Skip to main content
Log in

Effects of Stabilized Nanoparticles of Copper, Zinc, Manganese, and Iron Oxides in Low Concentrations on Lettuce (Lactuca sativa) Seed Germination: Nanotoxicants or Nanonutrients?

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript


Information on the phytotoxicity of nanoparticles (NPs) at low concentrations (e.g., ppb to low ppm) is scarce. Therefore, this study was conducted to assess the effects of laboratory-prepared Cu, Zn, Mn, and Fe oxide NPs in low concentrations (<50 ppm) on the germination of lettuce (Lactuca sativa) seeds in a water medium. The data showed that CuO NPs were slightly more toxic than Cu ions while the toxicity of ZnO NPs was similar to that of Zn ions, and MnOx NPs and FeOx NPs were not only less toxic than their ionic counterparts but also significantly stimulated the growth of lettuce seedlings by 12–54 %. This study showed that manufactured NPs were not always more toxic than other chemical species containing the same elements. Instead, Mn or Fe NPs can significantly enhance plant growth and have the potential to be effective nanofertilizers for increasing agronomic productivity.

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

Similar content being viewed by others


  • Adams, L. K., Lyon, D. Y., & Alvarez, P. J. (2006). Comparative eco-toxicity of nanoscale TiO2, SiO2, and ZnO water suspensions. Water Research, 40, 3527–3532.

    Article  CAS  Google Scholar 

  • Auffan, M., Rose, J., Bottero, J. Y., Lowry, G. V., Jolivet, J. P., & Wiesner, M. R. (2009). Towards a definition of inorganic nanoparticles from an environmental, health and safety perspective. Nature Nanotechnology, 4, 634–641.

    Article  CAS  Google Scholar 

  • Bowers, N., Pratt, J. R., Beeson, D., & Lewis, M. (1997). Comparative evaluation of soil toxicity using lettuce seeds and soil ciliates. Environmental Toxicology & Chemistry, 16, 207–213.

  • Delfani, M., Firouzabadi, M. B., Farrokhi, N., & Makarian, H. (2014). Some physiological responses of black-eyed pea to iron and magnesium nanofertilizers. Communication in Soil Science and Plant Analysis, 45, 530–540.

    Article  CAS  Google Scholar 

  • Dimkpa, C. O., McLean, J. E., Latta, D. E., Manangón, E., Britt, D. W., Johnson, W. P., Boyanov, M. I., & Anderson, A. J. (2012). CuO and ZnO nanoparticles: phytotoxicity, metal speciation, and induction of oxidative stress in sand-grown wheat. Journal of Nanoparticle Research, 14, 1125–1140.

    Article  CAS  Google Scholar 

  • Dixon, J. B., & White, G. N. (2002). Manganese oxides. In J. B. Dixon & D. G. Schulze (Eds.), Soil Mineralogy with Environmental Applications (pp. 367–388). Madison: Soil Science Society of America.

    Google Scholar 

  • Downs, R.T. (2006). The RRUFF Project: an integrated study of the chemistry, crystallography, Raman and infrared spectroscopy of minerals. Program and Abstracts of the 19th General Meeting of the International Mineralogical Association in Kobe, Japan. O03-13.,%20O/display=default/R060027. Accessed on 27 March 2015.

  • Fabricius, A.-L., Duester, L., Meermann, B., & Ternes, T. A. (2014). ICP-MS-based characterization of inorganic nanoparticles—sample preparation and off-line fractionation strategies. Analytical and Bioanalytical Chemistry, 406, 467–479.

    Article  CAS  Google Scholar 

  • Fageria, N. K. (2009). The use of nutrients in crop plants. Boca Raton, FL: CRC Press.

  • Feng, X., Liu, F., Tan, W., & Liu, X. (2004). Synthesis of birnessite from the oxidation of Mn2+ by O2 in alkali medium: effects of synthesis conditions. Clay and Clay Minerals, 52, 240–250.

    Article  CAS  Google Scholar 

  • Ghafariyan, M. H., Malakouti, M. J., Dadpour, M. R., Stroeve, P., & Mahmoudi, M. (2013). Effects of magnetite nanoparticles on soybean chlorophyll. Environmental Science & Technology, 47, 10645–10652.

    CAS  Google Scholar 

  • Gottschalk, F., Sun, T., & Nowak, B. (2013). Environmental concentrations of engineered nanomaterials: review of modeling and analytical studies. Environmental Pollution, 181, 287–300.

    Article  CAS  Google Scholar 

  • Hoagland, D. R., & Arnon, D. I. (1950). The water-culture method for growing plants without soil. California Agriculture Experiment Stat Circular, 347, 1–32. Accessed on 20 January 2015.

    Google Scholar 

  • Horie, M., Fujita, K., Kato, H., Endoh, S., Nishio, K., Komaba, L. K., Nakamura, A., Miyauchi, A., Kinugasa, H., Hagihara, Y., Niki, E., Yoshida, Y., & Iwahashi, H. (2012). Association of the physical and chemical properties and the cytotoxicity of metal oxide nanoparticles: metal ion release, adsorption ability and specific surface area. Metallomics, 4, 350–360.

    Article  CAS  Google Scholar 

  • Karlsson, H. L., Cronholm, P., Gustafsson, J., & Möller, L. (2008). Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. Chemical Research in Toxicology, 21, 1726–1732.

    Article  CAS  Google Scholar 

  • Kaweeteerawat, C., Ivask, A., Liu, R., Zhang, H., Chang, C. H., Low-Kam, C., Fischer, H., Ji, Z., Pokhrel, S., Cohen, Y., Telesca, D., Zink, J., Mädler, L., Holden, P. A., & Godwin, H. (2015). Toxicity of metal oxide nanoparticles in Escherichia coli correlates with conduction band and hydration energies. Environmental Science & Technology, 49, 1105–1112.

    Article  CAS  Google Scholar 

  • Kopittke, P. M., Blamey, F. P. C., Asher, C. J., & Menzies, N. W. (2010). Trace metal phytotoxicity in solution culture: a review. Journal of Experimental Botany, 61, 945–954.

    Article  CAS  Google Scholar 

  • Lee, S., Chung, H., Kim, S., & Lee, I. (2013). The genotoxic effect of ZnO and CuO nanoparticles on early growth of buckwheat Fagopyrum esculentum. Water Air Soil Pollution, 224, 1668–1678.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Liu, R., & Lal, R. (2014). Synthetic apatite nanoparticles as a phosphorus fertilizer for soybean (Glycine max). Scientific Reports, 4(5686), 1–6.

    Google Scholar 

  • Liu, R., & Lal, R. (2015). Potentials of engineered nanoparticles as fertilizers for increasing agronomic productions. Science of the Total Environment, 514, 131–139.

    Article  CAS  Google Scholar 

  • Ma, H., Williams, P. L., & Diamond, S. A. (2013). Ecotoxicity of manufactured ZnO nanoparticles—a review. Environmental Pollution, 172, 76–85.

    Article  CAS  Google Scholar 

  • Mahajan, P., Dhoke, S. K., & Khanna, A. S. (2011). Effect of nano-ZnO particle suspension on growth of mung (Vigna radiata) and gram (Cicer arietinum) seedlings using plant agar method. Journal of Nanotechnology, 696535, 1–7. doi:10.1155/2011/696535.

    Article  CAS  Google Scholar 

  • Montgomery, D. C. (2009). Design and analysis of experiments (7th ed.). New York, NY: John Wiley & Sons.

  • Navarro, E., Baun, A., Behra, R., Hartmann, N. B., Filser, J., Miao, A. J., Quigg, A., Santschi, P. H., & Sigg, L. (2008). Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology, 17, 372–386.

    Article  CAS  Google Scholar 

  • Peng, C., Duan, D., Xu, C., Chen, Y., Sun, L., Zhang, H., Yuan, X., Zheng, L., Yang, Y., Yang, J., Zhen, X., Chen, Y., & Shi, J. (2015). Translocation and biotransformation of CuO nanoparticles in rice (Oryza sativa L.) plants. Environmental Pollution, 197, 99–107.

  • Phu, N. D., Ngo, D. T., Hoang, L. H., Luong, N. H., Chau, N., & Hai, N. H. (2011). Crystallization process and magnetic properties of amorphous iron oxide nanoparticles. Journal of Physics D: Applies Physics, 44(345002), 1–7. doi:10.1088/0022-3727/44/34/345002.

    Google Scholar 

  • Portehault, D., Cassaignon, S., Baudrinc, E., & Jolivet, J. P. (2009). Structural and morphological control of manganese oxide nanoparticles upon soft aqueous precipitation through MnO4 /Mn2+ reaction. Journal of Materials Chemistry, 19, 2407–2416.

    Article  CAS  Google Scholar 

  • Pradhan, S., Patra, P., Das, S., Chandra, S., Mitra, S., Dey, K. K., Akbar, S., Palit, P., & Goswami, A. (2013). Photochemical modulation of biosafe manganese nanoparticles on Vigna radiata: a detailed molecular, biochemical, and biophysical study. Environmental Science & Technology, 47, 13122–13131.

    Article  CAS  Google Scholar 

  • Roco, M. C. (2011). The long view of nanotechnology development: the national nanotechnology initiative at 10 years. Journal of Nanoparticle Research, 13, 427–445.

    Article  Google Scholar 

  • Servin, A., Elmer, W., Mukherjee, A., Torre-Roche, R. D., Hamdi, H., White, J. C., Bindraban, P., & Dimkpa, C. (2015). A review of the use of engineered nanomaterials to suppress plant disease and enhance crop yield. Journal of Nanoparticle Research, 17, 92–112.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • USEPA—United State Environmental Protection Agency (2013). Secondary drinking water regulations: guidance for nuisance chemicals secondarystandards.cfm. Accessed on 06 April 2015.

  • USEPA—United State Environmental Protection Agency (2015). EPA is now distributing BMDS 2.6. Accessed on 03/26/2015.

  • Wu, S. G., Huang, L., Head, J., Chen, D. R., Kong, I. C., & Tang, Y. J. (2012). Phytotoxicity of metal oxide nanoparticles is related to both dissolved metals ions and adsorption of particles on seed surfaces. Journal of Petroleum & Environmental Biotechnology, 3, 126–130.

    CAS  Google Scholar 

  • Zhang, Y., Sun, C., Lu, P., Li, K., Song, S., & Xue, D. (2012). Crystallization design of MnO2 towards better supercapacitance. CrystEngComm, 14, 5892–5897.

    Article  CAS  Google Scholar 

  • Zhang, D., Hua, T., Xiao, F., Chen, C., Gersberg, R. M., Liu, Y., Stuckey, D., Ng, W. J., & Tan, S. K. (2015). Phytotoxicity and bioaccumulation of ZnO nanoparticles in Schoenoplectus tabernaemontani. Chemosphere, 120, 211–219.

    Article  CAS  Google Scholar 

  • 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. (2013). Influence of CeO2 and ZnO nanoparticles on cucumber physiological markers and bioaccumulation of Ce and Zn: A life cycle study. Journal of Agricultural and Food Chemistry, 61, 11945–11951.

Download references


This study was partly funded by Hechi University Start-Up Grant (XJ2015KQ006) awarded to Dr. Huying Zhang. The authors greatly appreciate Ms. Audrey McCray and Mr. Chris Eidson’s help with manuscript preparation.

Author information

Authors and Affiliations


Corresponding author

Correspondence to Huiying Zhang.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.


(DOC 317 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, R., Zhang, H. & Lal, R. Effects of Stabilized Nanoparticles of Copper, Zinc, Manganese, and Iron Oxides in Low Concentrations on Lettuce (Lactuca sativa) Seed Germination: Nanotoxicants or Nanonutrients?. Water Air Soil Pollut 227, 42 (2016).

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: