biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 62:801-808, 2018 | DOI: 10.1007/s10535-018-0813-4

Effects of zinc oxide nanoparticles on the growth, photosynthetic traits, and antioxidative enzymes in tomato plants

X. P. Wang1,2,3, Q. Q. Li3, Z. M. Pei2, S. C. Wang3,*
1 Key Laboratory of Optoelectronic Devices and Systems of Ministry of Education and Guangdong Province, College of Optoelectronic Engineering, Shenzhen University, Shenzhen, P.R. China
2 Shenzhen Key Laboratory of Marine Bioresources and Eco-environmental Science, Guangdong Engineering Research Center for Marine Algal Biotechnology, College of Life Science and Oceanography, Shenzhen University, Shenzhen, P.R. China
3 Key laboratory of Molecular Epigenetics of Ministry of Education, Northeast Normal University, Changchun, P.R. China

With the dramatic increase in nanotechnologies, it has become probable that biological systems will be exposed to excess of nanoparticles (NPs). However, the impact of NPs on plants, remains to be explored. The aim of this research was to determine the effects of ZnO NPs on tomato (Solanum lycopersicum L.) plants. Plant growth, photosynthetic characteristics, chlorophyll fluorescence parameters, and activities of antioxidative enzymes were measured in 35-d-old plants. The ZnO NP treatments significantly inhibited tomato root and shoot growth, decreased the content of chlorophylls a and b, and reduced photosynthetic efficiency and some other chlorophyll fluorescence parameters in a concentration-dependent manner. However, the supernatant of ZnO NP suspensions did not affect growth of tomato, despite the presence of small amounts of Zn2+. Taken together, these results suggest that toxic effects on tomato plants were from ZnO NPs, not from Zn2+ released into the solution; toxicity was likely caused by reduced chlorophyll content and damaged photochemical system, which in turn limited photosynthesis and led to the reduction in biomass accumulation. Also, ZnO NPs enhanced the transcription of genes related to antioxidant capacity, suggesting that ZnO NPs could enhance the defence response by increasing activities of antioxidant enzymes.

Keywords: carotenoids; catalase; chlorophyll content; chlorophyll fluorescence; net photosynthetic rate; stomatal conductance; Solanum lycopersicum; transpiration rate
Subjects: zinc; zinc oxide nanoparticles; carotenoids; chlorophyll content; chlorophyll fluorescence; net photosynthetic rate; transpiration rate; stomatal conductance; tomato

Received: September 11, 2017; Revised: January 25, 2018; Accepted: March 7, 2018; Published: August 1, 2018  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Wang, X.P., Li, Q.Q., Pei, Z.M., & Wang, S.C. (2018). Effects of zinc oxide nanoparticles on the growth, photosynthetic traits, and antioxidative enzymes in tomato plants. Biologia plantarum, 62(4), 801-808. doi: 10.1007/s10535-018-0813-4
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    Supplementary files

    Download filebpl-201804-0020_S1.pdf

    File size: 525.58 kB

    References

    1. Ambavaram, M.M., Basu, S., Krishnan, A., Ramegowda, V., Batlang, U., Rahman, L., Baisakh, N., Pereira, A.: Coordinated regulation of photosynthesis in rice increases yield and tolerance to environmental stress. - Nat. Commun. 5302: 5302, 2014. Go to original source...
    2. Bandyopadhyay, S., Peralta-Videa, J.R., Hernandez-Viezcas, J.A., Montes, M.O., Keller, A.A., Gardea-Torresdey, J.L.: Microscopic and spectroscopic methods applied to the measurements of nanoparticles in the environment. - Appl. Spectroscopy Rev. 180: 180-206, 2012a. Go to original source...
    3. Bandyopadhyay, S., Peralta-Videa, J.R., Plascencia-Villa, G., José-Yacamán, M., Gardea-Torresdey, J.L.: Comparative toxicity assessment of CeO2 and ZnO nanoparticles towards Sinorhizobium meliloti, a symbiotic alfalfa associated bacterium: use of advanced microscopic and spectroscopic techniques. - J. Hazard. Mater. 241-379: 379-386, 2012b. Go to original source...
    4. Bandyopadhyay, S., Plascencia-Villa, G., Mukherjee, A., Rico, C.M., José-Yacamán, M., Peralta-Videa, J.R., Gardea-Torresdey, J.L.: Comparative phytotoxicity of ZnO NPs, bulk ZnO, and ionic zinc onto the alfalfa plants symbiotically associated with Sinorhizobium meliloti in soil. - Sci. total Environ. 515-60: 60-69, 2015. Go to original source...
    5. Boonyanitipong, P., Kositsup, B., Kumar, P., Baruah, S., Dutta, J.: Toxicity of ZnO and TiO2 nanoparticles on germinating rice seed Oryza sativa L. - Int. J. Biosci., Biochem. Bioinform. 282: 282-285, 2011. Go to original source...
    6. Chance, B., Maehly, A.C.: Assay of catalases and peroxidases. - Method. Enzymol. 764: 764-775, 1955. Go to original source...
    7. Choi, O., Hu, Z.: Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. - Environ. Sci. Technol. 4583: 4583-4588, 2008. Go to original source...
    8. Cuypers, A., Vangronsveld, J., Clijsters, H.: The redox status of plant cells (AsA and GSH) is sensitive to zinc imposed oxidative stress in roots and primary leaves of Phaseolus vulgaris. - Plant Physiol. Biochem. 657: 657-664, 2001. Go to original source...
    9. Dietz, K.J., Herth, S.: Plant nanotoxicology. - Trends Plant Sci. 582: 582-589, 2011. Go to original source...
    10. Dimkpa, C.O., McLean, J.E., Britt, D.W., Anderson, A.J.: Bioactivity and biomodification of Ag, ZnO, and CuO nanoparticles with relevance to plant performance in agriculture. - Ind. Biotechnol. 344: 344-357, 2012. Go to original source...
    11. Gajewska, E., Sklodowska, M.: Effect of nickel on ROS content and antioxidative enzyme activities in wheat leaves.-Biometals 27: 27-36, 2007. Go to original source...
    12. Gechev, T.S., Hille, J.: Hydrogen peroxide as a signal controlling plant programmed cell death. - J. cell. Biol. 17: 17-20, 2005. Go to original source...
    13. Hernandez-Viezcas, J.A., Castillo-Michel, H., Servin, A.D., Peralta-Videa, J.R., Gardea-Torresdey, J.L.: Spectroscopic verification of zinc absorption and distribution in the desert plant Prosopis juliflora-velutina (velvet mesquite) treated with ZnO nanoparticles. - Chem. Engn. J. 346: 346-352, 2011. Go to original source...
    14. Hu, H., Wang, L., Wang, Q., Jiao, L., Hua, W., Zhou, Q., Huang, X.: Photosynthesis, chlorophyll fluorescence characteristics, and chlorophyll content of soybean seedlings under combined stress of bisphenol A and cadmium. - Environ. Toxicol. Chem. 2455: 2455-2462, 2014a. Go to original source...
    15. Hu, C.W., Liu, X., Li, X.L., Zhao, Y.J.: Evaluation of growth and biochemical indicators of Salvinia natans exposed to zinc oxide nanoparticles and zinc accumulation in plants. - Environ. Sci. Pollut. Res. 732: 732-739, 2014b. Go to original source...
    16. Karlsson, H.L.: The comet assay in nanotoxicology research. - Anal. Bioanal. Chem. 651: 651-666, 2010. Go to original source...
    17. Klaine, S.J., Alvarez, P.J., Batley, G.E., Fernandes, T.F., Handy, R.D., Lyon, D.Y., Mahendra, S., McLaughlin, M.J., Lead, J.R.: Nanomaterials in the environment: behavior, fate, bioavailability, and effects. - Environ. Toxicol. Chem. 1825: 1825-1851, 2008. Go to original source...
    18. Landa, P., Vankova, R., Andrlova, J., Hodek, J., Marsik, P., Storchova, H., White, J.C., Vanek, T.: Nanoparticle-specific changes in Arabidopsis thaliana gene expression after exposure to ZnO, TiO2, and fullerene soot. - J. Hazard. Mater. 241-55: 55-62, 2012. Go to original source...
    19. Lichtenthaler, H.K., Wellburn, A.R.: Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. - Biochem. Soc. Trans. 591: 591-592, 1983. Go to original source...
    20. Lee, C.W., Mahendra, S., Zodrow, K., Li, D., Tsai, Y.C., Braam, J., Alvarez, P.J.J.: Developmental phytotoxicity of metal oxide nanoparticles to Arabidopsis thaliana. - Environ. Toxicol. Chem. 669: 669-675, 2010. Go to original source...
    21. Lee, S., Kim, S., Kim, S., Lee, I.: Assessment of phytotoxicity of ZnO NPs on a medicinal plant, Fagopyrum esculentum. - Environ. Sci. Pollut. Res. 848: 848-854, 2013. Go to original source...
    22. Lee, W.M., An, Y.J., Yoon, H., Kweon, H.S.: 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. 1915: 1915-1921, 2008. Go to original source...
    23. Lin, D., Xing, B.: Phytotoxicity of nanoparticles: inhibition of seed germination and root growth. - Environ. Pollut. 243: 243-250, 2007. Go to original source...
    24. Lin, D., Xing, B.: Root uptake and phytotoxicity of ZnO nanoparticles. - Environ. Sci. Technol. 5580: 5580-5585, 2008. Go to original source...
    25. Lin, S., Reppert, J., Hu, Q., Hudson, J.S., Reid, M.L., Ratnikova, T.A., Rao, A.M., Luo, H., Ke, P.C.: Uptake, translocation, and transmission of carbon nanomaterials in rice plants.-Small 1128: 1128-1132, 2009. Go to original source...
    26. López-Moreno, M.L., Rosa, G.D.L., Cruz-Jiménez, G., Castellano, L., Peralta-Videa, J.R., Gardea-Torresdey, J.L.: Effect of ZnO nanoparticles on corn seedlings at different temperatures; X-ray absorption spectroscopy and ICP/OES studies. - Microchem. J. 54: 54-61, 2017. Go to original source...
    27. Ma, X., Geiser-Lee, J., Deng, Y., Kolmakov, A.: Interactions between engineered nanoparticles (ENPs) and plants: phytotoxicity, uptake and accumulation. - Sci. Total Environ. 3053: 3053-3061, 2010. Go to original source...
    28. Mehrabi, M., Wilson, R.: Intercalating gold nanoparticles as universal labels for DNA detection. - Small 1491: 1491-1495, 2007. Go to original source...
    29. Miralles, P., Church, T.L., Harris, A.T.: Toxicity, uptake, and translocation of engineered nanomaterials in vascular plants. - Environ. Sci. Technol. 9224: 9224-9239, 2012. Go to original source...
    30. Mittler, R., Vanderauwera, S., Gollery, M., Van Breusegem, F.: Reactive oxygen gene network of plants. - Trends Plant Sci. 490: 490-498, 2004. Go to original source...
    31. Mousavi Kouhi, S.M., Lahouti, M., Ganjeali, A., Entezar, M.H.: Comparative phytotoxicity of ZnO nanoparticles, ZnO microparticles, and Zn2+ on rapeseed (Brassica napus L.): investigating a wide range of concentrations. - Toxicol. Environ. Chem. 861: 861-868, 2014. Go to original source...
    32. Mukherjee, A., Pokhrel, S., Bandyopadhyay, S., Mädler, L., Peralta-Videa, J.R., Gardea-Torresdey, J.L.: A soil mediated phyto-toxicological study of iron doped zinc oxide nanoparticles (Fe@ZnO) in green peas (Pisum sativum L.). - Chem. Engn. J. 394: 394-401, 2014a. Go to original source...
    33. Mukherjee, A., Peralta-Videa, J.R., Bandyopadhyay, S., Rico, C.M., Zhao, L., Gardea-Torresdey, J.L.: Physiological effects of nanoparticulate ZnO in green peas (Pisum sativum L.) cultivated in soil. - Metallomics 132: 132-138, 2014b. Go to original source...
    34. Nakano, Y., Asada, K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. - Plant Cell Physiol. 867: 867-880, 1981.
    35. Nel, A., Xia, T., Mädler, L., Li, N.: Toxic potential of materials at the nanolevel. - Science 622: 622-627, 2006. Go to original source...
    36. Panda, S.K., Choudhury, S.: Chromium stress in plants. - Braz. J. Plant Physiol. 95: 95-102, 2005. Go to original source...
    37. Parsons, J.G., Lopez, M.L., Gonzalez, C.M., Peralta-Videa, J.R., Gardea-Torresdey, J.L.: Toxicity and biotransformation of uncoated and coated nickel hydroxide nanoparticles on mesquite plants. - Environ. Toxicol. Chem. 1146: 1146-1154, 2010. Go to original source...
    38. Priyanka, N., Venkatachalam, P.: Biofabricated zinc oxide nanoparticles coated with phycomolecules as novel micronutrient catalysts for stimulating plant growth of cotton. - Adv. nat. Sci. Nanosci. Nanotechnol. 045018: 045018, 2016. Go to original source...
    39. Schwab, F., Zhai, G., Kern, M., Turner, A., Schnoor, J.L., Wiesner, M.R.: Barriers, pathways and processes for uptake, translocation and accumulation of nanomaterials in plants-critical review. - Nanotoxicology 257: 257-278, 2016. Go to original source...
    40. Schreiber, U., Schliwa, U., Bilger, W.: Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. - Photosynth. Res. 51: 51-62, 1986. Go to original source...
    41. Stampoulis, D., Sinha, S.K., White, J.C.: Assay-dependent phytotoxicity of nanoparticles to plants. - Environ. Sci. Technol. 9473: 9473-9479, 2009. Go to original source...
    42. Stewart, R.R., Bewley, J.D.: Lipid peroxidation associated with accelerated aging of soybean axes. - Plant Physiol. 245: 245-248, 1980. Go to original source...
    43. Szabó, T., Németh, J., Dékány, I.: Zinc oxide nanoparticles incorporated in ultrathin layer silicate films and their photocatalytic properties. - Colloid Surface. A: Physicochem. Eng. Aspects 23: 23-35, 2003. Go to original source...
    44. Takahashi, F., Mizoguchi, T., Yoshida, R., Ichimura, K., Shinozaki, K.: Calmodulin-dependent activation of MAP kinase for ROS homeostasis in Arabidopsis. - Mol. Cell 41, 649-660, 2011. Go to original source...
    45. Thwala, M., Musee, N., Sikhwivhilu, L., Wepener, V.: The oxidative toxicity of Ag and ZnO nanoparticles towards the aquatic plant Spirodela punctuta and the role of testing media parameters. - Environ. Sci. Process. Impact. 1830: 1830-1843, 2013. Go to original source...
    46. Tso, C.P., Zhung, C.M., Shih, Y.H., Tseng, Y.M., Wu, S.C., Doong, R.A.: Stability of metal oxide nanoparticles in aqueous solutions. - Water Sci. Technol. 127: 127-133, 2010. Go to original source...
    47. Wang, P., Menzies, N.W., Lombi, E., McKenna, B.A., Johannessen, B., Glover, C.J., Kappen, P., Kopittke, P.M.: Fate of ZnO nanoparticles in soils and cowpea (Vigna unguiculata). - Environ. Sci. Technol. 13822: 13822-13830, 2013. Go to original source...
    48. Wang, X.P., Jiang, P., Ma, Y., Geng, S.J., Wang, S.C., Shi, D.C.: Physiological strategies of sunflower exposed to salt or alkali stresses: restriction of ion transport in the cotyledon node zone and solute accumulation. - Agron. J. 2181: 2181-2192, 2015. Go to original source...
    49. Whiteside, M.D., Treseder, K.K., Atsatt, P.R.: The brighter side of soils: quantum dots track organic nitrogen through fungi and plants. - Ecology 100: 100-108, 2009. Go to original source...
    50. Wild, E., Jones, K.C.: Novel method for the direct visualization of in vivo nanomaterials and chemical interactions in plants. - Environ. Sci. Technol. 5290: 5290-5294, 2009. Go to original source...
    51. Yang, Z.Z., Chen, J., Dou, R.Z., Gao, X., Mao, C.B., Wang, L.: Assessment of the phytotoxicity of metal oxide nanoparticles on two crop plants, maize (Zea mays L.) and rice (Oryza sativa L.). - Int. J. Environ. Res. Public Health 15100: 15100-15109, 2015. Go to original source...
    52. Yoon, S.J., Kwak, J.I., Lee, W.M., Holden, P.A., An, Y.J.: Zinc oxide nanoparticles delay soybean development: A standard soil microcosm study. - Ecotoxicol. Environ. Safety 131: 131-137, 2014. Go to original source...
    53. Zhao, L., Hernandez-Viezcas, J.A., Perlata-Videa, J.R., Bandyopadhyay, S., Peng, B., Munoz, B., Keller, A.A., Gardea- Torresdey, J.L.: ZnO nanoparticle fate in soil and zinc bioaccumulation in corn plants (Zea mays) influenced by alginate. - Environ. Sci. Process. Impact. 260: 260-266, 2013a. Go to original source...
    54. Zhao, L., Sun, Y., Hernandez-Viezcas, J.A., Servin, A.D., Hong, J., Niu, G., Peralta-Videa, J.R., Duarte-Gardea, M., Gardea- Torresdey, J.L.: Influence of CeO2 and ZnO nanoparticles on cucumber physiological markers and bioaccumulation of Ce and Zn: a life cycle study. - J. Agr. Food Chem. 11945: 11945-11951, 2013b. Go to original source...

    Return to the content