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Accumulation of Platinum Nanoparticles by Sinapis alba
and Lepidium sativum Plants
Monika Asztemborska &Romuald Steborowski &
Joanna Kowalska &Grazyna Bystrzejewska-Piotrowska
Received: 19 November 2013 /Accepted: 11 July 2014 /Published online: 1 April 2015
Abstract Nanoparticles (NPs) are commonly used, and
concerns about their possible adverse effects are being
voiced as well. However, little is known about the fates
of NPs released to the environment. The aim of the study
was to (i) evaluate the ability of Sinapis alba and
Lepidium sativum plants to take up platinum nanoparti-
cles (Pt-NPs) and translocate them to aboveground or-
gans, (ii) compare the accumulation efficiency of differ-
ent forms of platinum and (iii) identify the forms in
which platinum is stored in plant tissues. Plants were
cultivated on medium supplemented with different con-
centrations of Pt-NPs and [Pt(NH
3
)
4
](NO
3
)
2
. Platinum
content in plants was determined using inductively
coupled plasma mass spectrometry. For the identification
of the presence of Pt-NPs in plant tissues, gamma spec-
trometry following iron irradiation was applied. It
was found that L. sativum and S. alba are tolerant to
applied concentrations of Pt-NPs and have an ability to
take up platinum from the medium and translocate it to
aboveground organs. The highest concentration of plat-
inum was observed in plant roots (reaching 8.7 g kg
−1
for S. alba). We tentatively conclude that platinum is
accumulated as nanoparticles. The obtained results
suggest future application of plants for phytoremediation
and recovery of noble metal nanoparticles.
Keywords Platinum .Nanoparticles .Accumulation .
Plants .Sinapis alba .Lepidium sativum
1 Introduction
The unique properties of nanoscale materials, associated
with their high surface-to-volume ratio, have caused a
rapid increase in the implementation of nanotechnol-
ogies in the last 20 years. Many products based on
nanotechnologies are in everyday use now and many
more new ones are expected to appear on the market
soon (Maynard et al. 2006; Rejeski and Lekas 2008).
Nanoparticles of platinum (Pt-NPs) are of great scien-
tific interest as they have many industrial and biomed-
ical applications. Platinum is a rare element used in
jewellery and as a catalyst. In macro-size form, platinum
is not only one of the most effective but also very
expensive catalyst. As the catalytic reactivity depends
on the size and shape of particles, the effectiveness of
catalytic processes on nanoparticles is much higher be-
cause the reactive surface area increases significantly in
comparison with microparticles. Platinum nanoparticles
have also been used in biomedical applications
(Bhattacharya and Murkherjee 2008) and nanocrystals
of FePt@CoS
2
have been found to be more potent in
killing HeLa cells than cis-platinum (Gao et al. 2007).
Nanoscale platinum is suitable for designing new elec-
trochemical sensors and biosensors (Luo et al. 2006).
Water Air Soil Pollut (2015) 226: 126
DOI 10.1007/s11270-015-2381-y
M. Asztemborska (*):R. Steborowski :
G. Bystrzejewska-Piotrowska
Isotope Laboratory, Facultyof Biology, University of Warsaw,
Miecznikowa 1, 02-096 Warsaw, Poland
e-mail: asztemborska@biol.uw.edu.pl
J. Kowalska
Faculty of Chemistry, University of Warsaw,
Pasteura 1, 02-093 Warsaw, Poland
#The Author(s) 2015. This article is published with open access at Springerlink.com
The wide range of applications of Pt-NPs creates a
growing demand for more efficient and cost-effective
processes for their synthesis. Platinum nanoparticles can
be made, e.g. by reduction of hexachloroplatinate (Devi
and Rao 2000). Biological methods for nanoparticle
synthesis using microorganisms, plants or plant extracts
are very attractive and eco-friendly alternative to chem-
ical and physical methods (Konishi et al. 2007;
Mohanpuria et al. 2008; Kaushik et al. 2010;Song
et al. 2010).
One of the side effects of the growing application of
nanotechnologies is the release of nanomaterials to the
environment and the creation of a new type of waste,
containing residue nanomaterials—nanowaste
(Bystrzejewska-Piotrowska et al. 2009). This calls for
a comprehensive investigation of the uptake, bioaccu-
mulation and biotransformation of nanomaterials and
the risks associated with their use. Efficient removal of
NPs from the contaminated environment may prevent
their ecotoxicity (Oberdorster et al. 2005). Additionally,
recovery of nanoparticles of noble metals from the con-
taminated wastewater, water or soil is economically
justified. Here, phytoremediation techniques seem
promising as they enable both decontamination of the
environment and recovery of the nanoparticles, being
simultaneously eco-friendly and relatively cost-effective
(Kidd et al. 2009;Paz-AlbertoandSigua2013). Cost
estimates indicate savings for a phytoremediation com-
pared to a conventional treatment to be 50 to 80 %
depending on contaminant, matrix and applied remedi-
ation techniques (Environmental Protection Agency
2000, EPA/600/R-99/107).
The ability of platinum uptake by hydroponically
cultivated plants—Indian mustard (Sinapis alba L.)
and Anawa maize (Zea mays L.)—was investigated by
Kowalska et al. (2004a,b) and Hawienczyk et al.
(2005). It was found that both studied plant species
poses tolerance to relatively high inorganic Pt concen-
tration(upto500mgPtL
−1
in a form of
[Pt(NH
3
)
4
](NO
3
)
2
) and efficiently uptake and transport
platinum to aboveground parts. The platinum content:
exciding 400 and 200 mg kg
−1
for roots of Indian
mustard and Anawa maize, respectively, and about 40
and 10 mg kg
−1
for aboveground organs of both species
were found. It is known that some plant species are
hyperaccumulators of platinum, but information on the
bioaccumulation of Pt nanoparticles is lacking. Zhu
et al. (2008) showed that iron oxide nanoparticles
(Fe
3
O
4
) were taken up by Cucurbita maxima roots and
translocated through the plant tissues while no uptake or
transport of iron oxide nanoparticles was observed for
Phaseolus limensis. We reported accumulation of iron
oxide nanoparticles by Lepidium sativum
(Bystrzejewska-Piotrowska et al. 2012). Lin et al.
(2009) found that C70 fullerene not only could be easily
taken up by the roots of Oryza sativa and transported to
shoots but also could be transported downward from
leaves to roots through the phloem if itentered the plants
through the leaves. Other studies indicated no upward
translocation of ZnO nanoparticles from Lolium perenne
roots to shoots (Lin and Xing 2008). For metallic nano-
particles, Cu nanoparticles could be taken up and accu-
mulated by bean and wheat plants (Lee et al. 2008).
The aim of the present study was to evaluate the
ability of S. alba and L. sativum plants to take up
platinum nanoparticles and translocate them to above
ground organs. In our previous studies, we have shown
that S. alba accumulates platinum (Kowalska et al.
2004a,b; Hawienczyk et al. 2005)whileL. sativum
can accumulate iron oxide nanoparticles
(Bystrzejewska-Piotrowska et al. 2012). Additionally,
we compared the accumulation efficiency of different
forms of platinum and attempted to identify the forms in
which it is stored in plant tissues.
2MaterialsandMethods
Platinum nanoparticles (Pt-NPs, nanopowder, particle
size <50 nm (TEM), spec. surface area BET 98 m
2
/g)
were purchased from Sigma-Aldrich. According to the
Material Safety Data Sheet, platinum nanoparticles may
be harmful if inhaled (causing respiratory tract irrita-
tion), absorbed through skin (skin irritation) and may
cause eye irritation. Safety glasses, gloves, protective
clothing and air-purifying respirators were used during
handling of platinum nanoparticles.
Theparticlesizeandmorphologywereassessed
using LEO 912AB transmission electron microscope
(Zeiss) equipped with a Proscan High Speed Slow
Scan CCD camera. The TEM analysis was performed
using 20 mg L
−1
water suspensions. The platinum com-
plex [Pt(NH
3
)
4
](NO
3
)
2
was from Sigma-Aldrich. The
chemicals used for preparation of plant nutrient solu-
tions were from Avantor Performance Materials Poland
S.A., Poland. All solutions were prepared in 18 MΩcm
Milli-Q water (Millipore, USA). All solutions of nano-
particles were sonicated for 30 min.
126 Page 2 of 7 Water Air Soil Pollut (2015) 226: 126
For irradiation, samples of Pt nanoparticles (80–
100 mg) were weighed directly into HDPE snap-cap
capsules (Faculteit Biologie, Vrije Universiteit,
Amsterdam), wrapped in aluminium foil and irradiated
at the MARIA nuclear reactor (Świerk, Poland) for
10 min at a thermal neutron flux of 10
14
cm
−2
s
−1
.
After 10 days of cooling, the samples were unwrapped
and used for plant cultivation. The purity of irradiated
nanoparticles was confirmed using a GENIE-2000
gamma-ray spectrometer (Canberra Gamma
Spectrometry System) with an HPGe detector
(Canberra), active volume 255 cm
3
, well type, well
diameter 16 mm and depth 40 mm, resolution 2.4 keV
for the 1,332.4 keV peak of
60
Co and relative efficiency
24 %.
L. sativum plants were cultivated for 3 days in
300-mL containers (50 plants/container) with distilled
water. After that time, the plants were transferred to the
growth medium supplemented with Pt nanoparticles at
concentrations 0 (control), 1, 10 or 100 mg L
−1
.
Cultivation was carried out for the next 5 days. In
experiments with irradiated Pt-NPs (final concentration
85 mg L
−1
), the cultivation was 2 days only due to the
short half-life time of the isotopes.
S. alba L. was cultivated in 1.5-L containers (20
plants/container) according to the procedure described
elsewhere (Kowalska et al. 2004b). In the first experi-
ment, the nutrient solution was supplemented with Pt-
NPs at 0 (control), 1, 10 or 50 mg L
−1
. The second
experiment cultivation was performed in two variants.
Platinum was added to the nutrient solution to a final
concentration of 1 mg L
−1
as inorganic salt or as nano-
particles. S. alba plants were cultivated for 3 weeks.
After cultivation as above, the plants were harvested,
roots were washed with deionized water and plants were
divided into roots and shoots, which were than dried and
ground.
For analysis of platinum content, plant samples were
acid-digested using ETHOS 1 microwave laboratory
system with an ATC-400-CE automatic temperature
control (Milestone, Italy). About 250 mg of dried sam-
ple was weighed into a PTFE vessel and 3 mL of aqua
regia was added (65 % HNO
3
and 37 % HCl, both from
Merck). After digestion, samples were transferred quan-
titatively into volumetric flasks and brought up to 25 mL
with water. Samples were analyzed by inductively
coupled plasma mass spectrometry ICP MS (ELAN
6000 ICP mass spectrometer (PE-SCIEX, Concord,
Canada)).
The radionuclide content (energy line 81.00 keV)
was determined in dried plant samples by means of a
gamma spectrometer with an HPGe detector (Canberra
Packard).
3 Results and Discussions
Before uptake experiments, we characterize the plati-
num nanoparticles in standard solution using transmis-
sion electron microscopy (Fig. 1). Most particles were
spherical, and their size did not exceed 50 nm in agree-
ment with the declaration of the supplier.
The L. sativum and S. alba plants appeared tolerant to
the applied relatively high concentrations of Pt-NPs
because no visible phytotoxic effects were observed.
The colour of the plants, biomass production, root sys-
tem or tissues hydration did not differ substantially
between the control and the Pt-NP-exposed plants.
However, detailed tests for possible phytotoxic effects
on the cellular level were not undertaken.
Both plant species investigated took up platinum NPs
from the medium in considerable amounts. It was found
in both roots and shoots, although at markedly different
concentrations (Table 1). In both species, the roots
contained significantly higher concentration (per dry
weight) of platinum than shoots.
Fig. 1 Transmission electron micrograph of Pt nanoparticles
(20 mg L
−1
suspension in water). Scale bar 500 nm
Water Air Soil Pollut (2015) 226: 126 Page 3 of 7 126
L. sativum exposed to the highest Pt-NPs concentra-
tionapplied(100mgL
−1
) accumulated almost
7.5gkg
−1
of platinum in roots. In plants grown on the
medium with Pt-NPs at 1 or 10 mg L
−1
, the amount of
platinum in roots was about 50 and 40 times lower,
respectively. The platinum content in shoots clearly
depended on the Pt-NP content in medium, and for the
highest platinum concentration applied, it reached near-
ly 0.6 g kg
−1
. The efficiency of platinum accumulation,
defined as transfer factor (TF; platinum concentration in
plants [mg kg
−1
dry weight] divided by that in growth
medium [mg L
−1
]) decreased with the increase of parti-
cle concentration, both for shoots and roots of
L. sativum.
The accumulation of platinum in shoots of S. alba
exposed to Pt-NPs at 1 or 10 mg L
−1
was similar for
L. sativum cultivated in the same media, while for the
highest concentration of platinum nanoparticles used, it
was about 10 times lower than that in L. sativum.The
platinum content in roots of S. alba was significantly
higher in comparison with L. sativum. The TF decreased
with the increase of NP concentration for shoots, but
was constant for roots.
At the lowest concentration of Pt-NPs in the growth
medium, 1 mg L
−1
,95%oftheNPstakenupby
L. sativum accumulated in roots and only 5 % in the
shoot (Fig. 2). At the highest concentration, the fraction
of platinum translocated to the shoot increased signifi-
cantly to ca. 20 %. S. alba accumulated Pt mainly in
roots (∼95 %) as well, regardless of the Pt-NPs concen-
tration used. A comparison of the results for the two
plant species shows that they differ substantially at the
efficiency and mode of Pt-NPs uptake and transport.
Similar species specificity was reported earlier for a
number of plant species and diverse metals (Lee et al.
2008; Lin and Xing 2008; Zhu et al. 2008; Lin et al.
2009; Bystrzejewska-Piotrowska et al. 2012).
Further experiments focused on efficiency of the
platinum accumulation depending on its form in the
growth medium. S. alba was exposed to 1 mg L
−1
of
platinum in the form of nanoparticles or an inorganic
water soluble salt. As expected, in plants exposed to the
salt, the amounts of platinum were about 220, 30 and 3
times higher for leaves, stems and roots, respectively,
than in plants exposed to nanoparticles (Table 2). S. alba
cultivated on the Pt salt-contaminated medium accumu-
lated more than 60 % of platinum in shoots, while in
plants grown on medium with NPs, only 15 % of
platinum was transported to aboveground organs
(Fig. 3). These results confirm a better bioavailability
of metals from a salt than from nanoparticles. However,
it must be stressed that the platinum transport from the
medium to shoots is much more effective for the salt,
while the accumulation inroots is only twice higher. The
rather high amount of platinum found in roots exposed
to Pt-NPs and its poor upward transport are partly
caused by adsorption of the nanoparticles on the root
surface. The adsorption of platinum nanoparticles on the
root surface was macroscopic—visible without the use
of any equipment.
Relatively high amount of platinum in plants exposed
to nanoparticles does not answer the question whether
the platinum is taken up as nanoparticles. During further
studies, we sought the presence of platinum ions in the
growth medium and plants. For this purpose, growth
media (kept under experimental conditions with or with-
out plants) and water plant extracts were filtered and
ultracentrifuged, and the amount of platinum in the
Tabl e 1 Pt content and transfer factors for Lepidium sativum and Sinapis alba. Values given are mean±SD; n≥3
Pt-NPs concentration in medium (mg L
−1
) Pt content in plants (mg kg
−1
) (transfer factor)
Lepidium sativum Sinapis alba
Shoots Roots Shoots Roots
1 3.1± 0.3 (3.1) 148± 12 (148) 3.5± 0.3 (3.5) 190±15 (190)
10 17.6±1.1 (1.8) 179±16 (17.9) 16.5±1.0 (1.7) 1,855± 166 (185)
100/50
a
563± 33 (0.5) 7,460±516 (7.5) 54±3 (1.1) 8,752± 605 (175)
85
b
3.9± 0.4 (0.04) 278±33 (3.3) ––
TF platinum concentration in plants [mg kg
−1
dry weight] divided by that in the growth medium [mg L
−1
]
a
100mgL
−1
for L. sativum and 50 mg L
−1
for S. alba
b
Cultivation time 48 h; irradiated Pt-NPs
126 Page 4 of 7 Water Air Soil Pollut (2015) 226: 126
supernatant was determined. It was below the detection
limit, so no or very little Pt ions originating from nano-
particles are present in the medium or in the plants.
The problem of nanoparticle accumulation by plants
is very complex because in plant cells, many different
processes can take place. For instance, taking into con-
sideration that some plants can reduce metal ions to
elemental NPs inside their tissues (Harris and Bali
2008; Bali et al. 2010), we can expect that even if
platinum was taken up as ions, it could be present as
NPs in plant cells. In short, nanoparticles accumulated in
plants can potentially come from two sources—direct
accumulation of nanoparticles and reduction of metal
ions taken up.
As an excellent tool for tracing the environmental fate
of NPs and their uptake and accumulation in organisms
(Oughton et al. 2008; Bystrzejewska-Piotrowska et al.
2012), gamma spectrometry following neutron
activation of platinum was used for Pt-NP analysis in
plant tissues. Details of the procedure are described
elsewhere (Bystrzejewska-Piotrowska et al. 2012).
This method was previously successfully applied for
analysis of accumulation of Fe
3
O
4
nanoparticles by
Lepidium sativum
0%
20%
40%
60%
80%
100%
1 10 100 85*
Pt-NPs concentration in medium mg/L
Sinapis alba
0%
20%
40%
60%
80%
100%
11050
Pt-NPs concentration in medium mg/L
Fig. 2 Distribution of platinum between roots and shoots of Lepidium sativum and Sinapis alba
Tabl e 2 Pt content and transfer factors for Sinapis alba exposed
to platinum in the form of [Pt(NH
3
)
4
](NO
3
)
2
or Pt-NPs. Platinum
concentration in medium was in both case 1 mg L
−1
. Values given
are mean±SD; n≥3
Pt content in plants (mg kg
−1
) (transfer factor)
Pt(NH
3
)
4
](NO
3
)
2
Pt-NPs
Leaves 120± 4 (120) 0.55± 0.20 (0.6)
Stems 215± 6 (215) 6.8± 4.3 (6.8)
Roots 384± 4 (384) 145± 14 (145)
TF platinum concentration in plants [mg kg
−1
dry weight] divided
by that in the growth medium [mg L
−1
]
0%
20%
40%
60%
80%
100%
Pt-NPs Pt-salt
.
Fig. 3 Distribution of platinum between roots and shoots of Sinapis
alba exposed to platinum in the form of [Pt(NH
3
)
4
](NO
3
)
2
or Pt-
NPs. Platinum concentration in medium was in both case 1 mg L
−1
Water Air Soil Pollut (2015) 226: 126 Page 5 of 7 126
L. sativum (Bystrzejewska-Piotrowska et al. 2012). The
activity measured in the plant samples was within the
range 1.2 kBq g
−1
(shoots)–426.5 kBq g
−1
(roots), so we
could expect that Pt nanoparticles were present in plants.
The amount of platinum in L. sativum after only 2 days
of cultivation was about 4 and 280 mg kg
−1
for shoots
and rots, respectively, showing that the NPs are vigor-
ously taken up by plants from the first days of
cultivation.
On the basis of the obtained results, some general
conclusions can be drawn. Both plant species can be
potentially used for phytoremediation of the environ-
ment contaminated with platinum nanoparticles. The
higher biomass production makes S. alba better for that
purpose. Plants can also be used to recover nanoparticles
from the environment. It is especially important in the
case of platinum—a very useful and a very expensive
metal. We can also conclude that, as for the question of
environment contamination is concerned, nanoparticles
are much safer than inorganic forms of platinum are.
Accumulation in aboveground organs is 200 times less
for NPs than for platinum ions. Although appropriate
experiments were not performed here, one can safely
assume that the low accumulation of platinum nanopar-
ticles in the stem results in a negligible metal accumu-
lation in seeds. In conclusion, the chances of NPs enter-
ing the food chain are much lower in comparison with
ionic platinum.
Finally, it must be stressed that plants have an ability
to reduce platinum ions to form nanoparticles (Song
et al. 2010;Balietal.2010). Plant extracts are used for
Pt-NP synthesis as a very promising and ecologically
safe procedure. It is likely that ionic platinum that is
taken up can be transformed in plant cells to metallic
platinum in the form of individual nanoparticles. The
conditions in plant tissues favour accumulation of
nanoparticles.
During the presented studies, it was found that
L. sativum and S. alba aretoleranttorelativelyhigh
concentrations of Pt-NPs and have an ability to take up
platinum from the medium and translocate it to above-
ground organs. However, in both of these species, ca.
90 % remains associated with the roots. The efficiency
of platinum accumulation depends on its form and is
different for the two plant species. We propose that
platinum is accumulated as nanoparticles. The obtained
results give a perspective for future application of plants
for environment phytoremediation and recovery of no-
ble metal nanoparticles.
Acknowledgments This work was supported by The Ministry
of Science and Higher Education, Poland Grant No. N304 077535.
Open Access This article is distributed under the terms of the
Creative Commons Attribution License which permits any use,
distribution, and reproduction in any medium, provided the orig-
inal author(s) and the source are credited.
References
Bali, R., Siegele, R., & Harriset, A. T. (2010). Biogenic Pt uptake
and nanoparticle formation in Medicago sativa and Brassica
juncea. Journal of Nanoparticle Research, 12,3087–3095.
Bhattacharya, R., & Murkherjee, P. (2008). Biological properties
of “naked”metal nanoparticles. Advanced Drug Delivery
Reviews, 60,1289–1306.
Bystrzejewska-Piotrowska, G., Golimowski, J., & Urban, L.
(2009). Nanoparticles: their potential toxicity, waste and
environmental management. Waste Management, 29(9),
2587–2595.
Bystrzejewska-Piotrowska, G., Asztemborska, M., Steborowski,
R., Ryniewicz, J., Polkowska-Motrenko, H., & Danko, B.
(2012). Application of neutron activaton for investigation of
Fe
3
O
4
nanoparticles accumulation by plants. Nukleonika,
57(3), 427–430.
Devi, G. S., & Rao, V. J. (2000). Room temperature synthesis of
colloidal platinum nanoparticles. Bulletin of Materials
Science, 23(6), 467–470.
Environmental Protection Agency, USA, (2000) Introduction to
phytoremediation, EPA/600/R-99/10, 2000.
Gao, J., Liang, G., Zhang, B., Kuang, Y., Zhang, X., & Xu, B.
(2007). FePt@CoS2 yolk-shell nanocrystals as a potent agent
to kill HeLa cells. Journal of the American Chemical Society,
129,1428–1433.
Hawienczyk, M., Bystrzejewska-Piotrowska, G., Kowalska, J., &
Asztemborska, M. (2005). Platinum bioaccumulation by
mustard plants (Sinapis alba L.). Nukleonika, 50,S59–S61.
Harris, A. T., & Bali, R. (2008). On the formation and extent of
uptake of silver nanoparticles by live plants. Journal of
Nanoparticles Research, 10, 691–695.
Kaushik, N., Thakkar, M. S., Snehit, S., Mhatre, M. S., Rasesh, Y.,
& Parikh, M. S. (2010). Biological synthesis of metallic
nanoparticles. Nanomedicine: Nanotechnology, Biology and
Medicine, 6,257–262.
Kidd, P., Barcelo, J., Bernal, M. P., Navari-Izzo, F., Poschenrieder,
C., Shilev, S., Clementec, R., & Monterroso, C. (2009). Trace
element behaviour at the root–soil interface: implications in
phytoremediation. Environmental and Experimental Botany,
67(1), 243–259.
Konishi, Y., Ohno, K., Saitoh, N., Nomura, T., Nagamine, S.,
Hishida, H., Takahashi, Y., & Uruga, T. (2007).
Bioreductive deposition of platinum nanoparticles on the
bacterium Shewanella algae. Journal of Biotechnology,
128,648–653.
Kowalska, J., Huszał, S., Sawicki, M. G., Asztemborska, M.,
Stryjewska, E., Szalacha, E., Golimowski, J., & Gawroński,
S. W. (2004a). Voltammetric determination of platinum in
plant material. Electroanalysis, 16(15), 1266.
126 Page 6 of 7 Water Air Soil Pollut (2015) 226: 126
Kowalska, J., Asztemborska, M., & Bystrzejewska-Piotrowska,
G. (2004b). Platinum uptake by mustard (Sinapis alba L.)
and maize (Zea mays L.). Nukleonika, 49,S31–S34.
Lee, W., An, Y., Yoon, H., & Kweon, H. (2008). Toxicity and
bioavailability of copper nanoparticles to the terrestrial plants
mung bean (Phaseolus radiatus) and wheat (Triticum
awstivum): plant uptake for water insoluble nanoparticles.
Environmental Toxicology and Chemistry, 27(9), 1915–1921.
Lin, D., & Xing, B. (2008). Root uptake and phytotoxicity of ZnO
nanoparticles. Environmental Science and Technology, 42,
5580–5585.
Lin, S., Reppert, J., Hu, Q., Hunson, J. S., Reid, M. L., & Ratnikova,
T. (2009). Uptake, translocation and transmission of carbon
nanomaterials in rice plants. Small, 5(10), 1128–1132.
Luo, X., Morrin, A., Killard, A. J., & Smyth, M. R. (2006).
Application of nanoparticles in electrochemical sensors and
biosensors. Electroanalysis, 18(4), 319–326.
Maynard, A. D., Aitken, R. J., Butz, T., Colvin, V., Donaldson, K.,
Oberdorster, G., Philbert, M. A., Ryan, J., Seaton, A., Stone,
V., Tinkle, S. S., Tran, L., Walker, N. J., & Warheit, D. B.
(2006). Safe handling of nanotechnology. Nature, 444,267–
269.
Mohanpuria, P., Rana, N. K., & Yadav, S. K. (2008). Biosynthesis
of nanoparticles: technological concepts and future applica-
tions. Journal of Nanoparticle Research, 10,507–517.
Oberdorster, G., Maynard, A., Donaldson, K., Castranova, V.,
Fitzpatrick, J., Ausman, K., Carter, J., Karn, B., Kreyling,
W., Lai, D., Olin, S., Monteiro-Riviere, N., Warheit, D., &
Yang, H. (2005). Principles for characterizing the potential
human health effects from exposure to nanomaterials: ele-
ments of a screening strategy. Particle and Fibre Toxicology,
2,8–43.
Oughton, D.H., Hertel-Aas, T., Pollicer, E., Mendoza, E.,& Joner,
E. J. (2008). Neutron activation of engineered nanoparticles
as a tool for tracing their environmental fate and uptake in
organisms. Environmental Toxicology and Chemistry, 27(9),
1883–1887.
Paz-Alberto, A. M., & Sigua, G. C. (2013). Phytoremediation: a
green technology to remove environmental pollutants.
American Journal of Climate Change, 2,71–86.
Rejeski, D., & Lekas, D. (2008). Nanotechnology field observa-
tions: scouting the new industrial west. JournalofCleaner
Production, 16,1014–1017.
Song, J. Y., Kwon, E. Y., & Kim, B. S. (2010). Biological synthe-
sis of platinum nanoparticles using Diospyros kaki leaf ex-
tract. Bioprocess and Biosystems Engineering, 33,159–164.
Zhu, H., Han, J., Xiao, J. Q., & Jin, Y. (2008). Uptake, transloca-
tion and accumulation of manufactured iron oxide nanopar-
ticles by pumpkin plants. Journal of Environmental
Monitoring, 10,713–717.
Water Air Soil Pollut (2015) 226: 126 Page 7 of 7 126
