Skip to main content

Advertisement

SpringerLink
Log in

Partial alleviation of zinc induced oxidative stress by polyamines in Plantago ovata Forsk

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

Abstract

Zinc causes toxicity to the plants in an excess concentration and it is manifested by chlorosis, rolling of leaf margins, and disruption of membrane integrity. The heavy metal stress also triggers the stimulation of enzymatic and non-enzymatic antioxidant systems. Polyamines are naturally occurring, secondary metabolites, protecting plants from heavy metal-induced stress. Plants also up-regulate the mRNA expression of Metallothionein in response to heavy metal-induced oxidative stress. The alteration in Metallothionein type 2 (PoMT2) expression of a medicinally important herb Plantago ovata in presence of polyamines like Putrescine, Spermidine, and Spermine in addition to ZnSO4·H2O by the semi-quantitative and the quantitative methods have been demonstrated in the present study. We have observed reductions in the expression of the Metallothionein type 2 gene in the presence of the aforementioned polyamines which implies their protective and antioxidant properties to fight against the zinc induced stress. 1 mM Put has been more efficient in increasing the total chlorophyll content (compared to 2 mM Put) by about 36% each in 1000 µM ZnSO4 treated P. ovata seedlings. Spermidine also enhanced chlorophyll content. However, 2 mM Put and 0.5 mM Spm have shown better efficiency in increasing the total antioxidant and DPPH radical scavenging activities. The lipid peroxidation has been found to decrease in Put and Spm supplemented samples by up to about 47% in both cases. Significant reductions in lipid peroxidation and down-regulation of PoMT2 gene expression indicate the roles of polyamines in partially alleviating Zn-induced oxidative damage.

Key message

In this study we have demonstrated the alleviation of zinc-induced stress in Plantago ovata with the exogenous addition of polyamine and the effect of polyamine addition on the relative expression of Metallothionein type 2 in P. ovata.

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

  • Brand-Williams W, Cuvelier ME, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. Leb Wiss Technol 28:25–30

    Article  CAS  Google Scholar 

  • Brolis M, Gabetta B, Fuzzati N, Pace R, Panzeri F, Peterlongo F (1998) Identification by high performance liquid chromatography–diode array detection–mass spectrometry and quantification by high performance liquid chromatography–UV absorbance detection of active constituents of Hypericum perforatum. J Chromatogr 825:9–16

    Article  CAS  Google Scholar 

  • Calzadilla PI, Gazquez A, Maiale SJ, Ruiz OA, Bernardia MA (2014) Polyamines as indicators and modulators in the abiotic stress in plants., In: Anjum NA, Gill SS, Gill R (eds) Plant adaptation to environmental change: significance of amino acids and their derivatives. CAB International, Wallingford, UK, pp 109–128

    Chapter  Google Scholar 

  • Chen D, Shao Q, Yin L, Younis A, Zheng B (2019) Polyamine function in plants: Metabolism, regulation on development, and roles in abiotic stress responses, Front Plant Sci, 9: 1945, doi: https://doi.org/10.3389/fpls.2018.01945

  • Choudhary SP, Oral HV, Bhardwaj R, Yu JQ, Tran LSP (2012) Interaction of brassinosteroids and polyamines enhances copper stress tolerance in Raphanus sativus. J Exp Bot 63(15):5659–5675

    Article  CAS  Google Scholar 

  • Cicatelli A, Lingua G, Todeschini V, Biondi S, Torregiani P, Castiglione S (2010) Arbuscular mycorrhizal fungi restore normal growth in a white poplar clone grown on heavy metal-contaminated soil, and this is associated with upregulation of foliar metallothionein and polyamine biosynthetic gene expression. Ann Bot 106:791–802

    Article  CAS  Google Scholar 

  • Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Ann Rev Plant Biol 53:159–182

    Article  CAS  Google Scholar 

  • Das K, Adak MK (2015) Polyamine mediated anti-oxidation activity facilitates of Marsilea minuta L. under Cd toxicity. Plant Gene Trait 6(8):1–13

    Google Scholar 

  • Dutta S, Roy A, Pramanick P, Dey S, Raychaudhuri SS (2021) Studies on variation of phytochelatin 2 content and Metallothionein 2 gene expression in presence of cadmium stress in Plantago ovata forsk. Afr J Biol Sci 3(4):42–49. https://doi.org/10.33472/AFJBS.3.4.2021.42-49

    Article  CAS  Google Scholar 

  • Feigl G, Lehotai N, Molnar A, Ordog A, Rodriguez- Ruiz M, Palma Jose M, Corpus Francisco J, Erdei L, Kolbert Z (2015) Zinc induces distinct changes in the metabolism of reactive oxygen and nitrogen species (ROS and RNS) in the roots of two Brassica species with different sensitivity to zinc stress. Ann Bot 116:613–625

    Article  CAS  Google Scholar 

  • Ghoshal N, Talapatra S, Moulick A, Chakraborty A, Raychaudhuri SS (2013) Alterations in transcriptome and proteome on metallothioneins following oxidative stress induced by sub lethal doses of cadmium and gamma rays in Plantago ovata. Int J Radiat Biol 89(7):571–582

    Article  CAS  Google Scholar 

  • Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34:34–45

    Article  Google Scholar 

  • Groppa MD, Tomaro ML, Benavides MP (2001) Polyamines as protectors against cadmium or copper-induced oxidative damage in sunflower leaf discs. Plant Sci 161:481–488

    Article  CAS  Google Scholar 

  • Groppa MD, Tomaro ML, Benavides MD (2007) Polyamines and heavy metal stress: the antioxidant behavior of spermine in cadmium- and copper-treated wheat leaves. BioMetals 20:185–195

    Article  CAS  Google Scholar 

  • Hasanuzzaman M, Haifa ASA, Parvin K, Borhanuddin Bhuyan MHM, Tanveer M, Mohsin SM, Nahar K, Soliman MH, Mahmud JA, Fujita M (2019) Polyamine action under metal/ metalloid stress: regulation of biosynthesis, metabolism and molecular interactions. Int J Mol Sci 20:3215. https://doi.org/10.3390/ijms20133215

    Article  CAS  PubMed Central  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  Google Scholar 

  • Howladar SM, Al-Robai SA, Al-Zahrani FS, Howladar MM, Aldhebiani AY (2018) Silicon and its application method effects on modulation of cadmium stress responses in Triticum aestivum (L.) through improving the antioxidative defense system and polyamine gene expression. Ecotox Environ Safe 159:143–152

    Article  CAS  Google Scholar 

  • Imai A, Matsuyama T, Hanzawa Y, Akiyama T, Tamaoki M, Saji H, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Komeda Y, Takahashi T (2004) Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiol 135:1565–1573

    Article  CAS  Google Scholar 

  • Kumar P, Gogia N, Tiwari B (2014) Plants defensive response against cadmium toxicity stress: a review. J Kalash Sci 2(1):75–82

    Google Scholar 

  • Li Z, Zhang Y, Zhang X, Peng Y, Merewitz E, Ma X, Huang L, Yan Y (2016) The alterations of endogenous polyamines and phytohormones induced by exogenous application of spermidine regulate antioxidant metabolism, metallothionein and relevant genes conferring drought tolerance in white clover. Environ Exp Bot 124:22–38

    Article  CAS  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Liu JH, Wang W, Wu H, Gong X, Moriguchi T (2015) Polyamines function in stress tolerance: from synthesis to regulation. Front Plant Sci 6:827. doi: https://doi.org/10.3389/fpls.2015.00827

    Article  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 method _∆∆CT. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Lomozik L, Wojciechowska A (1989) Complexation of putrescine with copper (II), zinc (II), lead (II) and magnesium (II) in aqueous solution. Polyhedron 8(22):2645–2648

    Article  CAS  Google Scholar 

  • Lovaas E (1997) Antioxidant and metal—chelating effects of polyamines. Adv Pharmacol 38:119–149

    Article  CAS  Google Scholar 

  • Mandal C, Ghosh N, Adak MK, Dey N (2013) Interaction of polyamine on oxidative stress induced by exogenously applied hydrogen peroxide in Salvinia natans Linn. Theor Exp Plant Phys 25(3):203–212

    Article  Google Scholar 

  • Marco F, Alcazar R, Altabella T, Carrasco P, Gill SS, Tuteja N, Tiburcio AF (2012) Polyamines in developing stress-resistant crops, Improving crop resistance to abiotic stress, first. Wiley, Hoboken, pp 625–635. https://doi.org/10.1002/9783527632930.ch27

    Book  Google Scholar 

  • Morkunas I, Wozniak A, Mai VC, Rucinka- Sobkowiak R, Jeandat P (2018) The role of heavy metals in plant response to biotic stress. Molecules 23:2320. doi: https://doi.org/10.3390/molecules23092320

    Article  CAS  PubMed Central  Google Scholar 

  • Moulick A, Mukhopadhyay D, Talapatra S, Ghoshal N, Sen Raychaudhuri S (2013) Molecular cloning, modeling, and characterization of type 2 metallothionein from Plantago ovata Forsk. Sequencing

  • Pál M, Szalai G, Janda T (2015) Polyamines are important in abiotic stress signaling. Plant Sci 237:16–23

    Article  Google Scholar 

  • Pramanick P, Chakraborty A, Raychaudhuri SS (2017) Phenotypic and biochemical alterations in relation to MT2 gene expression in Plantago ovata Forsk under zinc stress. Biometals 30(2):171–184

    Article  CAS  Google Scholar 

  • Prieto P, Pineda M, Aguilar M (1999) Spectrophotometric quantitation of antioxidant capacity through the formation of a Phosphomolybdenum complex: specific application to the determination of vitamin E. Anal Biochem 269:337–341

    Article  CAS  Google Scholar 

  • Rouphael Y, Colla G, Bernardo L, Kane D, Trevisan M, Lucini L (2016) Zinc excess triggered polyamines accumulation in lettuce root metabolome, as compared to osmotic stress under high salinity. Front Plant Sci 7:842. https://doi.org/10.3389/fpls.2016.00842

    Article  PubMed  PubMed Central  Google Scholar 

  • Ruttkay-Nedecky B, Nejdl L, Gumulec J, Zitka O, Masarik M, Eckschlager T, Stiborova M, Adam V, Kizek R (2013) The role of metallothionein in oxidative stress. Int J Mol Sci 14:6044–6066

    Article  CAS  Google Scholar 

  • Sengupta M, Chakraborty A, Raychaudhuri SS (2013) Ionizing radiation induced changes in phenotype, photosynthetic pigments and free polyamine levels in Vigna radiata (L.) Wilczek. Appl Radiat Isot 75:44–49

    Article  CAS  Google Scholar 

  • Sengupta M, Raychaudhuri SS (2017) Partial alleviation of oxidative stress induced by gamma irradiation in Vigna radiata by polyamine treatment. Int J Radiat Biol 93(8):803–817

    Article  CAS  Google Scholar 

  • Sestak Z, Catsky J, Jarvis PG (1971) Plant photosynthetic production: manual of methods. The Hague, Dr. W Junk

    Google Scholar 

  • Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2016) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Life Sci 6:1143. https://doi.org/10.3389/fpls.2015.01143

    Article  Google Scholar 

  • Soudek P, Ursu M, Petrova S, Vanek T (2016) Improving crop tolerance to heavy metal stress by polyamine application. Food Chem 213:223–229

    Article  CAS  Google Scholar 

  • Sunitha MSL, Prashant S, Anil Kumar S, Rao S, Narasu ML, Kavi Kishor PB (2014) Cellular and molecular mechanisms of heavy metal tolerance in plants: a brief overview of transgenic plants overexpressing phytochelatin synthase and metallothionein genes. Plant Cell Biotechnol Mol Biol 14(1):33–48

    Google Scholar 

  • Takahashi T, Kakehi JI (2010) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 105:1–6

    Article  CAS  Google Scholar 

  • Wang X, Shi G, Xu Q (2003) Toxic effects of Cr6+ on Nymphoides peltatum mitigated by exogenous polyamine. Acta Sci Circumst 23:689–693. doi: https://doi.org/10.3321/j.issn:0253-2468.2003.05.024

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to express their sincere gratitude to the UGC- DAE Consortium for Scientific Research, Kolkata Centre, West Bengal, India (UGC- DAECSR- KC/CRS/13/RB- 01/0808) for financial support.

Author information

Authors and Affiliations

  1. Department of Biophysics, Molecular Biology and Bioinformatics, University of Calcutta, 92, Acharya Prafulla Chandra Road, Kolkata, West Bengal, 700009, India

    Paulami Pramanick & Sarmistha Sen Raychaudhuri

  2. UGC- DAE Consortium for Scientific Research, Kolkata Centre, LB- 8, Sector- III, Bidhan Nagar, Kolkata, West Bengal, 700098, India

    Anindita Chakraborty

Authors
  1. Paulami Pramanick
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anindita Chakraborty
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sarmistha Sen Raychaudhuri
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SSRC designed and supervised the research work. PP and SSRC conducted the experiments. AC helped with writing the manuscript. PP and SSRC analyzed the data and wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Sarmistha Sen Raychaudhuri.

Ethics declarations

Conflict of interest

There are no conflicts of interest.

Additional information

Communicated by Heidi Halbwirth.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 372 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pramanick, P., Chakraborty, A. & Raychaudhuri, S.S. Partial alleviation of zinc induced oxidative stress by polyamines in Plantago ovata Forsk. Plant Cell Tiss Organ Cult 148, 573–583 (2022). https://doi.org/10.1007/s11240-021-02209-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-021-02209-w

Keywords

Search

Navigation