Journal of Nanoparticle Research

, Volume 11, Issue 6, pp 1453–1463 | Cite as

The mechanism of metal nanoparticle formation in plants: limits on accumulation

  • R. G. HaverkampEmail author
  • A. T. Marshall
Research Paper


Metal nanoparticles have many potential technological applications. Biological routes to the synthesis of these particles have been proposed including production by vascular plants, known as phytoextraction. While many studies have looked at metal uptake by plants, particularly with regard to phytoremediation and hyperaccumulation, few have distinguished between metal deposition and metal salt accumulation. This work describes the uptake of AgNO3, Na3Ag(S2O3)2, and Ag(NH3)2NO3 solutions by hydroponically grown Brassica juncea and the quantitative measurement of the conversion of these salts to silver metal nanoparticles. Using X-ray absorption near edge spectroscopy (XANES) to determine the metal speciation within the plants, combined with atomic absorption spectroscopy (AAS) for total Ag, the quantity of reduction of AgI to Ag0 is reported. Transmission electron microscopy (TEM) showed Ag particles of 2–35 nm. The factors controlling the amount of silver accumulated are revealed. It is found that there is a limit on the amount of metal nanoparticles that may be deposited, of about 0.35 wt.% Ag on a dry plant basis, and that higher levels of silver are obtained only by the concentration of metal salts within the plant, not by deposition of metal. The limit on metal nanoparticle accumulation, across a range of metals, is proposed to be controlled by the total reducing capacity of the plant for the reduction potential of the metal species and limited to reactions occurring at an electrochemical potential greater than 0 V (verses the standard hydrogen electrode).


Silver Nanoparticle Phytomining Phytoremediation XAS XANES EXAFS Nanobiotechnology 



The authors wish to thank the Photon Factory Advanced Ring, Tsukuba, Japan, for beam time access under proposal 2008G207; Dr Masaharu Nomura and Garry Foran, Photon Factory, Tsukuba, for their assistance; NZ Synchrotron Group Limited for a travel grant; Prof Clive Davies for advice on hydroponics and Doug Hopcroft, Manawatu Microscopy Centre, for assistance with the TEM work.


  1. Aldrich MV, Gardea-Torresdey JL, Peralta-Videa JR, Parsons JG (2003) Uptake and reduction of Cr(VI) to Cr(III) by mesquite (Prosopis spp): chromate–plant interaction in hydroponics and solid media studied using XAS. Environ Sci Technol 37(9):1859–1864. doi: 10.1021/es0208916 PubMedCrossRefGoogle Scholar
  2. Anderson CWN, Brooks RR, Stewart RB, Simcock R (1998) Harvesting a crop of gold in plants. Nature (London, UK) 395(6702):553–554. doi: 10.1038/26875 CrossRefADSGoogle Scholar
  3. Arthur EL, Rice PJ, Rice PJ, Anderson TA, Baladi SM, Henderson KLD, Coats JR (2005) Phytoremediation—an overview. Crit Rev Plant Sci 24(2):109–122. doi: 10.1080/07352680590952496 CrossRefGoogle Scholar
  4. Aylward G, Findlay T (2002) SI chemical data, 5th edn. Wiley, MiltonGoogle Scholar
  5. Bard AJ, Parsons R, Jordan J (1985) Standard potentials in aqueous solution. Marcel Dekker, New YorkGoogle Scholar
  6. Bluskov S, Arocena JM, Omotoso OO, Young JP (2005) Uptake, distribution, and speciation of chromium in Brassica juncea. Int J Phytoremediation 7(2):153–165. doi: 10.1080/16226510590950441 PubMedCrossRefGoogle Scholar
  7. Bocquet ML, Michaelides A (2006) Exploring the catalytic activity of a noble metal: the Ag catalyzed ethylene epoxidation reaction. In: Grütter P, Hofer W, Rosei F (eds) Properties of single organic molecules on crystal surfaces. Imperial College Press, London, pp 389–424Google Scholar
  8. Brooks RR (1992) Noble metals and biological systems; their role in medicine, mineral exploration, and the environment. CRC, Boca RatonGoogle Scholar
  9. Brooks RR, Chambers MF, Nicks LJ, Robinson BH (1998) Phytomining. Trends Plant Sci 3(9):359–362. doi: 10.1016/S1360-1385(98)01283-7 CrossRefGoogle Scholar
  10. Brown WV, Mollenhauer H, Johnson C (1962) An electron microscope study of silver nitrate reduction in leaf cells. Am J Bot 49(1):57–63. doi: 10.2307/2439389 CrossRefGoogle Scholar
  11. Chen CH, Sarma LS, Wang GR, Chen JM, Shih SC, Tang MT, Liu DG, Lee JF, Chen JM, Hwang BJ (2006) Formation of bimetallic Ag–Pd nanoclusters via the reaction between Ag nanoclusters and Pd2+ ions. J Phys Chem B 110(21):10287–10295. doi: 10.1021/jp061095f PubMedCrossRefGoogle Scholar
  12. De La Rosa G, Peralta-Videa JR, Montes M, Parsons JG, Cano-Aguilera I, Gardea-Torresdey JL (2004) Cadmium uptake and translocation in tumbleweed (Salsola kali), a potential Cd-hyperaccumulator desert plant species: ICP/OES and XAS studies. Chemosphere 55(9):1159–1168. doi: 10.1016/j.chemosphere.2004.01.028 PubMedCrossRefGoogle Scholar
  13. Evangelou MWH, Ebel M, Schaeffer A (2007) Chelate assisted phytoextraction of heavy metals from soil effect, mechanism, toxicity, and fate of chelating agents. Chemosphere 68(6):989–1003. doi: 10.1016/j.chemosphere.2007.01.062 PubMedCrossRefGoogle Scholar
  14. Gardea-Torresdey J, Parsons J, Gomez E, Peralta-Videa J, Troiani H, Santiago P, Yacaman M (2002) Formation and growth of Au nanoparticles inside live alfalfa plants. Nano Lett 2(4):397–401. doi: 10.1021/nl015673+ CrossRefADSGoogle Scholar
  15. Gardea-Torresdey JL, Gomez E, Peralta-Videa JR, Parsons JG, Troiani H, Jose-Yacaman M (2003) Alfalfa sprouts: a natural source for the synthesis of silver nanoparticles. Langmuir 19(5):1357–1361. doi: 10.1021/la020835i CrossRefGoogle Scholar
  16. Gardea-Torresdey J, Rodriguez E, Parsons JG, Peralta-Videa JR, Meitzner G, Cruz-Jimenez G (2005a) Use of ICP and XAS to determine the enhancement of gold phytoextraction by Chilopsis linearis using thiocyanate as a complexing agent. Anal Bioanal Chem 382(2):347–352. doi: 10.1007/s00216-004-2966-6 PubMedCrossRefGoogle Scholar
  17. Gardea-Torresdey JL, Peralta-Videa JR, De La Rosa G, Parsons JG (2005b) Phytoremediation of heavy metals and study of the metal coordination by X-ray absorption spectroscopy. Coord Chem Rev 249(17–18):1797–1810. doi: 10.1016/j.ccr.2005.01.001 CrossRefGoogle Scholar
  18. Ghosh SK, Kundu S, Mandal M, Nath S, Pal T (2003) Studies on the evolution of silver nanoparticles in micelle by UV-photoactivation. J Nanopart Res 5(5–6):577–587. doi: 10.1023/B:NANO.0000006100.25744.fa CrossRefGoogle Scholar
  19. Hall JL, Williams LE (2003) Transition metal transporters in plants. J Exp Bot 54(393):2601–2613. doi: 10.1093/jxb/erg303 PubMedCrossRefGoogle Scholar
  20. Hannemann S, Grunwaldt JD, Krumeich F, Kappen P, Baiker A (2006) Electron microscopy and EXAFS studies on oxide-supported gold–silver nanoparticles prepared by flame spray pyrolysis. Appl Surf Sci 252(22):7862–7873. doi: 10.1016/j.apsusc.2005.09.065 CrossRefADSGoogle Scholar
  21. Harris AT, Bali R (2008) On the formation and extent of uptake of silver nanoparticles by live plants. J Nanopart Res 10(4):691–695. doi: 10.1007/s11051-007-9288-5 CrossRefGoogle Scholar
  22. Haverkamp RG, Marshall AT, van Agterveld D (2007) Pick your carats: nanoparticles of gold–silver–copper alloy produced in vivo. J Nanopart Res 9(4):697–700. doi: 10.1007/s11051-006-9198-y CrossRefGoogle Scholar
  23. Hubin A, Simons W, Pauwels L, Vereecken J (2004) Reduction of silver complexes: towards an ever more elaborated insight in the influence of the type of ligand on the reaction rate. J Electroanal Chem 572(2):399–408. doi: 10.1016/j.jelechem.2004.04.018 CrossRefGoogle Scholar
  24. Kramer U, Pickering IJ, Prince RC, Raskin I, Salt DE (2000) Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Plant Physiol 122(4):1343–1353. doi: 10.1104/pp.122.4.1343 PubMedCrossRefGoogle Scholar
  25. Luo CL, Shen ZG, Li XD (2005) Enhanced phytoextraction of Cu, Pb, Zn and Cd with EDTA and EDDS. Chemosphere 59(1):1–11. doi: 10.1016/j.chemosphere.2004.09.100 PubMedCrossRefGoogle Scholar
  26. Manceau A, Nagy KL, Marcus MA, Lanson M, Geoffroy N, Jacquet T, Kirpichtchikova T (2008) Formation of metallic copper manoparticles at the soil–root interface. Environ Sci Technol 42(5):1766–1772. doi: 10.1021/es072017o PubMedCrossRefGoogle Scholar
  27. Marshall AT, Haverkamp RG, Davies CE, Parsons JG, Gardea-Torresdey JL, van Agterveld D (2007) Accumulation of gold nanoparticles in Brassic juncea. Int J Phytoremediation 9(1–3):197–206. doi: 10.1080/15226510701376026 PubMedCrossRefGoogle Scholar
  28. Meers E, Hopgood M, Lesage E, Vervaeke P, Tack FMG, Verloo MG (2004) Enhanced phytoextraction: in search of EDTA alternatives. Int J Phytoremediation 6(2):95–109. doi: 10.1080/16226510490454777 PubMedCrossRefGoogle Scholar
  29. Mohanpuria P, Rana NK, Yadav SK (2008) Biosynthesis of nanoparticles: technological concepts and future applications. J Nanopart Res 10(3):507–517. doi: 10.1007/s11051-007-9275-x CrossRefGoogle Scholar
  30. Montes-Bayon M, Yanes EG, De Leon CP, Jayasimhulu K, Stalcup A, Shann J, Caruso JA (2002) Initial studies of selenium speciation in Brassica juncea by LC with ICPMS and ES-MS detection: an approach for phytoremediation studies. Anal Chem 74(1):107–113. doi: 10.1166/jbn.2007.041 PubMedCrossRefGoogle Scholar
  31. Nair LS, Laurencin CT (2007) Silver nanoparticles: synthesis and therapeutic applications. J Biomed Nanotechnol 3(4):301–316. doi: 10.1166/jbn.2007.041 CrossRefGoogle Scholar
  32. Nomura M, Koike Y, Sato M, Koyama A, Inada Y, Asakura K (2007) A new XAFS beamline NWIOA at the photon factory. In: Hedman B, Pianetta P (eds) XAFS13—13th international conference, 882 (X-ray absorption fine structure) AIP conference proceedingsGoogle Scholar
  33. Pickering IJ, Prince RC, George GN, Rauser WE, Wickramasinghe WA, Watson AA, Dameron CT, Dance IG, Fairlie DP, Salt DE (1999) X-ray absorption spectroscopy of cadmium phytochelatin and model systems. BBA-Protein Struct Mol Enzymol 1429(2):351–364CrossRefGoogle Scholar
  34. Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39. doi: 10.1146/annurev.arplant.56.032604.144214 PubMedCrossRefGoogle Scholar
  35. Polette LA, Gardea-Torresdey JL, Chianelli RR, George GN, Pickering IJ, Arenas J (2000) XAS and microscopy studies of the uptake and bio–transformation of copper in Larrea tridentata (creosote bush). Microchem J 65(3):227–236. doi: 10.1016/S0026-265X(00)00055-2 CrossRefGoogle Scholar
  36. Ravel B, Newville M (2005) ATHENA, ARTEMIS, HEPHAESTUS: data analysis for X-ray absorption spectroscopy using IFEFFIT. J Synchrotron Radiat 12:537–541. doi: 10.1107/S0909049505012719 PubMedCrossRefGoogle Scholar
  37. Salt DE, Prince RC, Baker AJM, Raskin I, Pickering IJ (1999) Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectroscopy. Environ Sci Technol 33(5):713–717. doi: 10.1021/es980825x CrossRefGoogle Scholar
  38. Scheckel KG, Lombi E, Rock SA, Mclaughlin NJ (2004) In vivo synchrotron study of thallium speciation and compartmentation in Lberis intermedia. Environ Sci Technol 38(19):5095–5100. doi: 10.1021/es049569g PubMedCrossRefGoogle Scholar
  39. Schutzendubel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53(372):1351–1365. doi: 10.1093/jexbot/53.372.1351 PubMedCrossRefGoogle Scholar
  40. Schwab AP, Zhu DS, Banks MK (2008) Influence of organic acids on the transport of heavy metals in soil. Chemosphere 72(6):986–994. doi: 10.1016/j.chemosphere.2008.02.047 PubMedCrossRefGoogle Scholar
  41. Sharma NC, Gardea-Torresdey JL, Parsons J, Sahi SV (2004) Chemical speciation and cellular deposition of lead in Sesbania drummondii. Environ Toxicol Chem 23(9):2068–2073. doi: 10.1897/03-540 PubMedCrossRefGoogle Scholar
  42. Sharma NC, Sahi SV, Nath S, Parsons JG, Gardea-Torresdey JL, Pal T (2007) Synthesis of plant-mediated gold nanoparticles and catalytic role of biomatrix-embedded nanomaterials. Environ Sci Technol 41(14):5137–5142. doi: 10.1021/es062929a PubMedCrossRefGoogle Scholar
  43. Wright EM, Diamond JM (1977) Anion selectivity in biological systems. Physiol Rev 57:109–156PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.School of Engineering and Advanced TechnologyMassey UniversityPalmerston NorthNew Zealand

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