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Environmental Science and Pollution Research

, Volume 23, Issue 2, pp 1732–1741 | Cite as

Root water transport of Helianthus annuus L. under iron oxide nanoparticle exposure

  • Domingo Martínez-Fernández
  • Didac Barroso
  • Michael Komárek
Research Article

Abstract

The application of nanomaterials in commercially available products is increasing rapidly for agriculture, phytoremediation and biotechnology. Since plants suppose the first sink for the accumulation of nanoparticles from the environment, emerging studies have focused on the general consequences for plants and their effects on the biomass production. However, effects on the root surface, as well as blockage of nutrients and water uptake by the roots, may also occur. This experiment was designed to prove if the plant water relations can be affected by the adsorption of nanoparticles on the root surface, causing a consequent stress for the plants. With this goal, plants of Helianthus annuus were previously grown in a hydroponic culture, and at age of 55 days, their roots were exposed to three different concentrations of nanomaghemite (NM) in the hydroponic solution for 5 days: control without NM; 50 and 100 mg l−1 NM. The main effect was related to the reduction of the root hydraulic conductivity (L o ) and the nutrients uptake. The concentrations of the macronutrients Ca, K, Mg and S in the shoot were reduced relative to the control plants, which resulted in lower contents of chlorophyll pigments. Although stress was not detected in the plants, after the analysis of stress markers like the accumulation of proline or ascorbate in the tissues, reduction of the root functionality by nanoparticles has been identified here, manifested as the effect of NM on L o . The treatment with 50 mg l−1 NM significantly reduced the L o , by up to 57 % of its control value, and it was reduced by up to 26 % at 100 mg l−1 NM. These results will be an important factor to take into account with regard to the applicability of NM for long-term use in crops, particularly during privative water conditions.

Keywords

Root hydraulic conductivity Nano-oxide Sunflower Metals Chlorophylls Uptake 

Notes

Acknowledgments

Domingo Martínez-Fernández is grateful for financial support from the European project Postdok ČZU (ESF/MŠMT CZ.1.07/2.3.00/30.0040). Michael Komárek is thankful for the support from the Czech Science Foundation (project 15-07117S). The authors thank Sylva Číhalová for her assistance with ICP analyses, and Martin Kočárek with the lyophilisation. The English revision by Dr. David J. Walker, the collaboration of Helena Neprasova and Miroslava Anderova from the IEM and The Academy of Sciences of the Czech Republic, for the use of the osmometer, are also acknowledged.

References

  1. Angadi SV, Entz MH (2002) Water relation of standard height and dwarf sunflower cultivars. Crop Sci 42:125–159CrossRefGoogle Scholar
  2. Asli S, Neumann PM (2009) Colloidal suspensions of clay or titanium dioxide nanoparticles can inhibit leaf growth and transpiration via physical effects on root water transport. Plant Cell Environ 32:577–584CrossRefGoogle Scholar
  3. Bandyopadhyay S, Plascencia-Villa G, Mukherjee A, Rico CM, José-Yacamán M, Peralta-Videa JR, Gardea-Torresdey JL (2015) Comparative phytotoxicity of ZnO NPs, bulk ZnO, and ionic zinc onto the alfalfa plants symbiotically associated with Sinorhizobium meliloti in soil. Sci Total Environ 515–516:60–69CrossRefGoogle Scholar
  4. Baruah S, Dutta J (2009) Nanotechnology applications in sensing and pollution degradation in agriculture. Environ Chem Lett 7:191–204CrossRefGoogle Scholar
  5. Bates LS, Waldern RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  6. Bell LW, Williams AH, Ryan MH, Ewing MA (2007) Water relations and adaptations to increasing water deficit in three perennial legumes, Medicago sativa, Dorycnium hirsutum and Dorycnium rectum. Plant Soil 290:231–243CrossRefGoogle Scholar
  7. Bittner F (2014) Molybdenum metabolism in plants and crosstalk to iron. Front Plant Sci 5:28CrossRefGoogle Scholar
  8. Bolan N, Kunhikrishnan A, Thangarajan R, Kumpiene J, Park J, Makino T, Kirkham MB, Scheckel K (2014) Remediation of heavy metal(loid)s contaminated soils—to mobilize or to immobilize? J Hazard Mater 266:141–166CrossRefGoogle Scholar
  9. Buzea C, Pacheco II, Robbie K (2007) Nanomaterials and nanoparticles: sources and toxicity. Biointerphases 2:17–71CrossRefGoogle Scholar
  10. Chen ZC, Ma JF (2013) Magnesium transporters and their role in Al tolerance in plants. Plant Soil 368:51–56CrossRefGoogle Scholar
  11. Conte SS, Walker EL (2011) Transporters contributing to iron trafficking in plants. Mol Plant 4(3):464–476CrossRefGoogle Scholar
  12. De La Torre-Roche R, Hawthorne J, Deng Y, Xing B, Cai W, Newman LA, Wang Q, Ma X, Hamdi H, White JC (2013) Multiwalled carbon nanotubes and C60 fullerenes differentially impact the accumulation of weathered pesticides in four agricultural plants. Environ Sci Technol 12539–12547Google Scholar
  13. Dietz K-J, Herth S (2011) Plant nanotoxicology. Trends Plant Sci 16(11):582–589CrossRefGoogle Scholar
  14. Elsaesser C, Howard V (2012) Toxicology of nanoparticles. Adv Drug Deliv Rev 64:129–137CrossRefGoogle Scholar
  15. Flagella Z, Rotunno T, Tarantino E, Di Caterina R, De Caro A (2002) Changes in seed yield and oil fatty acid composition of high oleic sunflower (Helianthus annuus L.) hybrids in relation to the sowing date and the water regime. Eur J Agron 17:221–230CrossRefGoogle Scholar
  16. Gao J, Youn S, Hovsepyan A, Llaneza VL, Wang Y, Bitton G, Bonzongo JJ (2009) Dispersion and toxicity of selected manufactured nanomaterials in natural river water samples: effects of water chemical composition. Environ Sci Technol 43:3322–3328CrossRefGoogle Scholar
  17. Gómez-Pastora J, Bringas E, Ortiz I (2014) Recent progress and future challenges on the use of high performance magnetic nano-adsorbents in environmental applications. Chem Eng J 256:187–204CrossRefGoogle Scholar
  18. Grieger KD, Fjordbøge A, Hartmann NB, Eriksson E, Bjerg PL, Baun A (2010) Environmental benefits and risks of zero-valent iron nanoparticles (nZVI) for in situ remediation: risk mitigation or trade-off? J Contam Hydrol 118(3–4):165–183CrossRefGoogle Scholar
  19. Hua M, Zhang S, Pan B, Zhang W, Lv L, Zhang Q (2012) Heavy metal removal from water/wastewater by nanosized metal oxides: a review. J Hazard Mater 211–212:317–331CrossRefGoogle Scholar
  20. Iannucci A, Rascio A, Russo M, Di Fonzo N, Martiniello P (2000) Physiological responses to water stress following a conditioning period in berseem clover. Plant Soil 223:217–227CrossRefGoogle Scholar
  21. IUPAC (1979) Reference material for trace analysis by radioanalytical methods: Bowen’s kale. Pure Appl Chem 51:1183–1193Google Scholar
  22. Jackson MB, Davies WJ, Else MA (1996) Pressure-flow relationships, xylem solutes and root hydraulic conductance in flooded tomato plants. Ann Bot 77:17–24CrossRefGoogle Scholar
  23. Judy JD, Bertsch PM (2014) Bioavailability, toxicity, and fate of manufactured nanomaterials in terrestrial ecosystems. In: Sparks D (ed) Advances in agronomy 123-1. AcademicGoogle Scholar
  24. Klaine SJ, Alvarez PJJ, Batley GE, Fernandes TF, Handy RD, Lyon DY, Mahendra S, McLaughlin MJ, Lead JR (2008) Nanomaterials in the environment: behavior, fate, bioavailability and effects. Environ Toxicol Chem 27:1825–1851CrossRefGoogle Scholar
  25. Komárek M, Vaněk A, Ettler V (2013) Chemical stabilization of metals and arsenic in contaminated soils using oxides—a review. Environ Pollut 172:9–22CrossRefGoogle Scholar
  26. Krishnaraj C, Jagan EG, Ramachandran R, Abirami SM, Mohan N, Kalaichelvan PT (2012) Process Biochem 47:651–658CrossRefGoogle Scholar
  27. Landa P, Vankova R, Andrlova J, Hodek J, Marsika P, Storchova H, White JC, Vanek T (2012) Nanoparticle-specific changes in Arabidopsis thaliana gene expression after exposure to ZnO, TiO2, and fullerene soot. J Hazard Mater 241–242:55–62CrossRefGoogle Scholar
  28. Lazcano-Ferrat I, Lovatt CJ (1999) Relationship between relative water content, nitrogen pools, and growth of Phaseolus vulgaris L. and P. acutifolius A. Gray during water deficit. Crop Sci 39:467–475CrossRefGoogle Scholar
  29. Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592CrossRefGoogle Scholar
  30. López-Moreno ML, de la Rosa G, Hernández-Viezcas JA, Castillo-Michel H, Bote CE, Peralta-Videa JR, Gardea-Torresdey JL (2010) Evidence of the differential biotransformation and genotoxicity of ZnO and CeO2 nanoparticles on soybean (Glycine max) plants. Environ Sci Technol 44:7315–7320CrossRefGoogle Scholar
  31. Lü P, Cao J, He S, Liu J, Li H, Cheng G, Ding Y, Joyce DC (2010) Nano-silver pulse treatments improve water relations of cut rose cv. Movie Star flowers. Postharvest Biol Technol 57(3):196–202CrossRefGoogle Scholar
  32. Ma X, Geisler-Lee J, Deng Y, Kolmakov A (2010a) Interactions between engineered nanoparticles (ENPs) and plants: phytotoxicity, uptake and accumulation. Sci Total Environ 408:3053–3061CrossRefGoogle Scholar
  33. Ma Y, Kuang L, He X, Bai W, Ding Y, Zhang Z, Zhao Y, Chai Z (2010b) Effects of rare earth oxide nanoparticles on root elongation of plants. Chemosphere 78:273–279CrossRefGoogle Scholar
  34. Ma C, Chhikara S, Xing B, Musante C, White JC, Parkash Dhankher O (2013a) Physiological and molecular response of Arabidopsis thaliana to nanoparticle cerium and indium oxide exposure. ACS sustain. Chem Eng 1:768–778Google Scholar
  35. Ma X, Gurung A, Deng Y (2013b) Phytotoxicity and uptake of nanoscale zero-valent iron (nZVI) by two plant species. Sci Total Environ 443:844–849CrossRefGoogle Scholar
  36. Ma Y, Zhang P, Zhang Z, He X, Li Y, Zhang J, Zheng L, Chu S, Yang K, Zhao Y, Chai Z (2014) Origin of the different phytotoxicity and biotransformation of cerium and lanthanum oxide nanoparticles in cucumber. Nanotoxicology 9:262–270CrossRefGoogle Scholar
  37. Manivannan P, Jaleel CA, Somasundaram R, Panneerselvam R (2008) Osmoregulation and antioxidant metabolism in drought stressed Helianthus annuus under triadimefon drenching. C R Biol 331:418–425CrossRefGoogle Scholar
  38. Martínez-Ballesta MC, Carvajal M (2014) New challenges in plant aquaporin biotechnology. Plant Sci 217–218:71–77CrossRefGoogle Scholar
  39. Martínez-Fernández D, Walker DJ, Romero-Espinar P, Flores P, del Río JA (2011) Physiological responses of Bituminaria bituminosa to heavy metals. J Plant Physiol 168:2206–2211CrossRefGoogle Scholar
  40. Martínez-Fernández D, Bingöl D, Komárek M (2014) Trace elements and nutrients adsorption onto nano-maghemite in a contaminated-soil solution: a geochemical/statistical approach. J Hazard Mater 276:271–277CrossRefGoogle Scholar
  41. Martínez-Fernández D, Vítková M, Bernal MP, Komárek M (2015) Effects of nano-maghemite on trace element accumulation and drought response of Helianthus annuus L. in a contaminated mine soil. Water Air Soil Pollut 226(4):1–4CrossRefGoogle Scholar
  42. Michálková Z, Komárek M, Šillerová H, Della Puppa L, Joussein E, Bordas F, Vaněk A, Vaněk O, Ettler V (2014) Evaluating the potential of three Fe- and Mn- (nano)oxides for the stabilization of Cd, Cu and Pb in contaminated soils. J Environ Manag 46:226–234CrossRefGoogle Scholar
  43. Mitrano DM, Motellier S, Clavaguera S, Nowack B (2015) Review of nanomaterial aging and transformations through the life cycle of nano-enhanced products. Environ Int 77:132–147CrossRefGoogle Scholar
  44. Moon Y-S, Park E-S, Kim T-O, Lee H-S, Lee S-E (2014) SELDI-TOF MS-based discovery of a biomarker in Cucumis sativus seeds exposed to CuO nanoparticles. Environ Toxicol Pharmacol 38(3):922–931CrossRefGoogle Scholar
  45. Nassar NN (2010) Rapid removal and recovery of Pb (II) from wastewater by magnetic nanoadsorbents. J Hazard Mater 184:538–546CrossRefGoogle Scholar
  46. Navarro E, Baun A, Behra R, Hartmann NB, Filser J, Miao A-J, Quigg A, Santschi PH, Sigg L (2008) Ecotoxicology 17:372–387CrossRefGoogle Scholar
  47. Nowack B, Bucheli T (2007) Occurrence, behavior and effects of nanoparticles in the environment. Environ Pollut 150(1):5–22CrossRefGoogle Scholar
  48. Paradiso A, Berardino R, de Pinto MC, di Toppi LS, Storelli MM, Tommasi F, De Gara L (2008) Increase in ascorbate–glutathione metabolism as local and precocious systemic responses induced by cadmium in durum wheat plants. Plant Cell Physiol 49(3):362–374CrossRefGoogle Scholar
  49. 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 59:3485–3498CrossRefGoogle Scholar
  50. Rico CM, Morales MI, Barrios AC, McCreary R, Hong J, Lee WY, Nunez J, Peralta-Videa JR, Gardea-Torresdey JL (2013) Effect of cerium oxide nanoparticles on the quality of rice (Oryza sativa L.) grains. J Agric Food Chem 61:11278–11285CrossRefGoogle Scholar
  51. Rondeau-Mouro C, Defer D, Leboeuf E, Lahaye M (2008) Assessment of cell wall porosity in Arabidopsis thaliana by NMR spectroscopy. Int J Biol Macromol 42:83–92CrossRefGoogle Scholar
  52. Song L, Vijver MG, Peijnenburg WJGM (2015) Comparative toxicity of copper nanoparticles across three Lemnaceae species. Sci Total Environ 518–519:217–224CrossRefGoogle Scholar
  53. Tang SCN, Lo IMC (2013) Magnetic nanoparticles: essential factors for sustainable environmental applications. Water Res 47(8):2613–2632CrossRefGoogle Scholar
  54. Trakal L, Martínez-Fernández D, Vítková M, Komárek M (2015) Phytoextraction of metals: modeling root metal uptake and associated processes. In: Ansari AA, Gill SS, Gill R, Lanza GR, Lee N (eds.) Phytoremediation: management of environmental contaminants. Springer. ISBN 978-3-319-10394- 5Google Scholar
  55. Trujillo-Reyes J, Vilchis-Nestor AR, Majumdar S, Peralta-Videa JR, Gardea-Torresdey JL (2013) Citric acid modifies surface properties of commercial CeO2 nanoparticles reducing their toxicity and cerium uptake in radish (Raphanus sativus) seedlings. J Hazard Mater 263:677–684CrossRefGoogle Scholar
  56. 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 267:255–263CrossRefGoogle Scholar
  57. Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759CrossRefGoogle Scholar
  58. Vítková M, Komárek M, Tejnecký V, Šillerová H (2015) Interactions of nano-oxides with low-molecular-weight organic acids in a contaminated soil. J Hazard Mater 293:7–14CrossRefGoogle Scholar
  59. Walker DJ, Romero P, de Hoyos A, Correal E (2008) Seasonal changes in cold tolerance, water relations and accumulation of cations and compatible solutes in Atriplex halimus L. Environ Exp Bot 64:217–224CrossRefGoogle Scholar
  60. Wang H, Kou X, Pei Z, Xiao JQ, Shan X, Xing B (2011) Physiological effects of magnetite (Fe3O4) nanoparticles on perennial ryegrass (Lolium perenne L.) and pumpkin (Cucurbita mixta) plants. Nanotoxicology 5:30–42CrossRefGoogle Scholar
  61. Waychunas GA, Kim CS, Banfiled JF (2005) Nanoparticulate iron oxide minerals in soils and sediments: unique properties and contaminant scavenging mechanisms. J Nanopart Res 7:409–433CrossRefGoogle Scholar
  62. Yang L, Watts DJ (2005) Particle surface characteristics may play an important role in phytotoxicity of alumina nanoparticles. Toxicol Lett 15:122–132CrossRefGoogle Scholar
  63. Zhang D, Hua T, Xiao F, Chen C, Gersberg RM, Liu Y, Stuckey D, Ng WJ, Tan SK (2015a) Phytotoxicity and bioaccumulation of ZnO nanoparticles in Schoenoplectus tabernaemontani. Chemosphere 120:211–219CrossRefGoogle Scholar
  64. Zhang W, Ebbs SD, Musante C, White JC, Gao C, Ma X (2015b) Uptake and accumulation of bulk and nanosized cerium oxide particles and ionic cerium by radish (Raphanus sativus L.). J Agric Food Chem 63:382–390CrossRefGoogle Scholar
  65. Zhu H, Han J, Xiao JQ, Jin Y (2008) Uptake, translocation, and accumulation of manufactured iron oxide nanoparticles by pumpkin plants. J Environ Monit 10:713–717CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Domingo Martínez-Fernández
    • 1
  • Didac Barroso
    • 1
  • Michael Komárek
    • 1
  1. 1.Department of Environmental Geosciences, Faculty of Environmental SciencesCzech University of Life Sciences PraguePrague 6Czech Republic

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