Skip to main content
Log in

Effect of copper oxide nanoparticles on growth, morphology, photosynthesis, and antioxidant response in Oryza sativa

  • Original Papers
  • Published:
Photosynthetica

Abstract

The physiological and biochemical behaviour of rice (Oryza sativa, var. Jyoti) treated with copper (II) oxide nanoparticles (CuO NPs) was studied. Germination rate, root and shoot length, and biomass decreased, while uptake of Cu in the roots and shoots increased at high concentrations of CuO NPs. The accumulation of CuO NPs was observed in the cells, especially, in the chloroplasts, and was accompanied by a lower number of thylakoids per granum. Photosynthetic rate, transpiration rate, stomatal conductance, maximal quantum yield of PSII photochemistry, and photosynthetic pigment contents declined, with a complete loss of PSII photochemical quenching at 1,000 mg(CuO NP) L−1. Oxidative and osmotic stress was evidenced by increased malondialdehyde and proline contents. Elevated expression of ascorbate peroxidase and superoxide dismutase were also observed. Our work clearly demonstrated the toxic effect of Cu accumulation in roots and shoots that resulted in loss of photosynthesis.

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.

Similar content being viewed by others

Abbreviations

AAS:

atomic absorption spectrophotometer

APX:

ascorbate peroxidase

DM:

dry mass

E :

transpiration rate

FM:

fresh mass

Fm :

maximum fluorescence

Fo :

initial fluorescence

Fs :

steady-state fluorescence

Fv/Fm :

maximal quantum yield of PSII photochemistry

GR:

glutathione reductase

gs :

stomatal conductance

IRGA:

infra red gas analyser

MDA:

malondialdehyde

NP(s):

nanoparticle(s)

P N :

photosynthetic rate

qP :

photochemical quenching

ROS:

reactive oxygen species

SEM:

scanning electron microscope

SOD:

superoxide dismutase

TBA:

thiobarbituric acid

TEM:

transmission electron microscope

XRD:

X-ray diffraction

References

  • Abdelkader A.F., Aronsson H., Solymosi K. et al.: High salt stress induces swollen prothylakoids in dark-grown wheat and alters both prolamellar body transformation and reformation after irradiation. — J. Exp. Bot. 58: 2553–2564, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Alia, Pardha Saradhi, P.: Proline accumulation under heavy metal stress. — J. Plant Physiol. 138: 554–558, 1991.

    Article  CAS  Google Scholar 

  • Bassi R., Sharma S.S.: Changes in proline content accompanying the uptake of zinc and copper by Lemna minor. — Ann. Bot.-London 72: 151–154, 1993.

    Article  CAS  Google Scholar 

  • Bates L.S., Waldren R.P., Teare I.D.: Rapid determination of free proline for water-stress studies. — Plant Soil 39: 205–207, 1973.

    Article  CAS  Google Scholar 

  • Bohnert H.J., Nelson D.E., Jensen R.G.: Adaptations to environmental stresses. — Plant Cell 7: 1099–1111, 1995.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Campbell R., Greaves M.P.: Anatomy and community structure of the rhizosphere. — In: Lynch J.M. (ed.): The Rhizosphere. Pp. 11–34. John Wiley and Sons Ltd. Publ., London 1990.

    Google Scholar 

  • Caverzan A., Passaia G., Rosa S.B. et al.: Plant responses to stresses: Role of ascorbate peroxidase in the antioxidant protection. — Genet. Mol. Biol. 35: 1011–1019, 2012.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Corredor E., Testillano P.S., Coronado M.-J. et al.: Nanoparticle penetration and transport in living pumpkin plants: in situ subcellular identification. — BMC Plant Biol. 9: 45–45, 2009.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Harrison P.: Emerging challenges: nanotechnology and the environment. — In: GEO Year Book 2007. Pp. 61–68. United Nations Environment Programme (UNEP), Nairobi 2007.

    Google Scholar 

  • Haverkamp R.G., Marshall A.T.: The mechanism of metal nanoparticle formation in plants: Limits on accumulation. — J. Nanoparticle Res. 11: 1453–1463, 2009.

    Article  CAS  Google Scholar 

  • Inzé D., Van Montagu M.: Oxidative stress in plants. — Curr. Opin. Biotech. 6: 153–158, 1995.

    Article  Google Scholar 

  • Kampfenkel K., Van Montagu M., Inzé D.: Extraction and determination of ascorbate and dehydroascorbate from plant tissue. — Anal. Biochem. 225: 165–167, 1995.

    Article  PubMed  CAS  Google Scholar 

  • Kennedy C.D., Gonsalves F.A.N.: The action of divalent zinc, cadmium, mercury, copper and lead on the trans-root potential and H+ efflux of excised roots. — J. Exp. Bot. 38: 800–817, 1987.

    Article  CAS  Google Scholar 

  • Kirchhoff H., Horstmann S., Weis E.: Control of the photosynthetic electron transport by PQ diffusion microdomains in thylakoids of higher plants. — BBA-Bioenergetics 1459: 148–168, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Klaine S.J., Alvarez P.J.J., Batley G.E. et al.: Nanomaterials in the environment: behavior, fate, bioavailability, and effects. — Environ. Toxicol. Chem. 27: 1825–1851, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Lee C.W., Mahendra S., Zodrow K. et al.: Developmental phytotoxicity of metal oxide nanoparticles to Arabidopsis thaliana. — Environ. Toxicol. Chem. 29: 669–675, 2010.

    Article  PubMed  CAS  Google Scholar 

  • Lee S., Kim S., Kim S. et al.: Assessment of phytotoxicity of ZnO NPs on a medicinal plant, Fagopyrum esculentum. — Environ. Sci. Pollut. Res. 20: 848–854, 2013.

    Article  CAS  Google Scholar 

  • Lee W.M., An Y.J., Yoon H. et al.: 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, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Lidon F.C., Henriques F.S.: Role of rice shoot vacuoles in copper toxicity regulation. — Environ. Exp. Bot. 39: 197–202, 1998.

    Article  CAS  Google Scholar 

  • Lin D., Xing B.: Root uptake and phytotoxicity of ZnO nanoparticles. — Environ. Sci. Technol. 42: 5580–5585, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Manceau A., Nagy K.L., Marcus M.A. et al.: Formation of metallic copper nanoparticles at the soil-root interface. — Environ. Sci. Technol. 42: 1766–1772, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Marschner H.: Mineral Nutrition of Higher Plants. Pp. 889. Academic Press, London 1995.

    Google Scholar 

  • Maynard A.D., Aitken R.J., Butz T. et al.: Safe handling of nanotechnology. — Nature 444: 267–269, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Mehta S.K., Gaur J.P.: Heavy metal-induced proline accumulation and its role in ameliorating metal toxicity in Chlorella vulgaris. — New Phytol. 143: 253–259, 1999.

    Article  CAS  Google Scholar 

  • Musante C., White J.C.: Toxicity of silver and copper to Cucurbita pepo: Differential effects of nano and bulk-size particles. — Environ. Toxicol. 27: 510–517, 2012.

    Article  PubMed  CAS  Google Scholar 

  • Nagajyoti P.C., Lee K.D., Sreekanth T.V.M. et al.: Heavy metals, occurrence and toxicity for plants: A review. — Environ. Chem. Lett. 8: 199–216, 2010.

    Article  CAS  Google Scholar 

  • Navarro E., Baun A., Behra R. et al.: Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. — Ecotoxicology 5: 372–386, 2008.

    Article  CAS  Google Scholar 

  • Nekrasova G.F., Ushakova O.S., Ermakov A.E. et al.: Effects of copper (II) ions and copper oxide nanoparticles on Elodea densa Planch. — Russian J. Ecol. 42: 458–463, 2011.

    Article  CAS  Google Scholar 

  • Noctor G., Foyer C.H.: Ascorbate and glutathione: Keeping active oxygen under control. — Annu. Rev. Plant Phys. 49: 249–279, 1998.

    Article  CAS  Google Scholar 

  • Ojamäe L., Aulin C., Pedersen H. et al.: IR and quantumchemical studies of carboxylic acid and glycine adsorption on rutile TiO2 nanoparticles. — J. Colloid Interface Sci. 296: 71–78, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Perreault F., Oukarroum A., Pirastru L. et al.: Evaluation of copper oxide nanoparticles toxicity using chlorophyll a fluorescence imaging in Lemna gibba. — J. Bot. 2010, 1–9, 2010.

    Article  CAS  Google Scholar 

  • Raven J.A., Evans M.C., Korb R.E.: The role of trace metals in photosynthetic electron transport in O2 - evolving organisms. — Photosynth. Res. 60: 111–150, 1999.

    Article  CAS  Google Scholar 

  • Rico C.M., Majumdar S., Duarte-Gardea M. et al.: Interaction of nanoparticles with edible plants and their possible implications in the food chain. — J. Agric. Food Chem. 59: 3485–3498, 2011.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Saison C., Perreault F., Daigle J.C. et al.: Effect of core-shell copper oxide nanoparticles on cell culture morphology and photosynthesis (photosystem II energy distribution) in the green alga, Chlamydomonas reinhardtii. — Aquat. Toxicol. 96: 109–114, 2010.

    Article  PubMed  CAS  Google Scholar 

  • Sankhalkar S., Sharma P.K.: Protection against photooxidative damage provided by enzymatic and non-enzymatic antioxidant system in sorghum seedlings. — Indian J. Exp. Biol. 40: 1260–1268, 2002.

    PubMed  CAS  Google Scholar 

  • Sharma P.K., Hall D.O.: Effect of photoinhibition and temperature on carotenoids in sorghum leaves. — Indian J. Biochem. Biophys. 33: 471–477, 1996.

    PubMed  CAS  Google Scholar 

  • Sharma P.K., Shetye R., Bhonsle S.: Effect of supplementary ultraviolet-B radiation on young wheat seedlings. — Curr. Sci. 72: 400–405, 1997.

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Shi J., Abid A.D., Kennedy I.M. et al.: To duckweeds (Landoltia punctata), nanoparticulate copper oxide is more inhibitory than the soluble copper in the bulk solution. — Environ. Pollut. 159: 1277–1282, 2011.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Smirnoff N.: Tansley Review 52. The role of active oxygen in the response of plants to water-deficit and desiccation. — New Phytol. 125: 27–58, 1993.

    Article  CAS  Google Scholar 

  • Solymosi K., Bertrand M.: Soil metals, chloroplasts, and secure crop production: a review. — Agron. Sustain. Dev. 32: 245–272, 2012.

    Article  CAS  Google Scholar 

  • Song, L., Vijver, M. G., Peijnenburg, W. J. G. M.: Comparative toxicity of copper nanoparticles across three Lemnaceae species. — Sci. Total Environ. 518–519: 217–224, 2015.

    Article  PubMed  CAS  Google Scholar 

  • Stampoulis D., Sinha S.K., White J.C.: Assay-dependent phytotoxicity of nanoparticles to plants. — Environ. Sci. Technol. 43: 9473–9479, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Ünnep R., Zsiros O., Solymosi K. et al.: The ultrastructure and flexibility of thylakoid membranes in leaves and isolated chloroplasts as revealed by small-angle neutron scattering. — BBA-Bioenergetics 1837: 1572–1580, 2014.

    Article  PubMed  CAS  Google Scholar 

  • Wang S.-H., Yang Z.-M., Yang H. et al.: Copper-induced stress and antioxidative responses in roots of Brassica juncea L. — Bot. Bull. Acad. Sin. 45: 203–212, 2004.

    CAS  Google Scholar 

  • Wierzbicka M.S., Obidzińska J.: The effect of lead on seed imbibition and germination in different plant species. — Plant Sci. 137: 155–171, 1998.

    Article  CAS  Google Scholar 

  • Wiesner M.R., Lowry G.V., Alvarez P. et al.: Assessing the risks of manufactured nanomaterials. — Environ. Sci. Technol. 40: 4336–4345, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Yoshimura K., Yabuta Y., Ishikawa T. et al.: Expression of spinach ascorbate peroxidase isoenzymes in response to oxidative stresses. — Plant Physiol. 123: 223–233, 2000.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yruela I.: Copper in plants. — Brazilian J. Plant Physiol. 17: 145–156, 2005.

    Article  CAS  Google Scholar 

  • Zhang W., Elliott D.W.: Applications of iron nanoparticles for groundwater remediation. — Remediat. J. 16: 7–21, 2006.

    Article  Google Scholar 

  • Zhang Z., He X., Zhang H. et al.: Uptake and distribution of ceria nanoparticles in cucumber plants. — Metallomics 3: 816–822, 2011.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P. K. Sharma.

Additional information

Acknowledgements: We thank the Department of Science & Technology (DST), New Delhi (SR/SO/PS-63/2009) and UGC-SAP (F. 3-50/2009 (SAP-II) for funding this work. We would like to thank All India Institute of Medical Sciences, New Delhi for TEM imaging; NIO, Goa for SEM imaging and atomic absorption spectrophotometry; Physics Department, Goa University for NP size determination using X-ray diffractometer. We are grateful to Andrew Willis, Centre for Agroecology, Water and Resilience (CAWR), Coventry University, Coventry, United Kingdom for correcting the English of the manuscript.

Both authors made equal contribution to the work presented in this paper.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Da Costa, M.V.J., Sharma, P.K. Effect of copper oxide nanoparticles on growth, morphology, photosynthesis, and antioxidant response in Oryza sativa . Photosynthetica 54, 110–119 (2016). https://doi.org/10.1007/s11099-015-0167-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-015-0167-5

Additional key words

Navigation