Advertisement

Photosynthetica

, Volume 54, Issue 1, pp 110–119 | Cite as

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

  • M. V. J. Da Costa
  • P. K. Sharma
Original Papers

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.

Additional key words

ascorbate nanoparticle proline superoxide dismutase thylakoid 

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)

PN

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

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 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.CrossRefPubMedGoogle Scholar
  2. Alia, Pardha Saradhi, P.: Proline accumulation under heavy metal stress. — J. Plant Physiol. 138: 554–558, 1991.CrossRefGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. Bates L.S., Waldren R.P., Teare I.D.: Rapid determination of free proline for water-stress studies. — Plant Soil 39: 205–207, 1973.CrossRefGoogle Scholar
  5. Bohnert H.J., Nelson D.E., Jensen R.G.: Adaptations to environmental stresses. — Plant Cell 7: 1099–1111, 1995.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 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
  7. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 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
  10. Haverkamp R.G., Marshall A.T.: The mechanism of metal nanoparticle formation in plants: Limits on accumulation. — J. Nanoparticle Res. 11: 1453–1463, 2009.CrossRefGoogle Scholar
  11. Inzé D., Van Montagu M.: Oxidative stress in plants. — Curr. Opin. Biotech. 6: 153–158, 1995.CrossRefGoogle Scholar
  12. Kampfenkel K., Van Montagu M., Inzé D.: Extraction and determination of ascorbate and dehydroascorbate from plant tissue. — Anal. Biochem. 225: 165–167, 1995.CrossRefPubMedGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. 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.CrossRefPubMedGoogle Scholar
  15. 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.CrossRefPubMedGoogle Scholar
  16. 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.CrossRefPubMedGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. 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.CrossRefPubMedGoogle Scholar
  19. Lidon F.C., Henriques F.S.: Role of rice shoot vacuoles in copper toxicity regulation. — Environ. Exp. Bot. 39: 197–202, 1998.CrossRefGoogle Scholar
  20. Lin D., Xing B.: Root uptake and phytotoxicity of ZnO nanoparticles. — Environ. Sci. Technol. 42: 5580–5585, 2008.CrossRefPubMedGoogle Scholar
  21. 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.CrossRefPubMedGoogle Scholar
  22. Marschner H.: Mineral Nutrition of Higher Plants. Pp. 889. Academic Press, London 1995.Google Scholar
  23. Maynard A.D., Aitken R.J., Butz T. et al.: Safe handling of nanotechnology. — Nature 444: 267–269, 2006.CrossRefPubMedGoogle Scholar
  24. 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.CrossRefGoogle Scholar
  25. 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.CrossRefPubMedGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. 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.CrossRefGoogle Scholar
  28. 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.CrossRefGoogle Scholar
  29. Noctor G., Foyer C.H.: Ascorbate and glutathione: Keeping active oxygen under control. — Annu. Rev. Plant Phys. 49: 249–279, 1998.CrossRefGoogle Scholar
  30. 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.CrossRefPubMedGoogle Scholar
  31. 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.CrossRefGoogle Scholar
  32. 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.CrossRefGoogle Scholar
  33. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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.CrossRefPubMedGoogle Scholar
  35. 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.PubMedGoogle Scholar
  36. Sharma P.K., Hall D.O.: Effect of photoinhibition and temperature on carotenoids in sorghum leaves. — Indian J. Biochem. Biophys. 33: 471–477, 1996.PubMedGoogle Scholar
  37. Sharma P.K., Shetye R., Bhonsle S.: Effect of supplementary ultraviolet-B radiation on young wheat seedlings. — Curr. Sci. 72: 400–405, 1997.Google Scholar
  38. Shaw A.K., Hossain Z.: Impact of nano-CuO stress on rice (Oryza sativa L.) seedlings. — Chemosphere 93: 906–915, 2013.CrossRefPubMedGoogle Scholar
  39. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 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.CrossRefGoogle Scholar
  41. Solymosi K., Bertrand M.: Soil metals, chloroplasts, and secure crop production: a review. — Agron. Sustain. Dev. 32: 245–272, 2012.CrossRefGoogle Scholar
  42. 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.CrossRefPubMedGoogle Scholar
  43. Stampoulis D., Sinha S.K., White J.C.: Assay-dependent phytotoxicity of nanoparticles to plants. — Environ. Sci. Technol. 43: 9473–9479, 2009.CrossRefPubMedGoogle Scholar
  44. 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.CrossRefPubMedGoogle Scholar
  45. 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.Google Scholar
  46. Wierzbicka M.S., Obidzińska J.: The effect of lead on seed imbibition and germination in different plant species. — Plant Sci. 137: 155–171, 1998.CrossRefGoogle Scholar
  47. Wiesner M.R., Lowry G.V., Alvarez P. et al.: Assessing the risks of manufactured nanomaterials. — Environ. Sci. Technol. 40: 4336–4345, 2006.CrossRefPubMedGoogle Scholar
  48. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Yruela I.: Copper in plants. — Brazilian J. Plant Physiol. 17: 145–156, 2005.CrossRefGoogle Scholar
  50. Zhang W., Elliott D.W.: Applications of iron nanoparticles for groundwater remediation. — Remediat. J. 16: 7–21, 2006.CrossRefGoogle Scholar
  51. Zhang Z., He X., Zhang H. et al.: Uptake and distribution of ceria nanoparticles in cucumber plants. — Metallomics 3: 816–822, 2011.CrossRefPubMedGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2016

Authors and Affiliations

  1. 1.Department of BotanyGoa UniversityGoaIndia

Personalised recommendations