Skip to main content

Evaluation of antioxidant bioindicators and growth responses in Malva parviflora L. exposed to cadmium

Physiology and Molecular Biology of Plants volume 24, pages 1005–1016 (2018)Cite this article

Abstract

In this study, the effect of cadmium (Cd) uptake and concentration on some growth and biochemical responses were investigated in Malva parviflora under Cd treatments including 0, 10, 50 and 100 µM. The shoots and roots were able to accumulate Cd. However, increased Cd dose led to a considerable Cd content in the roots. Cd stress decreased growth, increased lipid peroxidation and also enhanced proline and ascorbic acid contents in both shoots and roots. Chlorophyll and carotenoid contents decreased in the plants with the increasing Cd concentration. While the activities of catalase (CAT) and superoxide dismutase (SOD) increased in the shoots under different Cd doses, these activities decreased in the roots as compared to the control. Both shoots and roots demonstrated a significant increase in guaiacol peroxidase activity in response to Cd stress. Contrary to the aboveground parts, the roots subjected to Cd doses showed a rise in protein content. Despite higher Cd content in the roots, it seems that CAT and SOD do not play a key role in detoxification of Cd-induced oxidative stress. These findings confirm that reduced biomass and growth under Cd stress can be due to an increase in oxidative stress and a decrease in photosynthetic pigment content. The present study clearly indicates that the shoots and roots exploit different tolerance behaviors to alleviate Cd-induced oxidative stress in M. parviflora.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Abbreviations

AsA:

Ascorbate

CAT:

Catalase

DHA:

Dehydroascorbate

DW:

Dry weight

FW:

Fresh weight

GPX:

Guaiacol peroxidase

H2O2 :

Hydrogen peroxide

TBARS:

Thiobarbituric acid reactive substances

POX:

Peroxidase

PSB:

Potassium phosphate buffer

ROS:

Reactive oxygen species

O2 ˙ − :

Superoxide anion

SOD:

Superoxide dismutase

References

  • Abdel Latef AA (2013) Growth and some physiological activities of pepper (Capsicum annuum L.) in response to cadmium stress and mycorrhizal symbiosis. J Agric Sci Technol 15:1437–1448

    CAS  Google Scholar 

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    CAS  Article  Google Scholar 

  • Baker AJM, Reeves RD, Hajar ASM (1994) Heavy metal accumulation and tolerance in British populations of the metallophyte Thlaspi caerulescens J & C Presl (Brassicaceae). New Phytol 127:61–68

    CAS  Article  Google Scholar 

  • Bates S (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Boonyapookana B, Upatham ES, Kruatrachue M, Pokethitiyook P, Singhakaew S (2002) Phytoaccumulation and phytotoxicity of cadmium and chromium in duckweed Wolffia globosa. Int J Phytoremediation 4:87–100

    CAS  Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  Article  Google Scholar 

  • Chen F, Wang F, Sun H, Cai Y, Mao W, Zhang G, Vincze E, Wu F (2010) Genotype-dependent effect of exogenous nitric oxide on Cd-induced changes in antioxidative metabolism, ultrastructure, and photosynthetic performance in barley seedlings (Hordeum vulgare). J Plant Growth Regul 29:394–408

    CAS  Article  Google Scholar 

  • Deng Y, Li D, Huang Y, Huang S (2017) Physiological response to cadmium stress in kenaf (Hibiscus cannabinus L.) seedlings. Ind Crops Prod 107:453–457

    CAS  Article  Google Scholar 

  • Dinakar N, Nagajyothi PC, Suresh S, Udaykiran Y, Damodharam T (2008) Phytotoxicity of cadmium on protein, proline and antioxidant enzyme activities in growing Arachis hypogaea L. seedlings. J Environ Sci 20:199–206

    CAS  Article  Google Scholar 

  • Dong Y, Chen W, Xu L, Kong J, Liu S (2016) Nitric oxide can induce tolerance to oxidative stress of peanut seedling under cadmium toxicity. Plant Growth Regul 79:19–28

    CAS  Article  Google Scholar 

  • Gasparetto JC, Martins CAF, Hayashi SS, Otuky MF, Pontarolo R (2011) Ethnobotanical and scientific aspects of Malva sylvestris L.: a millennial herbal medicine. J Pharm Pharmacol 64(2):172–189

    Article  Google Scholar 

  • Gill SS, Khan NA, Tuteja N (2012) Cadmium at high dose perturbs growth, photosynthesis and nitrogen metabolism while at low dose it up regulates sulfur assimilation and antioxidant machinery in garden cress (Lepidium sativum L.). Plant Sci 182:112–120

    CAS  Article  Google Scholar 

  • Gopal R, Nautiyal N (2011) Phytotoxic effects of cadmium exposure and metal accumulation in sunflower. J Plant Nutr 34:1616–1624

    CAS  Article  Google Scholar 

  • Hattab S, Boutheina D, Chouba L, Kheder MB, Bousetta H (2009) Photosynthesis and growth responses of pea Pisum sativum L. under heavy metals stress. J Environ Sci 21:1552–1556

    CAS  Article  Google Scholar 

  • He JL, Qin JJ, Long LY, Ma YL, Li H, Li K, Jiang XN, Liu TX, Polle A, Liang ZS, Luo ZB (2011) Net cadmium flux and accumulation reveal tissue-specific oxidative stress and detoxification in Populus × canescens. Physiol Plant 143:50–63

    CAS  Article  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts 1. Kinetics and stoichiometry of fatty acid peroxidatoin. Arch Biochem Biophys 125:189–198

    CAS  Article  Google Scholar 

  • Hemeda HM, Klein BP (1990) Effects of naturally occurring antioxidants on peroxidase activity of vegetable extracts. J Food Sci 55:184–185

    CAS  Article  Google Scholar 

  • Hossain MA, Piyatida P, de Silva JAT, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot 2012:1–37

    Article  Google Scholar 

  • Irfan M, Ahmad A, Hayat S (2014) Effect of cadmium on the growth and antioxidant enzymes in two varieties of Brassica juncea. Saudi J Biol Sci 21:125–131

    CAS  Article  Google Scholar 

  • Jouili H, Bouazizi H, El Ferjani E (2011) Plant peroxidases: biomarkers of metallicstress. Acta Physiol Plant 33:2075–2082

    CAS  Article  Google Scholar 

  • Kovács B, Gŷori Z, Prokisch J, Loch J, Dániel P (1996) A study of plant sample preparation and inductively coupled plasma emission spectrometry parameters. Commun Soil Sci Plant Anal 27:1177–1198

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Marzban L, Akhzari D, Ariapour A, Mohammadparast B, Pessarakli M (2017) Effects of cadmium stress on seedlings of various rangeland plant species (Avena fatua L., Lathyrus sativus L. and Lolium temulentum L.): growth, physiological traits and cadmium accumulation. J Plant Nutr 40:2127–2137

    CAS  Article  Google Scholar 

  • Milone MT, Sgherri C, Clijsters H, Navari-Izzo F (2003) Antioxidative responses of wheat treated with realistic concentration of cadmium. Environ Exp Bot 50:265–276

    CAS  Article  Google Scholar 

  • Mohamed AA, Castagna A, Ranieri A, di Toppi LS (2012) Cadmium tolerance in Brassica juncea roots and shoots is affected by antioxidant status and phytochelatin biosynthesis. Plant Physiol Biochem 57:15–22

    CAS  Article  Google Scholar 

  • Mukherjee SP, Choudhuri MA (1983) Implications of water stress-induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiol Plant 58:166–170

    CAS  Article  Google Scholar 

  • Nahar K, Hasanuzzaman M, Alam MdM, Rahman A, Suzuki T, Fujita M (2016) Polyamine and nitric oxide crosstalk: antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense and methylglyoxal detoxification systems. Ecotoxicol Environ Saf 126:245–255

    CAS  Article  Google Scholar 

  • Qiu RL, Zhao X, Tang XZ, Yu FM, Hu PJ (2008) Antioxidative response to Cd in a newly discovered cadmium hyperaccumulator, Arabis paniculata F. Chemosphere 74:6–12

    CAS  Article  Google Scholar 

  • Rui H, Chen C, Zhang X, Shen Z, Zhang F (2016) Cd-induced oxidative stress and lignification in the roots of two Vicia sativa L. varieties with different Cd tolerances. J Hazard Mater 301:304–313

    CAS  Article  Google Scholar 

  • Siddiqi MY, Glass ADM, Ruth TJ, Rufty T (1990) Studies of the uptake of nitrate in barley: I. Kinetics of 13NO3 influx. Plant Physiol 93:1426–1432

    CAS  Article  Google Scholar 

  • Sun RL, Zhou QX, Sun FH, Jin CX (2007) Antioxidative defense and proline/phytochelatin accumulation in a newly discovered Cd-hyperaccumulator, Solanum nigrum L. Environ Exp Bot 60:468–476

    CAS  Article  Google Scholar 

  • Sun YB, Zhou QX, Wang L, Liu W (2009) Cadmium tolerance and accumulation characteristics of Bidens pilosa L. as a potential Cd-hyperaccumulator. J Hazard Mater 161:808–814

    CAS  Article  Google Scholar 

  • Tauqeer HM, Ali S, Rizwan M, Ali Q, Saeed R, Ahmad UR, Farid M, Abbasi GH (2016) Phytoremediation of heavy metals by Alternanthera bettzickiana: growth and physiological response. Ecotoxicol Environ Saf 126:138–146

    CAS  Article  Google Scholar 

  • Tran TA, Popova LP (2013) Functions and toxicity of cadmium in plants: recent advances and future prospects. Turk J Bot 37:1–13

    CAS  Google Scholar 

  • Ünyayar S, Keles Y, Çekiç FÖ (2005) The antioxidative response of two tomato species with different drought tolerances as a result of drought and cadmium stress combinations. Plant Soil Environ 51:57–64

    Article  Google Scholar 

  • Vecchia FD, La Rocca N, Moro I, De Faveri S, Andreoli C, Rascio N (2005) Morphogenetic, ultrastructural and physiological damages suffered by submerged leaves of Elodea Canadensis exposed to cadmium. Plant Sci 168:329–338

    Article  Google Scholar 

  • Willekens H, Chamnongpol S, Davey M, Schraunder M, Langebartels C, Van-Montagu M, Inzé D, Van-Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defense in C3 plants. EMBO J 16:4806–4816

    CAS  Article  Google Scholar 

  • World Health Organization (2007) WHO guidelines for assessing quality of herbal medicines with reference to contaminants and residues. WHO Publishers, Geneva

    Google Scholar 

  • Wu Z, Zhao X, Sun X, Tan Q, Tang Y, Nie Z, Qu C, Chen Z, Hu C (2015) Antioxidant enzyme systems and the ascorbate–glutathione cycle as contributing factors to cadmium accumulation and tolerance in two oilseed rape cultivars (Brassica napus L.) under moderate cadmium stress. Chemosphere 138:526–536

    CAS  Article  Google Scholar 

  • Xu J, Yin HX, Li X (2009) Protective effects of proline against cadmium toxicity in micropropagated hyperaccumulator, Solanum nigrum L. Plant Cell Rep 28:325–333

    CAS  Article  Google Scholar 

  • Yılmaz DD, Parlak KU (2011) Changes in proline accumulation and antioxidative enzyme activities in Groenlandia densa under cadmium stress. Ecol Indic 11:417–423

    Article  Google Scholar 

  • Zhang S, Chen M, Li T, Xu X, Deng L (2010) A newly found cadmium accumulator-Malva sinensis Cavan. J Hazard Mater 173:705–709

    CAS  Article  Google Scholar 

  • Zhang H, Guo Q, Yang J, Shen J, Chen T, Zhu G, Chen H, Shao C (2015) Sub cellular cadmium distribution and antioxidant enzymatic activities in the leaves of two castor (Ricinus communis L.) cultivars exhibit differences in Cd accumulation. Ecotoxicol Environ Saf 120:184–192

    CAS  Article  Google Scholar 

  • Zouari M, Ahmed CB, Elloumi N, Bellassoued K, Delmail D, Labrousse P, Abdallah FB, Rouina BB (2016) Impact of proline application on cadmium accumulation, mineral nutrition and enzymatic antioxidant defense system of Olea europaea L. cv Chemlali exposed to cadmium stress. Ecotoxicol Environ Saf 128:195–205

    CAS  Article  Google Scholar 

  • Zoufan P, Saadatkhah A, Rstegarzadeh S (2015) Amount of Mn and Zn in herbaceous plants growing on industrial area of steel production companies in southeast of Ahvaz, Iran. Prog Biol Sci 5:181–193

    Google Scholar 

  • Zoufan P, Jalali R, Karimiafshar A, Motamedi H (2017) Assessment of heavy metal accumulation and antibacterial activity of some medicinal herbs grown in an industrial area of steel production, Ahvaz. Iran J Pharm Sci 13:73–86

    Google Scholar 

Download references

Acknowledgements

This work was supported by the Research Affairs of Shahid Chamran University of Ahvaz (Grant No. 94/3/02/31579).

Author information

Affiliations

  1. Department of Biology, Faculty of Science, Shahid Chamran University of Ahvaz, Ahvaz, Iran

    Parzhak Zoufan, Roya Jalali & Elham Neisi

  2. Department of Agronomy and Plant Breeding, Faculty of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz, Iran

    Payman Hassibi

  3. Department of Chemistry, Faculty of Science, Shahid Chamran University of Ahvaz, Ahvaz, Iran

    Saadat Rastegarzadeh

Authors
  1. Parzhak Zoufan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roya Jalali
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Payman Hassibi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elham Neisi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Saadat Rastegarzadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

PZ designed and conducted the research, analyzed the data and wrote the paper; RJ performed all the assessments related to growth and biochemical parameters; EN measured cadmium concentration of plant tissues; PH and SR helped as consultant to carry out measurement protocols.

Corresponding author

Correspondence to Parzhak Zoufan.

Ethics declarations

Conflict of interest

The authors declared that they have no conflict of interest.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zoufan, P., Jalali, R., Hassibi, P. et al. Evaluation of antioxidant bioindicators and growth responses in Malva parviflora L. exposed to cadmium. Physiol Mol Biol Plants 24, 1005–1016 (2018). https://doi.org/10.1007/s12298-018-0596-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12298-018-0596-2

Keywords

  • Ascorbate
  • Heavy metal
  • Photosynthetic pigments
  • Proline
  • Oxidative stress