MNV (2013) Heavy metal-induced oxidative damage, defence reactions, and detoxification mechanisms in plants. Acta Physiol Plant 35:985–999

    Article  CAS  Google Scholar 

  • Sytar O, Brestic M, Taran N, Zivcak M (2016) Plants used for biomonitoring and phytoremediation of trace elements in soil and water. In: Ahmad P (ed) Plant metal interaction: emerging remediation techniques. Elsevier, Amsterdam, pp 361–384

    Chapter  Google Scholar 

  • Tang B, Zhu B, Liang Y, Bi L, Hu Z, Chen B, Zhang K, Zhu J (2011) Asiaticoside suppresses collagen expression and TGF-b/Smad signaling through inducing Smad7 and inhibiting TGF-bRI and TGF-bRII in keloid fibroblasts. Arch Dermatol Res 303:563–572

    Article  CAS  PubMed  Google Scholar 

  • Tanyolac D, Ekmekci Y, Unalan S (2007) Changes in photochemical and antioxidant enzyme activities in maize (Zea mays L.) leaves exposed to excess copper. Chemosphere 67:89–98

    Article  CAS  PubMed  Google Scholar 

  • Thomas G, Stärk HJ, Wellenreuther G, Dickinson BC, Küpper H (2013) Effects of nanoMar copper on water plants—Comparison of biochemical and biophysical mechanisms of deficiency and sublethal toxicity under environmentally relevant conditions. Aquat Toxicol 140:27–36

    Article  PubMed  Google Scholar 

  • Verma K, Shekhawat GS, Sharma A, Mehta SK, Sharma V (2008) Cadmium induced oxidative stress and changes in soluble and ionically bound cell wall peroxidase activities in roots of seedling and 3–4 leaf stage plants of Brassica juncea (L.) czern. Plant Cell Rep 27:1261–1269

    Article  CAS  PubMed  Google Scholar 

  • **ong ZT, Liu C, Geng B (2006) Phytotoxic effects of copper on nitrogen metabolism and plant growth in Brassica pekinensis Rupr. Ecotoxicol Environ Saf 64:273–280

    Article  CAS  PubMed  Google Scholar 

  • Yendo ACA, Costa F, Gosmann G, Fett-Neto AG (2010) Production of plant bioactive triterpenoid saponins: elicitation strategies and target genes to improve yields. M Biotechnol 46:94–104

    Article  CAS  Google Scholar 

  • Yruela I (2009) Copper in plants: acquisition, transport and interactions. Funct Plant Biol 36:409–430

    Article  CAS  Google Scholar 

  • Zelezniak A, Sheridan S, Patil KR (2014) Contribution of network connectivity in determining the relationship between gene expression and metabolite concentration changes. PLOS Comput Biol 10:e1003572

    Article  PubMed  PubMed Central  Google Scholar 

  • Zengin FK, Kirbag S (2007) Effects of copper on chlorophyll, proline, protein and abscisic acid level of sunflower (Helianthus annuus L.) seedlings. J Environ Biol 28:561–566

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Director CSIR-CIMAP, Lucknow for providing facilities to execute the work. A part of this work was carried out under a sponsored project Grant No. SR/SO/Ps-28/07 of Department of Science & Technology (DST), New Delhi, India to AM. The first author (AP) thanks Council of Scientific & IndustrialResearch, New Delhi for the award of Senior Research Fellowship during this investigation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Archana Mathur.

Ethics declarations

Conflict of interest

The author declares that there are no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Prasad, A., Kumari, M., Srivastava, N.K. et al. Copper-Induced Modulation of Biomass Growth, Physiological Parameters, Bioactive Centellosides, and Expression of Biosynthetic Pathway Genes in an Important Medicinal Herb, Centella asiatica . J Plant Growth Regul 37, 471–480 (2018). https://doi.org/10.1007/s00344-017-9745-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-017-9745-z

Keywords

Navigation