Skip to main content

Advertisement

Log in

Changes in the Growth, Redox Status and Expression of Oxidative Stress Related Genes in Chickpea (Cicer arietinum L.) in Response to Copper Oxide Nanoparticle Exposure

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

Abstract

Copper oxide nanoparticles (CuONPs) are used in a variety of applications and their release into the environment may lead to the contamination of agricultural fields. However, the toxicity of CuONPs is hard to evaluate due to the lack of knowledge of their toxicity in major food crops. In this study, we investigated the toxic effects of CuONPs in germinating seedlings of chickpea (Cicer arietinum L.). The plants were grown in 1/2 strength Murashige and Skoog medium containing 0, 50, 100, 200, 400, and 500 mg L−1 of CuONPs in a growth chamber at 26 ± 2 °C, 16/8 h light/dark photoperiod for 10 days. The toxic effect of CuONPs was tested on seedling development (shoot, root growth, and fresh weight), reactive oxygen species (ROS) generation, peroxidase (POD) enzyme activity, root lignification, and changes in root anatomy. The expression of the oxidative stress-related genes viz. CuZn-SOD (CuZn-superoxide dismutase), CAT (catalase), and APX (ascorbate peroxidase) were studied using real-time polymerase chain reaction. The CuONPs were toxic to chickpea seedlings and decreased the shoot and root growth. The ROS generation and lipid peroxidation level was high in CuONP-treated seedlings. Significant increases in POD enzyme activity and lignin content were observed with increased CuONPs concentrations. Exposure to different concentrations of CuONPs caused retardation of root growth, excess lignification, and cytotoxicity in root cells. Cross sections of roots exposed to CuONPs showed an increase in the number of xylem vessels and also enhanced lignification of xylem vessels. Expression of the CuZn-SOD and CAT genes did not change in shoots under CuONPs exposure. Significant up-regulation of CuZn-SOD gene was observed in roots upon exposure to different concentrations of CuONPs. The expression of the CAT gene was significantly high under 50, 100, and 200 mg L−1 of CuONPs. However, no significant change in the expression of the CAT gene was observed upon exposure to 400 and 500 mg L−1 of CuONPs. The expression levels of the APX gene did not change in shoots and roots under exposure to different concentrations of CuONPs.

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

Access this article

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
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Adhikari T, Kundu S, Biswas AK, Tarafdar JC, Rao AS (2012) Effect of copper oxide nano particle on seed germination of selected crops. J Agric Sci Technol A2:815–823

    Google Scholar 

  • Bowler C, Van Montagu M, Inzé D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116

    Article  CAS  Google Scholar 

  • Brar SK, Verma M, Tyagi RD, Surampalli RY (2010) Engineered nanoparticles in waste water and waste water sludge-evidence and impacts. Waste Manag 30:504–520

    Article  CAS  PubMed  Google Scholar 

  • Castillo FJ (1986) Extra cellular peroxidases as markers of stress? In: Greppin H, Penel C, Gaspar T (eds) Molecular and Physiological Aspects of Plant Peroxidases. University of Geneva Press, Geneva, pp 419–426

    Google Scholar 

  • Christensen JH, Bauw G, Welinder KG, Van Montagu M, Boerjan W (1998) Purification and characterization of peroxidases correlated with lignification in poplar xylem. Plant Physiol 118:125–135

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Croser JS, Clarke HJ, Siddique KH, Khan TN (2003) Low-temperature stress: implications for chickpea (Cicer arietinum L.) improvement. Crit Rev Plant Sci 22:185–219

    Article  Google Scholar 

  • Dastjerdi R, Montazer M (2010) A review on the application of inorganic nano structured materials in the modification of textiles: focus on antimicrobial properties. Colloids Surf B 79:5–18

    Article  CAS  Google Scholar 

  • Dietz KJ, Baier M, Kramer U (1999) Free radicals and reactive oxygen species as mediators of heavy metal toxicity in plants. In: Prasad MNV (ed) Heavy metal stress in plants: from molecules to ecosystems. Springer, Berlin, pp 73–79

    Chapter  Google Scholar 

  • Fielding JL, Hall JL (1978) A biochemical and cytochemical study of peroxidase activity in roots of Pisum sativum. J Exp Bot 29:969–981

    Article  CAS  Google Scholar 

  • Finger-Teixeira A, Ferrarese Mde L, Soares AR, da Silva D, Ferrarese-Filho O (2010) Cadmium-induced lignification restricts soybean root growth. Ecotoxicol Environ Saf 73:1959–1964

    Article  CAS  PubMed  Google Scholar 

  • García-Limones C, Dorado G, Navas-Cortés JA, Jiménez-Díaz RM, Tena M (2009) Changes in the redox status of chickpea roots in response to infection by Fusarium oxysporum f. sp. ciceris: apoplastic antioxidant enzyme activities and expression of oxidative stress-related genes. Plant Biol 11(2):194–203

    Article  PubMed  Google Scholar 

  • Gaspar T, Penel C, Castillo FJ, Greppin H (1985) A two step control of basic and acidic peroxidases and its significance for growth and development. Physiol Plant 64:418–423

    Article  CAS  Google Scholar 

  • Kwasniewski M, Chwialkowsk K, Kwasniewsk J, Kusak J, Siwinski K, Szarejko I (2013) Accumulation of peroxidase-related reactive oxygen species in trichoblasts correlates with root hair initiation in barley. J Plant Physiol 170:185–195

    Article  CAS  PubMed  Google Scholar 

  • Lamport DTA (1986) Roles for peroxidases in cell wall genesis. In: Greppin H, Penel C, Gaspar T (eds) Molecular and physiological aspects of plant peroxidases. University of Geneva Press, Geneva, pp 199–208

    Google Scholar 

  • Lee WM, An YJ, Yoon H, Kweon HS (2008) Toxicity and bioavailability of copper nanoparticles to the terrestrial plants Mung bean (Phaseolus radiatus) and Wheat (Triticum aestivum): plant agar test for water-insoluble nanoparticles. Environ Toxicol Chem 27:1915–1921

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Hyein C, Kim S, Lee IS (2013) The genotoxic effect of ZnO and CuO nanoparticles on early growth of buckwheat, Fagopyrum Esculentum. Water Air Soil Pollution 224:1688–1689

    Article  Google Scholar 

  • Lequeux H, Hermans C, Lutts S, Nathalie V (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 

  • Li TC, Feg TY, Chen WS, Liu ZH (2001) The acute effect of copper on the levels of indole 3- acetic acid and lignin in peanut roots. Austn J Plant Physiol 28:1–6

    Google Scholar 

  • Lin D, Xing B (2007) Phytotoxicity of nanoparticles: inhibition of seed germination and root growth. Environ Pollut 150:243–250

    Article  CAS  PubMed  Google Scholar 

  • Lin CC, Chen LM, Liu ZH (2005) Rapid effect of copper on lignin biosynthesis in soybean roots. Plant Sci 168:855–861

    Article  CAS  Google Scholar 

  • Liu ZJ, Guo YK, Bai JG (2010) Exogenous hydrogen peroxide changes antioxidant enzyme activity and protects ultra structure in leaves of two cucumber ecotypes under osmotic stress. J Plant Growth Regul 29:171–183

    Article  Google Scholar 

  • Madhava Rao KV, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeon pea (Cajanus cajan L. Millspaugh) in response to Zn and Ni stresses. Plant Sci 157:113–128

    Article  CAS  PubMed  Google Scholar 

  • Mazhoudi S, Chaoui A, Ghorbal MH, Elferjani E (1997) Response of antioxidant enzyme to excess copper in tomato (Lycopersicon esculentum Mill). Plant Sci 127:129–137

    Article  CAS  Google Scholar 

  • Melegari SP, Perreault F, Popovic RHRC, Radovan Matias WG (2013) Evaluation of toxicity and oxidative stress induced by copper oxide nanoparticles in the green alga Chlamydomonas reinhardtii. Aquat Toxicol 142–143:431–440

    Article  PubMed  Google Scholar 

  • Nair PMG, Chung IM (2014) Impact of copper oxide nanoparticles exposure on Arabidopsis thaliana growth, root system development, root lignificaion and molecular level changes. Environ Sci Pollut Res 21:12709–12722

    Article  CAS  Google Scholar 

  • Nair R, Varghese SH, Nair BG, Maekawa T, Yoshida Y, Kumar DS (2010) Nanoparticulate material delivery to plants. Plant Sci 179:154–163

    Article  CAS  Google Scholar 

  • Navarro E, Baun A, Behra R, Hartmann NB, Filser J, Miao AJ, Quigg A, Santschi PH, Sigg L (2008) Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants and fungi. Ecotoxicol 17:372–386

    Article  CAS  Google Scholar 

  • Oleszczuk P, Josko I, Xing BS (2011) The toxicity to plants of the sewage sludges containing multiwalled carbon nanotubes. J Hazard Mater 186:436–442

    Article  CAS  PubMed  Google Scholar 

  • Passardi F, Cosio C, Penel C, Dunand C (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Rep 24:255–265

    Article  CAS  PubMed  Google Scholar 

  • Perez-de-Luque Alejandro, Rubiales Diego (2009) Nanotechnology for parasitic plant control. Pest Manag Sci 65:540–545

    Article  CAS  PubMed  Google Scholar 

  • Perreault F, Samadani M, Dewez D (2014) Effect of soluble copper released from copper oxide nanoparticles solubilisation on growth and photosynthetic processes of Lemna gibba L. Nanotoxicol 8:374–382

    Article  CAS  Google Scholar 

  • Polle A, Otter T, Seifert F (1994) Apoplastic peroxidase and lignification in needles of Norway spruce (Picea abies L.). Plant Physiol 106:53–60

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ren G, Hu D, Cheng EWC, Vargas-Reus MA, Reip P, Allaker RP (2009) Characterization of copper oxide nanoparticles for antimicrobial applications. Int J Antimicrob Agents 33:587–590

    Article  CAS  PubMed  Google Scholar 

  • Rico CM, Majumdar S, Duarte-Gardea M, Peralta-Videa JR, Gardea-Torresdey JL (2011) Interaction of nanoparticles with edible plants and their possible implications in the food chain. J Agri Food Chem 59:3485–3498

    Article  CAS  Google Scholar 

  • Rogers LA, Dubos C, Surman C, Willment J, Cullis IF, Mansfield SD, Campbell MM (2005) Comparison of lignin deposition in three ectopic lignification mutants. New Phytol 168:123–140

    Article  CAS  PubMed  Google Scholar 

  • Sanchez M, Revilla G, Zarra I (1995) Changes in peroxidase activity associated with cell walls during pine hypocotyl growth. Ann Bot 75:415–419

    Article  CAS  Google Scholar 

  • Sandmann G, Boger P (1980) Copper-mediated lipid peroxidation processes in photosynthetic membranes. Plant Physiol 66:797–800

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shaw AK, Hossain Z (2013) Impact of nano-CuO stress on rice (Oryza sativa L.) seedlings. Chemosphere 93:906–915

    Article  CAS  PubMed  Google Scholar 

  • Shaw AK, Ghosh S, Kalaji HM, Bosa K, Brestic M, Zivcak M, Hossain Z (2014) Nano-CuO stress induced modulation of antioxidative defense and photosynthetic performance of syrian barley (Hordeum vulgare L.). Environ Exp Bot 102:37–47

    Article  CAS  Google Scholar 

  • Shi J, Peng C, Yang Y, Yang J, Zhang H, Yuan X, Chen Y, Hu T (2014) Phytotoxicity and accumulation of copper oxide nanoparticles to the Cu-tolerant plant Elsholtzia splendens. Nanotoxicol 8:179–188

    Article  CAS  Google Scholar 

  • Stampoulis D, Sinha SK, White JC (2009) Assay-dependent phytotoxicity of nanoparticles to plants. Environ Sci Technol 43:9473–9479

    Article  CAS  PubMed  Google Scholar 

  • Takeshi M, In Sook ML, Noriyuki S, Takakiro I (1997) Identification of S100b protein as copper-binding protein and its suppression of copper-induced cell damage. J Biol Chem 272:23037–23041

    Article  Google Scholar 

  • Torney F, Trewyn BG, Lin VSY, Wang K (2007) Mesoporous silica nanoparticles deliver DNA and chemicals into plants. Nature Nanotechnol 2:295–300

    Article  CAS  Google Scholar 

  • Tripathi BN, Mehta SK, Amar A, Gaur JP (2006) Oxidative stress in Scenedesmus sp. during short- and long-term exposure to Cu and Zn. Chemosphere 62:538–544

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Xie X, Zhao J, Liu X, Feng W, White JC, Xing B (2012) Xylem and phloem based transport of CuO nanoparticles in maize (Zea mays L.). Environ Sci Technol 46:4434–4441

    Article  CAS  PubMed  Google Scholar 

  • Wu SG, Huang L, Head J, Chen DR, Kong IC, Tang YJ (2012a) Phytotoxicity of metal oxide nanoparticles is related to both dissolved metals ions and adsorption of particles on seed surfaces. J Pet Environ Biotechnol 3:126

    CAS  Google Scholar 

  • Wu Z, Song L, Feng S, Liu Y, He G, Yioe Y, Liu SQ, Huang D (2012b) Germination dramatically increases isoflavonoid content and diversity in chickpea (Cicer arietinum L.) seeds. J Agric Food Chem 60:8606–8615

    Article  CAS  PubMed  Google Scholar 

  • Xiong ZT, Wang H (2005) Copper toxicity and bioaccumulation in Chinese cabbage (Brassica pekinensis Rupr.). Environ Toxicol 20:188–194

    Article  CAS  PubMed  Google Scholar 

  • Yruela I (2005) Copper in plants. Braz J Plant Physiol 17:145–146

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This paper was supported by the KU Research Professor Program of Konkuk University, Seoul, South Korea to Prakash M. Gopalakrishnan Nair. This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT and Future Planning (2014R1A2A2A01002202).

Conflict of interest

The authors declare no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ill Min Chung.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nair, P.M.G., Chung, I.M. Changes in the Growth, Redox Status and Expression of Oxidative Stress Related Genes in Chickpea (Cicer arietinum L.) in Response to Copper Oxide Nanoparticle Exposure. J Plant Growth Regul 34, 350–361 (2015). https://doi.org/10.1007/s00344-014-9468-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-014-9468-3

Keywords

Navigation