Discovery of nano-sized gold particles in natural plant tissues

Abstract

Biological effects of nanoparticles have attracted widespread attention. However, the interaction between plants and nanoparticles remains unclear. The purpose of this study was to investigate characteristics of nano-sized metal particles in two representative plant species, Erigeron canadensis and Boehmeria nivea, in the Guangdong Province, China. The stems of the plants were sliced and placed on Ni–C grids for field-emission transmission electron microscopy (TEM). The metal-bearing nanoparticles were further analysed for their size, shape, composition, content and other characteristics using X-ray energy spectrum analysis, scanning TEM and selected-area electron diffraction pattern. The results revealed that the plants contain nano-sized Au-bearing particles with a diameter of 5–50 nm, ellipsoid, spherical and bone-rod shapes or irregular morphology with smooth edges. These nanoparticles primarily consisted of Au, Cu, O and Cl. The discovery of Au-bearing nanoparticles in natural plant tissues is of great significance for biological nanoscience. Here, we discuss the function and absorption mechanism of Au-bearing nanoparticles in plants and present the influence of the discovery of Au-bearing nanoparticles in natural plants.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Anand RR, Aspandiar MF, Noble RRP (2016) A review of metal transfer mechanisms through transported cover with emphasis on the vadose zone within the Australian regolith. Ore Geol Rev 73:394–416. https://doi.org/10.1016/j.oregeorev.2015.06.018

    Article  Google Scholar 

  2. Andreotti F, Mucha AP, Caetano C, Rodrigues P, Gomes CR, Almeida CMR (2015) Interactions between salt marsh plants and Cu nanoparticles—effects on metal uptake and phytoremediation processes. Ecotoxicol Environ Saf 120:303–309. https://doi.org/10.1016/j.ecoenv.2015.06.017

    Article  CAS  Google Scholar 

  3. Avellan A, Schwab F, Masion A, Chaurand P, Borschneck D, Vidal V et al (2017) Nanoparticle uptake in plants: gold nanomaterial localized in roots of Arabidopsis thaliana by X-ray computed nanotomography and hyperspectral imaging. Environ Sci Technol 51:8682–8691. https://doi.org/10.1021/acs.est.7b01133

    Article  CAS  Google Scholar 

  4. Bali R, Siegele R, Harris AT (2010) Phytoextraction of Au: uptake, accumulation and cellular distribution in Medicago sativa and Brassica juncea. Chem Eng J 156(2):286–297. https://doi.org/10.1016/j.cej.2009.10.019

    Article  CAS  Google Scholar 

  5. Bhatt I, Tripathi BN (2011) Interaction of engineered nanoparticles with various components of the environment and possible strategies for their risk assessment. Chemosphere 82:308–317. https://doi.org/10.1016/j.chemosphere.2010.10.011

    Article  CAS  Google Scholar 

  6. Brooks RR, Lee J, Reeves RD, Jaffre T (1977) Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J Geochem Explor 7:49–57. https://doi.org/10.1016/0375-6742(77)90074-7

    Article  CAS  Google Scholar 

  7. Brumfiel G (2003) Nanotechnology: a little knowledge. Nature 424:246–248. https://doi.org/10.1038/424246a

    Article  CAS  Google Scholar 

  8. Cao JJ, Hu X, Jiang D (2009) Transmission electron microscopy study of adsorption of colloidal gold nanoparticles on lepidocrocite and kaolinite. Micro Nano Lett 4:95–98. https://doi.org/10.1049/mnl.2009.0023

    Article  CAS  Google Scholar 

  9. Cifuentes Z, Custardoy L, de la Fuente JM, Marquina C, Ibarra MR, Rubiales D et al (2010) Absorption and translocation to the aerial part of magnetic carbon-coated nanoparticles through the root of different crop plants. J Nanobiotechnol 8(1):26. https://doi.org/10.1186/1477-3155-8-26

    Article  CAS  Google Scholar 

  10. Cwn A, Brooks RR, Stewart RB, Simcock R (1998) Harvesting a crop of gold in plants. Nat Lond 395:553–554

    Article  CAS  Google Scholar 

  11. Dykman L, Khlebtsov N (2012) Gold nanoparticles in biomedical applications: recent advances and perspectives. Chem Soc Rev 41(6):2256–2282. https://doi.org/10.1002/chin.201224275

    Article  CAS  Google Scholar 

  12. Eichert T, Kurtz A, Steiner U, Goldbach HE (2008) Size exclusion limits and lateral heterogeneity of the stomatal foliar uptake pathway for aqueous solutes and water-suspended nanoparticles. Physiol Plant 134(1):151–160. https://doi.org/10.1111/j.1399-3054.2008.01135.x

    Article  CAS  Google Scholar 

  13. El-Temsah YS, Joner EJ (2012) Impact of Fe and Ag nanoparticles on seed germination and differences in bioavailability during exposure in aqueous suspension and soil. Environ Toxicol 27(1):42–49. https://doi.org/10.1002/tox.20610

    Article  CAS  Google Scholar 

  14. Fontes RLF, Pereira JMN, Neves JCL, Fontes RLF, Pereira JMN, Neves JCL (2014) Uptake and translocation of Cd and Zn in two lettuce cultivars. Anais Acad Bras Cienc 86:907–922. https://doi.org/10.1590/0001-37652014117912

    Article  CAS  Google Scholar 

  15. Gan PP, Li SFY (2012) Potential of plant as a biological factory to synthesize gold and silver nanoparticles and their applications. Rev Environ Sci Bio/Technol 11(2):169–206. https://doi.org/10.1007/s11157-012-9278-7

    Article  CAS  Google Scholar 

  16. Gardea-Torresdey JL, Parsons JG, Gomez E, Peralta-Videa J et al (2002) Formation and growth of Au nanoparticles inside live alfalfa plants. Nano Lett 2(4):397–401. https://doi.org/10.1021/nl015673

    Article  CAS  Google Scholar 

  17. Glauert AM (1975) Fixation, dehydration and embedding of biological specimens. North-Holland Pub. Co, Oxford

    Google Scholar 

  18. Hagler HK (2007) Ultramicrotomy for biological electron microscopy. Methods Mol Biol 369:67–96. https://doi.org/10.1007/978-1-59745-294-6_5

    Article  CAS  Google Scholar 

  19. Hu G, Cao JJ, Lai PX, Hopke PK, Holub RF, Zeng JN, Wang ZH, Wu ZQ (2015) Characteristics and geological significance of particles on fractures from the Dongshengmiao polymetallic pyrite deposit, Inner Mongolia, China. Geochem Explor Environ Anal 15:373–381. https://doi.org/10.1144/geochem2014-312

    Article  CAS  Google Scholar 

  20. Hu G, Cao J, Jiang T, Wang Z, Yi Z (2017) Prospecting application of nanoparticles and nearly nanoscale particles within plant tissues. Resour Geol 67(3):316–329. https://doi.org/10.1111/rge.12130

    Article  CAS  Google Scholar 

  21. Kumar V, Guleria P, Kumar V, Yadav SK (2013) Gold nanoparticle exposure induces growth and yield enhancement in Arabidopsis thaliana. Sci Total Environ 461–462:462–468. https://doi.org/10.1016/j.scitotenv.2013.05.018

    Article  CAS  Google Scholar 

  22. Kumari M, Mukherjee A, Chandrasekaran N (2009) Genotoxicity of silver nanoparticles in Allium cepa. Sci Total Environ 407:5243–5246. https://doi.org/10.1016/j.scitotenv.2009.06.024

    Article  CAS  Google Scholar 

  23. Kurepa J, Paunesku T, Vogt S, Arora H, Rabatic BM, Lu J et al (2010) Uptake and distribution of ultrasmall anatase TiO2 Alizarin red S nanoconjugates in Arabidopsis thaliana. Nano Lett 10(7):2296–2302. https://doi.org/10.1021/nl903518f

    Article  CAS  Google 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. https://doi.org/10.1897/07-481.1

    Article  CAS  Google Scholar 

  25. 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. https://doi.org/10.1016/j.chemosphere.2011.10.013

    Article  CAS  Google Scholar 

  26. Lin D, Xing B (2007) Phytotoxicity of nanoparticles: inhibition of seed germination and root growth. Environ Pollut 150:243–250. https://doi.org/10.1016/j.envpol.2007.01.016

    Article  CAS  Google Scholar 

  27. Lin D, Xing B (2008) Root uptake and phytotoxicity of ZnO nanoparticles. Environ Sci Technol 42:5580–5585. https://doi.org/10.1021/es800422x

    Article  CAS  Google Scholar 

  28. Lin S, Reppert J, Hu Q, Hudson JS, Reid ML, Ratnikova TA, Ke PC (2009) Uptake, translocation, and transmission of carbon nanomaterials in rice plants. Small 5:1128–1132. https://doi.org/10.1002/smll.200801556

    Article  CAS  Google Scholar 

  29. Lintern M, Anand R, Ryan C, Paterson D (2013) Natural gold particles in Eucalyptus leaves and their relevance to exploration for buried gold deposits. Nat Commun 4(4):2614. https://doi.org/10.1038/ncomms3614

    CAS  Article  Google Scholar 

  30. Liu A, Ye B (2013) Application of gold nanoparticles in biomedical researches and diagnosis. Clin Lab 59(1–2):23. https://doi.org/10.7754/clin.lab.2012.120614

    CAS  Article  Google Scholar 

  31. Liu R, Zhang H, Lal R (2016) 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(1):1–14. https://doi.org/10.1007/s11270-015-2738-2

    Article  CAS  Google Scholar 

  32. Meyer DE, Curran MA, Gonzalez MA (2009) An examination of existing data for the industrial manufacture and use of nanocomponents and their role in the life cycle impact of nanoproducts. Environ Sci Technol 43(5):1256–1263. https://doi.org/10.1021/es8023258

    Article  CAS  Google Scholar 

  33. Mubarakali D, Thajuddin N, Jeganathan K, Gunasekaran M (2011) Plant extract mediated synthesis of silver and gold nanoparticles and its antibacterial activity against clinically isolated pathogens. Colloids Surf B 85(2):360–365. https://doi.org/10.1016/j.colsurfb.2011.03.009

    Article  CAS  Google Scholar 

  34. Nair R, Varghese SH, Nair BG, Maekawa T, Yoshida Y, Kumar DS (2010) Nanoparticulate material delivery to plants. Plant Sci 179(3):154–163. https://doi.org/10.1016/j.plantsci.2010.04.012

    Article  CAS  Google Scholar 

  35. Navarro E, Baun A, Behra R, Hartmann NB, Filser J, Miao AJ, Sigg L (2008) Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology 17(5):372–386. https://doi.org/10.1007/s10646-008-0214-0

    Article  CAS  Google Scholar 

  36. Nel A, Xia T, Mädler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311(5761):622–627. https://doi.org/10.1126/science.1114397

    Article  CAS  Google Scholar 

  37. Parsons JG, Lopez ML, Gonzalez CM, Peralta-Videa JR, Gardea-Torresdey JL (2010) Toxicity and biotransformation of uncoated and coated nickel hydroxide nanoparticles on mesquite plants. Environ Toxicol Chem 29(5):1146–1154. https://doi.org/10.1002/etc.146

    CAS  Article  Google Scholar 

  38. Rico CM, Majumdar S, Duarte-Gardea M (2011) Interaction of nanoparticles with edible plants and their possible implications in the food chain. J Agric Food Chem 59(8):3485–3498. https://doi.org/10.1021/jf104517j

    Article  CAS  Google Scholar 

  39. Robinson BH, Brooks RR, Howes AW, Kirkman JH, Gregg PEH (1997) The potential of the high-biomass nickel hyperaccumulator Berkheya coddii for phytoremediation and phytomining. J Geochem Explor 60(2):115–126. https://doi.org/10.1016/s0375-6742(97)00036-8

    Article  CAS  Google Scholar 

  40. Schreiber L (2010) Transport barriers made of cutin, suberin and associated waxes. Trends Plant Sci 15(10):546–553. https://doi.org/10.1016/j.tplants.2010.06.004

    Article  CAS  Google Scholar 

  41. Service RF (2003) Nanomaterials show signs of toxicity. Science 300:243. https://doi.org/10.1126/science.300.5617.243a

    Article  Google Scholar 

  42. Shankar SS, Ahmad A, Pasricha R, Sastry M (2003) Bioreduction of chloroaurate ions by geranium leaves and its endophytic fungus yields gold nanoparticles of different shapes. J Mater Chem 13(7):1822–1826. https://doi.org/10.1039/b303808b

    Article  CAS  Google Scholar 

  43. Shankar SS, Rai A, Ahmad A, Sastry M (2004) Rapid synthesis of Au, Ag, and bimetallic Au core–Ag shell nanoparticles using Neem (Azadirachta indica) leaf broth. J Colloid Interface Sci 275(2):496–502. https://doi.org/10.1016/j.jcis.2004.03.003

    Article  CAS  Google Scholar 

  44. Sotnikov DV, Zherdev AV, Dzantiev BB (2015) Development and application of a label-free fluorescence method for determining the composition of gold nanoparticle–protein conjugates. Int J Mol Sci 16(1):907–923. https://doi.org/10.3390/ijms16010907

    Article  CAS  Google Scholar 

  45. Stampoulis D, Sinha SK, White JC (2009) Assay-dependent phytotoxicity of nanoparticles to plants. Environ Sci Technol 43(24):9473–9479. https://doi.org/10.1021/es901695c

    Article  CAS  Google Scholar 

  46. Stone MB (2010) Differential uptake of carbon nanoparticles by plant and Mammalian cells. Small 6(5):612–617. https://doi.org/10.1002/smll.200901911

    Article  CAS  Google Scholar 

  47. Wang Z, Xie X, Zhao J, Liu X, Feng W, White JC, Xing B (2012) Xylem- and phloem-based transport of CuO nanoparticles in maize (Zea mays L.). Environ Sci Technol 46(8):4434–4441. https://doi.org/10.1021/es204212z

    Article  CAS  Google Scholar 

  48. Wild E, Jones KC (2009) Novel method for the direct visualization of in vivo nanomaterials and chemical interactions in plants. Environ Sci Technol 43(14):5290–5294. https://doi.org/10.1021/es900065h

    Article  CAS  Google Scholar 

  49. Yang X, Pan H, Wang P, Zhao FJ (2016) Particle-specific toxicity and bioavailability of cerium oxide (CeO2) nanoparticles to Arabidopsis thaliana. J Hazard Mater 322(Pt A):292–300. https://doi.org/10.1016/j.jhazmat.2016.03.054

    CAS  Article  Google Scholar 

  50. Yin L, Cheng Y, Espinasse B, Colman BP, Auffan M, Wiesner M, Bernhardt ES (2011) More than the ions: the effects of silver nanoparticles on Lolium multiflorum. Environ Sci Technol 45(6):2360–2367. https://doi.org/10.1021/es103995x

    Article  CAS  Google Scholar 

  51. 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 Integr Biometal Sci 3(8):816. https://doi.org/10.1039/c1mt00049g

    Article  CAS  Google Scholar 

  52. Zhu H, Han J, Xiao JQ, Jin Y (2008) Uptake, translocation, and accumulation of manufactured iron oxide nanoparticles by pumpkin plants. J Environ Monit JEM 10(6):713–717. https://doi.org/10.1039/b805998e

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant Nos. 41473040 and 41030425). The authors wish to thank Chen Dong of the School of Life Science of the Sun Yat-sen University for assisting with the pretreatment of plant samples and acknowledge Huang Qingli of the Instrument Analysis Center of the Yangzhou University for the assistance in TEM analysis.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Jianjin Cao.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Luo, X., Cao, J. Discovery of nano-sized gold particles in natural plant tissues. Environ Chem Lett 16, 1441–1448 (2018). https://doi.org/10.1007/s10311-018-0749-0

Download citation

Keywords

  • Au nanoparticles
  • Plant tissues
  • TEM study
  • Characteristic
  • Absorption mechanism
  • Environment