Environmental Science and Pollution Research

, Volume 22, Issue 3, pp 1841–1853 | Cite as

Uptake and translocation of metals and nutrients in tomato grown in soil polluted with metal oxide (CeO2, Fe3O4, SnO2, TiO2) or metallic (Ag, Co, Ni) engineered nanoparticles

  • Livia Vittori Antisari
  • Serena CarboneEmail author
  • Antonietta Gatti
  • Gilmo Vianello
  • Paolo Nannipieri
Research Article


The influence of exposure to engineered nanoparticles (NPs) was studied in tomato plants, grown in a soil and peat mixture and irrigated with metal oxides (CeO2, Fe3O4, SnO2, TiO2) and metallic (Ag, Co, Ni) NPs. The morphological parameters of the tomato organs, the amount of component metals taken up by the tomato plants from NPs added to the soil and the nutrient content in different tomato organs were also investigated. The fate, transport and possible toxicity of different NPs and nutrients in tomato tissues from soils were determined by inductively coupled plasma-optical emission spectrometry (ICP-OES). The tomato yield depended on the NPs: Fe3O4-NPs promoted the root growth, while SnO2-NP exposure reduced it (i.e. +152.6 and −63.1 % of dry matter, respectively). The NP component metal mainly accumulated in the tomato roots; however, plants treated with Ag-, Co- and Ni-NPs showed higher concentration of these elements in both above-ground and below-ground organs with respect to the untreated plants, in addition Ag-NPs also contaminated the fruits. Moreover, an imbalance of K translocation was detected in some plants exposed to Ag-, Co- and Fe3O4-NPs. The component metal concentration of soil rhizosphere polluted with NPs significantly increased compared to controls, and NPs were detected in the tissues of the tomato roots using electron microscopy (ESEM-EDS).


Nanoparticles Tomato (Lycopersicon esculentum Mill.) Pollution Translocation Electron microscopy Inductively coupled plasma-optical emission spectrometry 



This study was supported by the INESE project funded by the Italian Institute of Technology (IIT, Genoa, Italy).


  1. American Society for Testing and Materials (2006) Standard terminology relating to nanotechnology. E 2456–06. West Conshohocken, PAGoogle Scholar
  2. Anjum N, Gill S, Duarte A, Pereira E, Ahmad I (2013) Silver nanoparticles in soil-plant systems. J Nanoparticle Res 15(1896):1–26. doi: 10.1007/s11051-013-1896-7 Google Scholar
  3. Ball AS, Shah D, Wheatley CF (2000) Assessment of the potential of a newspaper/horse manure-based compost. Bioresour Technol 73:163–167. doi: 10.1016/S0960-8524(99)00169-8 CrossRefGoogle Scholar
  4. Ben-Moshe T, Dror I, Berkowitz B (2010) Transport of metal oxide nanoparticles in saturated porous media. Chemosphere 81:387–393. doi: 10.1016/j.chemosphere.2010.07.007 CrossRefGoogle Scholar
  5. Birbaum K, Brogioli R, Schellenberg M, Martinoia E, Stark WJ, Günther D, Limbach LK (2010) No evidence for cerium dioxide nanoparticle translocation in maize plants. Environ Sci Technol 44:8718–8723. doi: 10.1021/es101685f CrossRefGoogle Scholar
  6. British Standards Institution (2007) Terminology for nanomaterials. PAS 136: 2007. London, UKGoogle Scholar
  7. Carvajal M, Cerda A, Martnez V (2000) Does calcium ameliorate the negative effect of NaCl on melon root water transport by regulating aquaporing activity? New Phytol 145:439–441CrossRefGoogle Scholar
  8. Carvalho Bertoli CA, Cannata MG, Carvalho R, Ribeiro Bastos AR, Freitas MP, dos Santos A (2012) Lycopersicon esculentum submitted to Cd-stressful conditions in nutrition solution: nutrient contents and translocation. Ecotoxicol Environ Saf 86:176–181. doi: 10.1016/j.ecoenv.2012.09.011 CrossRefGoogle Scholar
  9. Dimkpa CO, McLean JE, Britt DW, Anderson AJ (2012) Bioactivity and biomodification of Ag, ZnO, and CuO nanoparticles with relevance to plant performance in agriculture (Review). Ind Biotechnol 8:344–357CrossRefGoogle Scholar
  10. Dimkpa CO, McLean JE, Martineau N, Britt DW, Haverkamp R, Anderson AJ (2013) Silver nanoparticles disrupt wheat (Triticum aestivum L.) growth in a sand matrix. Environ Sci Technol 47:1082–1090. doi: 10.1021/es302973y CrossRefGoogle Scholar
  11. Dinesh R, Anandaraj M, Srinivasan V, Hamza S (2012) Engineered nanoparticles in the soil and their potential implications to microbial activity. Geoderma 173–174:19–27. doi: 10.1016/j.geoderma.2011.12.018 CrossRefGoogle Scholar
  12. Dong J, Wu F, Zhang G (2006) Influence of cadmium on antioxidant capacity and four microelement concentrations in tomato seedlings (Lycopersicon esculentum). Chemosphere 64:1659–1666. doi: 10.1016/j.chemosphere.2006.01.030 CrossRefGoogle Scholar
  13. Du W, Sun Y, Ji R, Zhu J, Wu J, Guo H (2011) TiO2 and ZnO nanoparticles negatively affect wheat growth and soil enzyme activities in agricultural soil. J Environ Monit 13:822–828. doi: 10.1039/C0EM00611D CrossRefGoogle Scholar
  14. El-Temsah YS, Joner EJ (2010) Impact of Fe and Ag nanoparticles on seed germination and differences in bioavailability during exposure in aqueous suspension and soil. Environ Toxicol 27:42–49. doi: 10.1002/tox.20610 CrossRefGoogle Scholar
  15. Farré M, Sanchís J, Barceló D (2011) Analysis and assessment of the occurrence, the fate and the behavior of nanomaterials in the environment. TrAC Trends Anal Chem 30:517–527. doi: 10.1186/2190-4715-24-5 CrossRefGoogle Scholar
  16. Fernandes JC, Henriques FS (1991) Biochemical, physiological, and structural effects of excess copper in plants. Bot Rev 57:246–273. doi: 10.1007/BF02858564 CrossRefGoogle Scholar
  17. Gardea-Torresdey JL, Rico CM, White JC (2014) Trophic transfer, transformation, and impact of engineered nanomaterials in terrestrial environments. Environ Sci Technol 48:2526–2540. doi: 10.1021/es4050665 CrossRefGoogle Scholar
  18. Geisler-Lee J, Wang Q, Yao Y, Zhang W, Geisler M, Li K, Huang Y, Chen Y, Kolmakov A, Ma X (2013) Phytotoxicity, accumulation and transport of silver nanoparticles by Arabidopsis thaliana. Nanotoxicology 3:323–337. doi: 10.3109/17435390.2012.658094 CrossRefGoogle Scholar
  19. Gottschalk F, Sonderer T, Scholz RW, Nowack B (2009) Modeled environmental concentrations of engineered nanomaterials (TiO2, ZnO, Ag, CNT, Fullerenes) for different regions. Environ Sci Technol 43:9216–9222. doi: 10.1021/es9015553 CrossRefGoogle Scholar
  20. Hernandez-Viezcas JA, Castillo-Michel H, Andrews JC, Cotte M, Rico C, Peralta-Videa JR, Ge Y, Priester JH, Holden PA, Gardea-Torresdey JL (2013) In situ synchrotron x-ray fluorescence mapping and speciation of CeO2 and ZnO nanoparticles in soil cultivated soybean (Glycine max). ACS Nano 7:1415–1423CrossRefGoogle Scholar
  21. Kim YH, Kim CY, Song WK, Park DS, Kwon SY, Lee HS, Bang HW, Kwak SS (2008) Over expression of sweet potato swpa4 peroxidase results in increased hydrogen peroxide production and enhances stress tolerance in tobacco. Planta 227:867–881. doi: 10.1007/s00425-007-0663-3 CrossRefGoogle Scholar
  22. Kumari M, Mukherjee A (2009) Genotoxicity of silver nanoparticle in Allium cepa. Sci Total Environ 407:5243–5246. doi: 10.1016/j.scitotenv.2009.06.024 CrossRefGoogle Scholar
  23. Larbi A, Morales F, Abadía A, Gogorcena Y, Lucena JJ, Abadía J (2002) Effects of Cd and Pb in sugar beet plants grown in nutrient solution: induced Fe deficiency and growth inhibition. Funct Plant Biol 29:1453–64CrossRefGoogle Scholar
  24. 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. doi: 10.1897/07-481.1 CrossRefGoogle Scholar
  25. Lee CW, Mahendra S, Zodrow K, Li D, Tsai YC, Braam J, Alvarez PJJ (2010) Developmental phytotoxicity of metal oxide nanoparticles to Arabidopsis thaliana. Environ Toxicol Chem 29:669–675. doi: 10.1002/etc.58 CrossRefGoogle Scholar
  26. Lee WM, Kwak JI, An YJ (2012) Effect of silver nanoparticles in crop plants Phaseolus radiatus and Sorghum bicolor: media effect on phytotoxicity. Chemosphere 86:491–499. doi: 10.1016/j.chemosphere2011.10.013 CrossRefGoogle Scholar
  27. Levent Tuna A, Kaya C, Ashraf M, Altunlu H, Yokas I, Yagmur B (2007) The effects of calcium sulphate on growth, membrane stability and nutrient uptake of tomato plants grown under salt stress. Environ Exp Bot 59:173–178CrossRefGoogle Scholar
  28. Lin D, Xing B (2007) Phytotoxicity of nanoparticles: inhibition of seed germination and root growth. Environ Pollut 150:243–250. doi: 10.1016/j.envpol.2007.01.016 CrossRefGoogle Scholar
  29. Lopez-Moreno ML, De La Rosa G, Hernandez-Viezcas JA, Peralta-Videa JR, Gardea-Torresdey JL (2010) X-ray adsorption spectroscopy (XAS) corroboration of the uptake and storage of CeO2 nanoparticles and assessment of their differential toxicity in four edible plant species. J Agric Food Chem 58:3689–3693. doi: 10.1021/jf904472e CrossRefGoogle Scholar
  30. Mandeh M, Omidi M, Rahaie M (2012) In vitro influences of TiO2 nanoparticles on barley (Hordeum vulgare L.) tissue culture. Biol Trace Elem Res 150:376–80. doi: 10.1007/s12011-012-9480-z CrossRefGoogle Scholar
  31. Ouzounidou G, Asfi M, Sotirakis N, Papadopoulou P, Gaitis F (2008) Olive mill wastewater triggered changes in physiology and nutritional quality of tomato (Lycopersicon esculentum Mill.) depending on growth substrate. J Hazard Mater 158:523–530. doi: 10.1016/j.tcb.2009.07.004 CrossRefGoogle Scholar
  32. Paiva HN, Carvalho JG, Siqueira JO (2002) Índice de translocação de nutrientes em mudas de cedro (Cedrela fissilis Vell.) e de ipê-roxo (Tabebuia impetiginosa Mart. Standl.) submetidas a doses crescentes de cádmio, níquel e chumbo. Rev Tree 26:467–473Google Scholar
  33. Pidgeon N, Harthorn BH, Bryant K, Rogers-Hayden T (2009) Deliberating the risks of nanotechnologies for energy and health applications in the United States and United Kingdom. Nat Nanotechnol 4:95–98. doi: 10.1038/nnano.2008 CrossRefGoogle Scholar
  34. Priester JH, Ge Y, Mielke RE, Horst AM, Cole Moritz S, Espinosa K, Gelb J, Walkerg SL, Nisbet RM, Ani YJ, Schimel JP, Palmer RG, Hernandez-Viezcas JA, Zhao L, Gardea-Torresdey JL, Holden PA (2012) Soybean susceptibility to manufactured nanomaterials with evidence for food quality and soil fertility interruption. PNAS Plus. doi: 10.1073/pnas.1205431109 Google Scholar
  35. Remédios C, Rosário F, Bastos V (2012) Environmental nanoparticles interaction with plants: morphological, physiological and genotoxic aspects. J Bot 751686:8. doi: 10.1155/2012/751686 Google Scholar
  36. 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 Agric Food Chem 59:485–3498. doi: 10.1021/jf104517j CrossRefGoogle Scholar
  37. Rico CM, Morales MI, McCreary R, Castillo-Michel H, Barrios AC, Hong J, Tafoya A, Lee W-Y, Varela-Ramirez A, Peralta-Videa JR, Gardea-Torresdey JL (2013a) Cerium oxide nanoparticles modify the antioxidative stress enzyme activities and macromolecule composition in rice seedlings. Environ Sci Technol 47:14110–14118. doi: 10.1021/es4033887 CrossRefGoogle Scholar
  38. Rico CM, Morales MI, Barrios AC, McCreary R, Hong J, Lee W-Y, Nunez J, Peralta-Videa JR, Gardea-Torresdey JL (2013b) Effect of cerium oxide nanoparticles on the quality of rice (Oryza sativa L.) grains. J Agric Food Chem 61:11278–11285. doi: 10.1021/jf404046v CrossRefGoogle Scholar
  39. Ruffini Castiglione M, Giorgetti L, Geri C, Cremonini N (2011) The effects of nano-TiO2 on seed germination development and mitosis of root tip cells of Vicia narborensis L., and Zea mays L. J Nanoparticle Res 13:2443–2449. doi: 10.1007/s11051-010-0135-8 CrossRefGoogle Scholar
  40. Schwabe F, Schulin R, Limbach LK, Stark W, Bürge D (2013) Influence of two types of organic matter on interaction of CeO2 nanoparticles with plants in hydroponic culture. Chemosphere 91:512–520. doi: 10.1016/j.chemosphere.2012 CrossRefGoogle Scholar
  41. Scientific Committee on Emerging and Newly Identified Health Risks (2007) The appropriateness of the risk assessment methodology in accordance with the Technical Guidance. Documents for new and existing substances for assessing the risks of nanomaterials, 21–22 June 2007. European Commission, Brussels, BelgiumGoogle Scholar
  42. Servin AD, Castillo-Michel H, Hernandez-Viezcas JA, Diaz BC, Peralta-Videa JR, Gardea-Torresdey JL (2012) Synchrotron micro-XRF and micro-XANES confirmation of the uptake and translocation of TiO2 nanoparticles in cucumber (Cucumis sativus) plants. Environ Sci Technol 46:7637–7643. doi: 10.1021/es300955b CrossRefGoogle Scholar
  43. Servin AD, Morales MI, Castillo-Michel H, Hernandez-Viezcas JA, Munoz B, Zhao L, Nunez JE, Peralta-Videa JR, Gardea-Torresdey JL (2013) Synchrotron verification of TiO2 accumulation in cucumber fruit: a possible pathway of TiO2 nanoparticle transfer from soil into the food chain. Environ Sci Technol 47:11592–11598. doi: 10.1021/es403368j CrossRefGoogle Scholar
  44. Sheykhbaglou R, Sedghi M, Tajbakhsh Shishvan M, Seyed Sharifi R (2010) Effect of nano-iron particles on agronomic traits of soybean. Not Sci Biol 2:112–113Google Scholar
  45. Song U, Jun H, Waldman B, Roh J, Kim Y, Yi J, Lee EJ (2013) Functional analyses of nanoparticle toxicity: a comparative study of the effects of TiO2 and Ag on tomatoes (Lycopersicon esculentum). Ecotoxicol Environ Saf 93:60–67. doi: 10.1016/j.ecoenv.2013.03.033 CrossRefGoogle Scholar
  46. Stampoulis D, Sinha SK, White JC (2009) Assay-dependent phytotoxicity of nanoparticles in plants. Environ Sci Technol 43:9473–9479. doi: 10.1021/es901695c CrossRefGoogle Scholar
  47. Taiz L, Zeiger E (1998) Plant physiology, 2nd edn. Sinauer Associates, SunderlandGoogle Scholar
  48. Trujillo-Reyes J, Majumdar S, Botez CE, Peralta-Videa JR, Gardea-Torresdey JL (2014) Exposure studies of core-shell Fe/Fe3O4 and Cu/CuO NPs to lettuce (Lactuca sativa) plants: are they a potential physiological and nutritional hazard? J Hazard Mater 267:255–263. doi: 10.1016/j.jhazmat.2013.11.067 CrossRefGoogle Scholar
  49. Turpault MP (2006) Sampling of rhizosphere soil for physico-chemical and mineralogical analyses by physical separation based on drying and shaking. In: Luster J, Finlay R (eds) Handbook of methods used in rhizosphere research. Swiss Federal Research Institute WSL, Birmensdorf, pp 196–197Google Scholar
  50. United States Environmental Protection Agency (USEPA) (2009) Test methods for evaluating solid waste: physical/chemical methods. USEPA, Washington, DC, USA. (SW-846, 3)Google Scholar
  51. Vittori Antisari L, Carbone S, Ferronato C, Simoni A, Vianello G (2011a) Characterization of heavy metals atmospheric deposition for assessment of urban environmental quality in the Bologna city (Italy). EQA 7:49–63. doi: 10.6092/issn.2281-4485/3834 Google Scholar
  52. Vittori Antisari L, Carbone S, Fabrizi A, Gatti A, Vianello G (2011b) Response of soil microbial biomass to CeO2. EQA 7:1–16. doi: 10.6092/issn.2281-4485/3829 Google Scholar
  53. Vittori Antisari L, Carbone S, Gatti A, Fabrizi A, Vianello G (2012) Toxicological effects of engineered nanoparticles on earthworms (Lumbricus rubellus) in short exposure. EQA 8:51–60. doi: 10.6092/issn.2281-4485/3750 Google Scholar
  54. Vittori Antisari L, Carbone S, Gatti A, Vianello G, Nannipieri P (2013) Toxicity of metal oxide (CeO2, Fe3O4, SnO2) engineered nanoparticles on soil microbial biomass and their distribution in soil. Soil Biol Biochem 60:87–94. doi: 10.1016/j.soilbio.2013.01.016 CrossRefGoogle Scholar
  55. Wang S, Kurepa J, Smalle JA (2011) Ultra-small TiO2 nanoparticles disrupt microtubular networks in Arabidopsis thaliana. Plant Cell Environ 34:811–20. doi: 10.1111/j.1365-3040.2011.02284.x CrossRefGoogle Scholar
  56. Wang Q, Ma X, Zhang W, Pei H, Chen Y (2012) The impact of cerium oxide nanoparticles on tomato (Solanum lycopersicum L.) and its implications for food safety. Metallomics 4:1105–1112. doi: 10.1039/c2mt20149f CrossRefGoogle Scholar
  57. Wang J, Koo Y, Alexander A, Yang Y, Westerhof S, Zhang Q, Schnoor JL, Colvin VL, Braam J, Alvarez PJ (2013) Phytostimulation of poplars and Arabidopsis exposed to silver nanoparticles and Ag+ at sublethal concentrations. Environ Sci Technol 47:5442–5449. doi: 10.1021/es4004334 CrossRefGoogle Scholar
  58. Wu J, Qui H, Yang G, Dong B, Gu H (2003) Nutrient uptake of rice roots in response to infestation of Nilaparvata lugens (Stal) (Homoptera: Delphacidae). J Econ Entomol 96:1798–804CrossRefGoogle Scholar
  59. Yang L, Watts DJ (2009) Particle surface characteristics may play an important role in phytotoxicity of allumina nanoparticles. Toxicol Lett 158:122–132. doi: 10.1016/j.toxlet.2005.03.003 CrossRefGoogle Scholar
  60. Zhang Z, He X, Zhang H, Ma Y, Zhang P, Ding Y, Zhao Y (2011) Uptake and distribution of ceria nanoparticles in cucumber plants. Metallomics 3:816–822. doi: 10.1039/C1MT00049G CrossRefGoogle Scholar
  61. Zhao L, Videa JRP, Ramirez AV, Castillo-Michel H, Li C, Zhang J, Aguilera RJ, Keller AA, Torresdey JLG (2012) Effect of surface coating and organic matter on the uptake of CeO2 NPs by corn plants grown in soil: insight into the uptake mechanism. J Hazard Mater 225–226:131–138. doi: 10.1016/j.jhazmat.2012.05.008 CrossRefGoogle Scholar
  62. Zhu H, Han J, Xiao JQ, Jin Y (2008) Uptake, translocation, and accumulation of manufactured iron oxide nanoparticles by pumpkin plants. J Environ Monit 10:713–717. doi: 10.1039/b805998e CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Livia Vittori Antisari
    • 1
  • Serena Carbone
    • 1
    Email author
  • Antonietta Gatti
    • 2
  • Gilmo Vianello
    • 1
  • Paolo Nannipieri
    • 3
  1. 1.Dipartimento di Scienze Agrarie, Alma Mater StudiorumUniversità di BolognaViale Fanin 40Italy
  2. 2.NanodiagnosticsSan Vito di SpilambertoItaly
  3. 3.Dipartimento di Scienze Delle Produzioni Agroalimentari e Dell’AmbienteUniversità di FirenzeFlorenceItaly

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