Research PaperUptake, translocation, weathering and speciation of gold nanoparticles in potato, radish, carrot and lettuce crops
Graphical Abstract
Introduction
Based on the United Nations Sustainable Development Goals report, the world’s population will be ~10 billion by 2050, and growth in agricultural product demand is expected to increase by at least 50% compared to 2013 (FAO, 2017). The application of nanomaterials holds major promise to support more accurate and productive agricultural practices, in terms of promoting plant growth and yields, by providing, e.g., smart fertilization, micronutrient supply, and precise delivery of pesticides (Bian et al., 2011, Glenn et al., 2012, Judy et al., 2012, Sabo-Attwood et al., 2012, Anderson et al., 2017). Future use of nanomaterials in agriculture will lead to extensive environmental exposure, so that understanding the fate of nanoparticles in the soil-plant environment, and their potential presence in food and feed products, is required.
The uptake and translocation of NPs has been demonstrated previously under different conditions and for many types of plants (e.g. Nath et al., 2018, 2019; Wojcieszek et al., 2020). However, assessment of nanoparticle (NP) uptake by plants and NP transport across the plant body is limited and often controversial. For example, small (~4 nm) Au-NPs are taken up by different plants while 18 nm NPs agglomerate on roots (Glenn et al., 2012, Sabo-Attwood et al., 2012). Tobacco plants bioaccumulate 10–50 nm Au-NPs (4), but wheat shows no gold uptake for the same conditions. In general, NP behavior and transformation rates are influenced by environmental factors such as pH, aqueous ionic strength, and presence of humic acids or root exudates (Bian et al., 2011, Anderson et al., 2017, Hortin et al., 2019), as well as by the properties of the NP. Identifying the speciation of NPs within plant parts remains a major challenge: it is not clear what portion of the NPs (if at all) is converted to ions, and if NPs found in plant parts are transformed during uptake and translocation.
To address the lack of information on plant uptake, translocation and speciation (in terms of particle size change and formation of ions) of NPs from soil, the goals of this study were to examine these processes for Au-NPs in four important crops. Au-NPs are considered relatively stable in the environment and background levels of gold in soil and plant matrices are minimal, which enables their study in complex environmental matrices. However, recently it was demonstrated that cyanide, which is produced by some plants and microorganisms, effectively dissolves Au-NPs in soil and water environments (Avellan et al., 2018, McGivney et al., 2019). To date, Au-NP uptake by plants and their consequent impacts have been studied mostly via hydroponic exposure, examining, e.g., how barley production and macronutrient/micronutrient uptake are affected by Au-NP exposure (Feichtmeier et al., 2015).
Another critical issue is the quantitative determination of NP speciation during plant uptake. Several reviews discuss methods to detect and characterize NPs in plants tissues (Tsz-Shan Lum and Sze-Yin Leung, 2017, Picó et al., 2017, Lv et al., 2019). They indicate that the main techniques to determine size and size distributions are (sp)-ICP-MS, TEM, and hybrid methods that combine size-separation steps with elemental analysis; for environmentally relevant concentrations, only ICP-MS methods provide suitable sensitivity. For example, sp-ICP-MS was used successfully to detect Ag and CeO2 NP accumulation in plant samples after exposure in soil (Wagener et al., 2019).
Here, we quantitatively measure the uptake and speciation of Au-NPs in different plant tissues of potato, radish, carrot and lettuce that were grown in soil. We show that most of the gold in the different plant tissues is in the form of NPs, and that the Au-NPs in the plant are distinct from those applied to the soil. In particular, we find evidence that plants can alter nanoparticles in the rhizosphere prior to uptake, and subsequently reorganize ionic metals as nanoparticles in their tissues.
Section snippets
Chemicals
ICP-MS stock tuning solution containing 10 mg L−1 each of Li, Y, Ce, Tl and Co in a matrix of 2% HNO3 (Agilent Technologies, USA). Concentrated HNO3 (≥ 69%, TraceSelect, Fluka France). Gold nanoparticle suspension with a nominal diameter of 60 nm (60 ± 3 nm) and Au mass concentration of 31.92 ± 0.57 mg L−1, stabilized in citrate buffer, was obtained from Sigma-Aldrich (USA) and used as a standard to verify recovery and stability of the Au-NPs. The Au(III) standard for ICP (1000 mg L−1, in 5%
Plant tissue digestion
To detect and analyze Au-NPs in plant parts, gold must be separated from the organic matrices, with good yield and without changing the original speciation of the analyte. Three procedures for plant sample digestion were employed:
- (i)
Acid digestion by ashing the organic matrix and dissolution in strong acid, to determine the total Au content in plants; this protocol was applied for dried and homogenized samples of different plant parts or for the soil used for cultivation.
- (ii)
Enzymatic plant digestion,
Conclusions
Our experiments demonstrate three major points: (i) The feasibility of determining the presence/concentration and distribution of NPs in different (dried) plant parts, which differ from plant to plant. Critically, we identify the evident capacity of plants to break down (or substantially change the properties of) NPs prior to uptake in the rhizosphere, as well as the evident capacity of plants to reorganize ionic metals (at least, gold) as NPs in their tissues. This could lead to NP exposure
CRediT authorship contribution statement
I.D. and B.B. conceived and designed the experiments. T.V. and P.L. planned and executed the plant-growing experiments. J.M. and B.G.Z. conceived and executed the digestion protocols. J.M., B.G.Z., I.D. and J.N. performed the analytical measurements. I.D. and B.B. processed the experimental data, performed the analysis and prepared the initial draft with inputs from all co-authors; all authors discussed the results and commented on the manuscript.
Declaration of Competing Interest
The authors declare no competing interests.
Acknowledgments
The authors kindly acknowledge the financial support from the Polish National Science Centre (UMO-2014/15/B/ST4/04641), the European Regional Development Fund-Project "Centre for Experimental Plant Biology" (No. CZ.02.1.01/0.0/0.0/16_019/0000738), and the Ministry of Science, Technology and Space, Israel (Grant No. 3-13036). The SEM measurements were conducted by Ifat Kaplan-Ashiri at the Irving and Cherna Moskowitz Center for Nano and BioNano Imaging (Weizmann Institute of Science). The
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