J Nanopart Res (2013) 15:1896
DOI 10.1007/s11051-013-1896-7
REVIEW
Silver nanoparticles in soil–plant systems
Naser A. Anjum • Sarvajeet S. Gill •
Armando C. Duarte • Eduarda Pereira •
Iqbal Ahmad
Received: 8 June 2013 / Accepted: 22 July 2013
Ó Springer Science+Business Media Dordrecht 2013
Abstract Silver nanoparticles (AgNPs) have broad
spectrum antimicrobial/biocidal properties against all
classes of microorganisms and possess numerous
distinctive physico-chemical properties compared to
bulk Ag. Hence, AgNPs are among the most widely
used engineered NPs in a wide range of consumer
products and are expected to enter natural ecosystems
including soil via diverse pathways. However, despite:
(i) soil has been considered as a critical pathway for
NPs environmental fate, (ii) plants (essential base
component of all ecosystems) have been strongly
recommended to be included for the development of a
comprehensive toxicity profile for rapidly mounting
NPs in varied environmental compartments, and (iii)
the occurrence of an intricate relationship between
‘‘soil–plant systems’’ where any change in soil
N. A. Anjum (&)  A. C. Duarte  E. Pereira  I. Ahmad
CESAM-Centre for Environmental and Marine Studies,
Department of Chemistry, University of Aveiro,
3810-193 Aveiro, Portugal
e-mail: anjum@ua.pt
S. S. Gill
Stress Physiology and Molecular Biology Lab, Centre for
Biotechnology, Faculty of Life Sciences, MD University,
Rohtak 124001, India
I. Ahmad (&)
CESAM-Centre for Environmental and Marine Studies,
Department of Biology, University of Aveiro,
3810-193 Aveiro, Portugal
e-mail: ahmadr@ua.pt
chemical/biological properties is bound to have
impact on plant system, the knowledge about AgNPs
in soils and investigations on AgNPs–plants interac-
tion is still rare and in its rudimentary stage. To this
end, the current paper: (a) overviews sources, status,
fate, and chemistry of AgNPs in soils, AgNPs-impact
on soil biota, (b) critically discusses terrestrial plant
responses to AgNPs exposure, and (c) illustrates the
knowledge-gaps in the current perspective. Based on
the available literature critically appraised herein, a
multidisciplinary integrated approach is strongly rec-
ommended for future research in the current direction
aimed at unveiling the rapidly mounting AgNPs-fate,
transformation, accumulation, and toxicity potential in
‘‘soil–plant systems,’’ and their cumulative impact on
environmental and human health.
Keywords Silver  Nanoparticle  Soil–plant
systems  Phytotoxicity  Tolerance
Introduction
Engineered nanoparticles (NPs)-based technologies
have fascinated almost every walk of life. However, a
credible number of recent studies have demonstrated
that not all engineered NPs are inherently benign and
also their indiscriminate multidisciplinary applica-
tions can be fatal for both environmental and human
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Page 2 of 26
health. Owing to the growing markets for engineered
NPs-based products, the annual production of engi-
neered NPs is increasing at war level. Nevertheless,
this trend has been expected to lead to the appearance
of varied NPs in air, water, soils, and organisms
(Blaser et al. 2008; Mueller and Nowack 2008;
Navarro et al. 2008; Ma et al. 2010). According to a
recent estimate, 63–91 % of over 260,000–309,000
metric ton of global engineered NP-production in the
year 2010 ended up in landfills, with the balance
released into soils (8–28 %), water bodies (0.4–7 %),
and atmosphere (0.1–1.5 %) (Keller et al. 2013).
Among a credible number of NPs, metallic NPs have a
high specific surface area and a high surface-to-
volume ratio besides exhibiting unique electrical,
chemical, optical, and photo-electrochemical proper-
ties, and can be easily synthesized and modified
chemically. Hence, metallic NPs have enchanted
researchers from multiple disciplines including phys-
ics, chemistry, electronics, and biology (Lanje et al.
2010). Nevertheless, the Woodrow Wilson Interna-
tional Centre for Scholars product inventory of
nanomaterials, indicated that 1,015 different nano-
containing products were on the market in 2009, and
these products mostly involved metal-based NPs
(http://www.nanotechproject.org/inventories/consumer/
analysis_draft). Thus, as a result of multidisciplinary
applications (such as electronics, optics, textiles, medical
applications, cosmetics, food packaging, water-treat-
ment technology, fuel cells, catalysts, biosensors and
agents for environmental remediation), exposure of
varied metallic NPs to the environment and humans is
becoming increasingly widespread which needs an
urgent and exhaustive evaluation (Handy et al. 2008;
Thakkar et al. 2010; Gerloff et al. 2012; Luque-Garcia
et al. 2013). Additionally, NPs are extensively used or
tried for environmental (soil, water) remediation (Zhang
et al. 2013; Ngomsik et al. 2005; Uheida et al. 2006),
where information on their fate and impact is largely
limited. Varied NPs, thus released to the atmosphere,
may be deposited in the soil where they can persist for a
long time or be taken up by biological organisms; hence,
can act as ecotoxicological hazard, undergo biodegra-
dation or bio-accumulate in the food chain (SCENIHR
2006; Bystrzejewska-Piotrowska et al. 2009). Since
there always exist difficulties in the evaluation of
potential toxic effects of majority of NPs, their multi-
disciplinary uses represent important toxicological risks
to both environmental and human health. Nevertheless,
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J Nanopart Res (2013) 15:1896
biotic communities interaction with varied environ-
mental compartments contaminated potentially with
NPs may cause bioaccumulation where subsequent
exposure of higher level organisms to NPs through food
chain cannot be ignored (Blaser et al. 2008; Navarro et al.
2008; Ma et al. 2010; Priester et al. 2012; Rico et al.
2011, 2013).
Silver nanoparticles (AgNPs)
AgNPs have a size range from 1 to 100 nm and consist
of about 20–15,000 Ag atoms. Compared to bulk Ag, a
number distinctive physico-chemical properties such
as a high electrical and thermal conductivity, surface-
enhanced Raman scattering, chemical stability, cata-
lytic activity and nonlinear optical behavior make
AgNPs unique (Frattini et al. 2005; Warheit et al.
2007; Chen and Schluesener 2008; Wijnhoven et al.
2009; Fabrega et al. 2011). In addition, AgNPs possess
large surface area-to-volume ratio, exhibit a better
contact with the microorganism and are known potent
and broad spectrum antibacterial agents with activity
against diverse species within both Gram-positive and
Gram-negative bacteria (Morones et al. 2005; Kim
et al. 2007; Lee et al. 2007; Vigneshwaran et al. 2007;
Marambio-Jones and Hoek 2010). AgNPs can form
different nanoshapes, like nanocylinders, nanorods,
nanowires, nanoplates, or nanobelts (Sun et al. 2003;
Pal et al. 2007; Wiley et al. 2007; Jana et al. 2012; Kim
et al. 2012; reviewed by Schluesener and Schluesener
2013). Nevertheless, AgNPs can be nanoscale in zero
dimension (atomic clusters, filaments and cluster
assemblies), one dimension (surface films, multilay-
ers), two dimensions (strands, ultrafine-grained over-
layers or buried layers and fibers), or three dimensions
(particles, nanophase materials consisting of equiaxed
nanometer sized grains) (Golovina and Kustov 2013).
Since several pathogenic bacteria have developed
resistance against various antibiotics, metallic Ag in the
form of AgNPs has made a remarkable comeback as a
potential antimicrobial agent. Hence, AgNPs have
emerged up with diverse medical applications ranging
from Ag-based dressings, Ag-coated medicinal devices,
such as nanogels, nanolotions, etc. (Rai et al. 2009).
Nevertheless, AgNP-products have been claimed earlier
to ‘‘eliminate 99 % of bacteria’’ render material ‘‘per-
manently antimicrobial and antifungal’’ ‘‘kill approxi-
mately 650 kinds of harmful germs and viruses’’ and
‘‘kill bacteria in a short time as 30 min and can be
J Nanopart Res (2013) 15:1896
effective 2–5 times faster than other forms of Ag
(Shahrokh and Emtiazi 2009). Moreover, since Ag ions
attack various proteins in cells, these ions have widely
been used as antifungal and antimicrobial agents
(Panáček et al. 2009) and also to increase the efficacy
of antiseptics (Golubeva et al. 2010). Hence due mainly
to remarkable antimicrobial properties, AgNPs are one
of the most widely used engineered NPs in over 250
consumer products including antimicrobial agent in
domestic appliances (e.g., fridges, vacuum cleaners, air
conditioning), paints, textiles/fabrics, plastics, varnish,
clothes, socks and laboratory gowns, as well as in
medical products, such as surgical gowns and dressing
bandages (Boxall et al. 2007; Kim et al. 2007; Blaser
et al. 2008; Klaine et al. 2008; Ma et al. 2010). However,
US-EPA (2008) has classified all products containing
nanoscale Ag as pesticides and also recommended the
analysis of their potential risks to human and environ-
mental health. Nevertheless, Ag? and/or AgNPs com-
posites are also widely applicable in various agricultural
activities including for the control of various phyto-
pathogens and for plant disease management (Liu et al.
2002; Park et al. 2006; Jo et al. 2009). It was reported
that about 25 % of the [1,300 NPs-containing con-
sumer products contain AgNPs (Yu et al. 2013).
Recently, Nowack et al. (2011) have reported the
current production and industrial use of about 320 ton
AgNPs per year. Nevertheless, the number of the AgNP-
containing products has already been increased from 30
in 2006 to over 300 at the beginning of 2011; whereas
the use of 1,120 ton of AgNP has been estimated until
2015 (Stensberg et al. 2011). It has also been reported
that the number of consumer products with AgNPs
surpassed threefold that of the succeeding component
as of March 2011 (http://www.nanotechproject.org/
inventories/consumer/analysis_draft). In the United
States only, a production of AgNPs between 2.8 and
20 ton year-1 has been estimated (Hendren et al.
2011). Moreover, though, the National Institute for
Occupational Safety and Health has considered
0.01 mg-1 m-3 as permitted exposure limit for all
forms of Ag (NIOSH 1992) but severe damages were
reported in mammalian models at levels lower than
the permissible one (Kim et al. 2008; Sung et al.
2009). In this context, a separate review has been
strongly advocated for AgNP-exposure (Kulthong
et al. 2010).
Owing to a wide use in a vast number of AgNP-
based consumer products, the entry of AgNPs into
Page 3 of 26
varied environmental compartments including soil–
plant systems and subsequently to human food chain
may increase manifolds. Unfortunately, due to their
nanoscale size, high reactivity and ill-defined disso-
lution properties, AgNPs’ environmental risks were
considered very difficult to determine (Benoit et al.
2013). Of particular concern is whether there are new
risks that are a direct consequence of their nanoscale
size. In addition, the identification of AgNPs potential
risks associated with their nanoscale structure has
been difficult due to the fundamental challenge of
detecting and monitoring nanoparticles in products or
the environment (Glover et al. 2011). To this end,
based on the Woodrow Wilson Database (2010) and
the review by Fabrega et al. (2011), Fig. 1 summarizes
AgNP-containing major products available in the
market.
Soil–plant systems
Soil has always been vital to humans and fundamental
to human health since it is the main resource for food
production and is the major source of trace elements
Creams and Cosmetics Items
32.4 %
Textiles and Clothing
18.0 %
Household Items
16.4 %
Air and Water Filters
12.3 %
Others
8.6 %
Detergents
8.2 %
Health Supplements
4.1 %
AgNPs-Containing Products
Fig. 1 Major products in the market containing silver nano-
particles (AgNPs). [Woodrow Wilson Database (March 2010);
modified from Fabrega et al. (2011)]
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entering the food chain. The ‘‘soil–plant systems’’ are
intricately linked where any change in soil chemical
and biological properties are bound to have impact on
plant growth, development and productivity. Environ-
mental buildup of engineered NPs could profoundly
alter soil-based food crop quality and yield. In
particular, majority of AgNPs released from consumer
products are expected to enter terrestrial ecosystems
through land-application of biosolids (Blaser et al.
2008). Where AgNPs have widely been reported to
threaten soil system-inhabitants including free-living
nitrogen-fixing bacteria and symbiotic relationships
involving fungi, bacteria, which cumulatively may
affect soil’s physico-chemical characteristics. Hence,
AgNPs may potentially alter ecosystem productivity
and biogeochemistry by negatively impacting ‘‘soil–
plant systems’’-lead vital ecosystem services (Klaine
et al. 2008; Navarro et al. 2008). Moreover, the
incorporation of wastewater-released AgNPs into
sewage sludge released and their subsequent spread
further on agricultural fields has been evidenced
(Blaser et al. 2008).
To the other, being essential base components of all
ecosystems and having sessile nature plants expose
huge interfaces to the air and soil environment, thus,
have greater chance to interact with rapidly mounting
varied NPs; where their possible toxicological impacts
and underlying basic mechanisms are speculative and
unsubstantiated (Navarro et al. 2008; Ma et al. 2010;
Dietz and Herth 2011). Moreover, earlier, information
on mode of interaction, uptake, accumulation and
impact on the bio-systems at various levels of NPs in
plants have been considered essential to device and
implement proper mitigation or control measures to
avoid nano-pollution hence to turn-out to be a serious
ecological deterioration (Navarro et al. 2008; Ma et al.
2010). In addition, extensive research on ‘‘soil–plant
systems’’-NPs interaction has also been strongly
advocated (Dietz and Herth 2011). However, much
less attention has been paid to soils, despite the
importance of this pathway; and also data on terrestrial
plants and other photosynthetic organisms are also
lacking (Navarro et al. 2008; Monica and Cremonini
2009; Benoit et al. 2013). Based on modeling
approaches and the use of probabilistic methods, the
‘‘predicted environmental concentrations’’ status val-
ues for soil and sludge-treated soils for Europe and the
United States (Gottschalk et al. 2009; Fabrega et al.
2011) have been summarized in Fig. 2a.
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J Nanopart Res (2013) 15:1896
However, despite the fact that: (a) soil system is the
ultimate sink of directly or indirectly released varied
NPs and may wide-open the most significant exposure
avenues for assessing potential environmental risk by
opening-up more chances for NPs-entry into food
webs and human access to contaminated agriculture
(Unrine et al. 2010; Pan and Xing 2012; Remédios
et al. 2012), (b) soil microbial consortia and plant
growth are closely related, and any perturbation in the
former can have significant consequences for ecosys-
tems and also influence by/also affect plant growth
(Davidson and Janssens 2006), (c) AgNP-interaction
with soil environment may yield changes in the
chemistry of AgNPs and/or that of soils which may,
in turn may control AgNP-stability, and consequently
their transport through the environment and availabil-
ity and subsequent toxicity to organisms (Benn and
Westerhoff 2008; Geranio et al. 2009; Kim et al. 2010;
Nowack 2010; Stone et al. 2010; Levard et al. 2012),
and (d) plants—being a critical component of ecosys-
tems, may significantly interact with NPs including
AgNPs and control their fate and transport in the
environment by accumulating them into their biomass
(Navarro et al. 2008; Ma et al. 2010; Dietz and Herth
2011; Rico et al. 2011, 2013) by serving a potential
pathway for AgNP-transport and bioaccumulation into
food chains (Rico et al. 2011, 2013; Priester et al.
2012), there exists a dearth of literature on AgNPs
chemistry modulation in a range of soil types and
subsequent AgNP-impact on terrestrial plants and soil
microbial communities (Navarro et al. 2008; Ma et al.
2010; Kumar et al. 2011; Cornelis et al. 2012; Coutris
et al. 2012a; Tourinho et al. 2012; Benoit et al. 2013).
Hence given the information paucity particularly on
AgNPs in ‘‘soil–plant systems,’’ considering recent
breakthroughs on AgNPs, the current paper: (a) over-
views sources, status, fate, and chemistry of AgNPs in
soils, AgNPs-impact on soil biota, (b) critically dis-
cusses terrestrial plant responses to AgNPs exposure,
and (c) illustrates the knowledge-gaps in the current
perspective.
Silver nanoparticles in soils
Sources and status
Though AgNPs can be generated spontaneously from
manmade objects but because of a multidisciplinary
J Nanopart Res (2013) 15:1896 Page 5 of 26

United States
Sludge treated soil: 1581 Sludge treated soil: 662

Europe Soil: 22 Soil: 8.3

AgNPs-Predicted Environmental
concentrations (PECs)
B

Soil Chemistry Particle Size

Major Factors Affecting

AgNPs-Toxicity

Particle Shape Particle Stability

Fig. 2 a Status of the values for predicted environmental and Fabrega et al. (2011)], and b the summary of major factors
concentrations (PECs; shown as mode, i.e., most frequent value) affecting silver nanoparticle (AgNP) toxicity. See text for
for Europe and the United States for soil and sludge-treated discussion
soils. [Base year 2008; modified from Gottschalk et al. (2009)

use, AgNPs may come to soils from the wet or dry
deposition of AgNPs suspended in air, or from point
sources such as production facilities, application of
organic wastes in agriculture, application of a plant
growth-promoting spray, sewage sludge recycling as a
fertilizer to agricultural soils, waste incineration plants
and landfill, or from nonpoint sources such as AgNPs-
containing consumer products (Mueller and Nowack
2008; Navarro et al. 2008; Benn et al. 2010; Bernhardt
et al. 2010; Glover et al. 2011; Coutris et al. 2012a, b;
VandeVoort et al. 2012). Nevertheless, on-site waste-
water management systems, biosolids application,
improper disposal, accidental spills, as well as the
application of AgNPs as an ‘‘organic’’ fertilizer/
pesticide may also significantly contaminate different
soils (Blaser et al. 2008; Walters 2011; Calder et al.
2012). However, as it can happen with other NPs,
accidental release during AgNP-production or AgNP-
transport is also possible. In addition, intentional
release of AgNP into soil system is also possible.
Despite our knowledge of potential environmental
release pathways of AgNPs, information on the
current budget for AgNPs in the soil system is lacking.
Moreover, despite AgNPs are credibly synthesized
following eco-friendly and cost-effective procedures
(Poliakoff et al. 2002; Sharma et al. 2009; Ahmed et al.
2013; Bhaduri et al. 2013; Khan et al. 2013; Rao and
Paria 2013), a huge amount of AgNPs are added
globally to varied environmental compartments
including soils. The current global production of
AgNPs has been estimated at about 500 ton per annum
(Mueller and Nowack 2008), and a steady increase on
the volume manufactured was predicted for the next
few years (Boxall et al. 2008). A higher extent of
partition of AgNPs has been expected into sewage
sludge contingent to advanced waste treatments (Bla-
ser et al. 2008). In this perspective, with the use of
sewage sludge, Mueller and Nowack (2008) projected
input of 1 lg kg-3 of AgNPs to agricultural land per
year. According to the Federal Environmental Agency
of Germany (Umweltbundesamt 2008), AgNPs-utili-
zation in Germany can be approximately estimated to
1,100 kg year-1. In the United States only, amounts in
the order of 2,500 ton year-1 have been reported, out

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of which 150 ton ended up in sewage sludge and
80 ton have been released into surface waters (Kha-
ydarov et al. 2009; El-Temsah and Joner 2012). Based
on the use of environmental exposure models and the
application of simple algorithms, Boxall et al. (2008)
estimated 0.43 lg Ag kg-1 of soil arising from con-
sumer products. Though incineration of annually
produced sewage sludge is performed (Gottschalk
et al. 2009) but in countries such as the United
Kingdom and United States, a large proportion of such
wastes is used as a fertilizer in agricultural soil
(Nicholson et al. 2003) which in turn may act as major
sources of AgNPs in agricultural soil system. More-
over, since natural background levels of Ag can be
considered very low, the quantity of AgNPs produced
has been considered as the main factor determining the
concentrations found in all environmental compart-
ments (Gottschalk et al. 2009; Johnson et al. 2011;
Tourinho et al. 2012). Hence, the exact disposal route
may strongly affect the amount of AgNPs that each
environmental compartment receives (Fabrega et al.
2011). However, despite soils are known to be exposed
to most manufactured NPs there is a paucity of
information on the availability of the methodology for
the assessment of their retention in soils, which in fact,
determines potential mobility and bioavailability
(Cornelis et al. 2010).
Silver nanoparticle chemistry versus soil
properties
Soil environment can act as a major sink for AgNPs
contributed by diverse pathways including on-site
wastewater management systems, biosolids applica-
tion, improper disposal, accidental spills, and the
application of AgNPs-constituted organic fertilizers/
pesticides (Blaser et al. 2008; Walters 2011; Calder
et al. 2012). Nevertheless, soils represent a solid
matrix and a relatively complex medium with which
NPs may interact and provide a good opportunity for
the understanding manufactured NP-physico-chemi-
cal behavior (Pan and Xing 2012; Tourinho et al.
2012). AgNP-properties (such as dispersibility,
agglomeration/aggregation, dissolution rate, aging,
size, surface area, transformation and charge, and
surface chemistry) can be modified by their interaction
with soil environments which in turn may control
AgNP-stability, and consequently their transport
through the environment and availability, and
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J Nanopart Res (2013) 15:1896
subsequent toxicity to organisms (Benn and Wester-
hoff 2008; Geranio et al. 2009; Kim et al. 2010;
Nowack 2010; Stone et al. 2010; Cornelis et al. 2012;
Coutris et al. 2012a; Levard et al. 2012; Tourinho et al.
2012; Benoit et al. 2013). To this end, however, a
comprehensive understanding of the distribution,
transformation, toxicity of AgNPs, and the signifi-
cance of soil system-physico-chemical variables in the
current context has been strongly considered impor-
tant to correctly forecast and/or understand their
benefits and risks to environmental and human health
(Calder et al. 2012; Yin et al. 2012; Yu et al. 2013).
Nevertheless, despite: (a) the importance of the soil as
the major pathway of terrestrial AgNP contamination,
and (b) the consideration of physico-chemical inter-
actions between soils and NPs has been strongly
advocated while studying the chemistry and behavior
of NPs including AgNPs hence to scientifically
extrapolate the effects of pure culture research to
realistic field scenarios (Yin et al. 2012), much less
attention has been paid to this end and also AgNP’s
fate, behavior and bioavailability particularly in soil
environment are largely unexplored and unsubstanti-
ated (Cornelis et al. 2012; Benoit et al. 2013; Wang
et al. 2013). Rather to date, most studies available in
the literature in the current context have examined the
AgNPs-fate and behavior in aquatic systems (Benn
and Westerhoff 2008; Mueller and Nowack 2008;
Geranio et al. 2009; Gottschalk et al. 2009; Kulthong
et al. 2010; Liu and Hurt 2010). Hence given the
above, a critical appraisal of the available recent
literature on the AgNPs chemistry modulation only
under soil environment is presented hereunder.
A number of variables, such as the particle size,
surface charge of AgNPs and the soil physico-
chemical traits largely govern the chemistry, fate,
and transport of AgNPs in soil system, and hence their
bioavailability and subsequent toxicity to biota (To-
laymat et al. 2010; Oromieh 2011; Shoults-Wilson
et al. 2011; Cornelis et al. 2012; Sagee et al. 2012;
VandeVoort et al. 2012; Benoit et al. 2013). A
differential AgNP retention has been evidenced in
suspensions of natural soils which was correlated
mainly with the clay content of the soil (Cornelis et al.
2012). The authors advocated the role of heterocoag-
ulation of AgNP with naturally occurring colloids to
explain this correlation. Various stabilizing agents
have been reported to modify AgNPs where their
mobility may be altered by the electrostatic interaction
J Nanopart Res (2013) 15:1896
with different soil types (Tolaymat et al. 2010). For
example, a positive charged soil may prevent the long
distance mobility of negative charge-bearing citrate-
capped AgNPs. On the contrary, a negative charged
soil may cause AgNPs to be more mobile in such soils
(Tolaymat et al. 2010; reviewed by Yu et al. 2013).
The strong adsorption capability of AgNPs onto soils
has also been documented (Jacobson et al. 2005;
Oromieh 2011; VandeVoort et al. 2012). Oromieh
(2011) reviewed the possible fate of both Ag and
AgNPs in soils; where a high soil pH value and cation
exchange capacity (CEC) were reported to enhance
Ag-sorption to the soil due to higher negatively
charged sites and more cation exchange reactions,
respectively. In addition, soils with fine texture were
reported to exhibit higher surface areas which also
facilitate Ag-sorption (Jacobson et al. 2005). Ag-
sorption and mobility are also controlled by soil
organic matters (Jones and Peterson 1986). Soils with
high organic matter concentration sorb Ag more
strongly than to mineral soils; where the sorption of
Ag to soil was advocated due either to cation
exchanges or complexation reactions (Jacobson et al.
2005). Moreover, higher binding affinity of Ag to
reduced sulfur groups (thiol) on soil organic matter in
order to form S–Ag–S bonds has been reported (Bell
and Kramer 1999). Enhanced mobility of AgNPs was
reported in the presence of organic matter such as
surfactants or humic acid (Tian et al. 2010; Lin et al.
2012; Thio et al. 2012); whereas the promotion of
AgNP-aggregation and retention was widely evi-
denced due to higher ionic strength and divalent
cations (Lin et al. 2011; Thio et al. 2012). In addition
to organic matter, pH has also been evidenced
important soil property controlling the occurrence
and the transformation of AgNP amendments to soils
(Benoit et al. 2013). AgNP-aggregation and soil
adsorption behavior have been reported to be closely
associated with environmental factors such as ionic
strength and natural organic matter (Bae et al. 2013).
The authors observed increased aggregation rate of
AgNPs with increasing ionic strength and decreasing
natural organic matter concentration. Additionally, at
higher ionic strength, the AgNPs were found unstable,
where AgNPs tended to be adsorbed to the soil, while
increased natural organic matter concentration hin-
dered soil adsorption. Hence, a thorough understand-
ing of particle–particle interaction mechanisms
assessment has been suggested in order to correctly
Page 7 of 26
assess AgNP-environmental fate and transport (Bae
et al. 2013). The authors also reported more availabil-
ity of free Ag ions in acidic soils, while in the presence
of organic matter, Ag ions were reported to be tightly
bound in complexes. Information is still sparse on the
mobility of AgNP in natural soils under dynamic flow
conditions, and the effect of soil properties on AgNP-
transport in soils (Cornelis et al. 2012). Negative f
potential of most natural soil minerals results in a high-
energy barrier for the attachment of AgNPs (Christian
et al. 2008; Theng and Yuan 2008; Lin et al. 2011) and
the demonstration of relatively high mobility of
AgNPs was expected (Sagee et al. 2012). In context
with the retention and dissolution of AgNPs in natural
soils: (a) free Ag? was expected to preferentially bind
to thiol groups and natural organic matter (Van-
deVoort et al. 2012), (b) Ag ions exhibit strong
binding capacities of the humic and fulvic acids;
resulting into less than 5 % of the total dissolved Ag to
be biologically available (Jacobson et al. 2005),
(c) much of the Ag in soils has been evidenced to be
bound either to colloidal particles (size 10–200 nm) or
adsorbed to the soils (Coutris et al. 2012a, and (d) the
most of the Ag? are highly retained by the soil
(Cornelis et al. 2012). The modulation of soil denitri-
fication kinetics by AgNPs (35–60 nm, uncoated and
coated with 0.3 % polyvinylpyrrolidone; 1, 10, or
100 mg L-1) was correlated with AgNP affinity for
soil surfaces (Kd), as determined through the isotherm
study (VandeVoort et al. 2012).
Soil-harbored environmental pollutant’s aging, as
physical or chemical transformations over time, is a
well-known phenomenon that describes temporal
aspects of their bio-accessibility (Coutris et al.
2012b). In context also with AgNPs, the aging has
been considered essential for understanding their fate
in the environment (Scheckel et al. 2010; Shoults-
Wilson et al. 2011; Coutris et al. 2012b). Moreover,
since AgNPs are susceptible to environmental trans-
formations (changes in aggregation state, oxidation
state, precipitation of secondary phases, sorption of
(in)organic species), the assessment of the toxicity of
the transformed NPs as well as the ‘‘fresh’’ ones has
been recommended (Levard et al. 2012). Since AgNPs
have small particle size, the kinetics of AgNPs was
expected to be faster than for bulk Ag which in fact is
the reason behind the significantly reduced lifetime of
the metallic state of Ag in nature. AgNPs may also
readily transform in the environment, which can
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modify their properties and alter their transport, fate,
and toxicity. Hence, the consideration of such trans-
formations has been strongly recommended when
assessing the potential environmental impact of Ag-
NPs in realistic complex natural systems (Levard et al.
2012; Lowry et al. 2012). Additionally because of
availability of Ag-corrosion agents in nature, AgNP-
environmental transformations have been envisaged to
strongly affect their surface properties (Liu et al. 2010)
and consequently their transport, reactivity, and tox-
icity in soils and aqueous systems (Levard et al. 2012).
However, despite the previous facts, most of the
information available on potential environmental
transformations of AgNPs are restricted to aqueous
systems (Elzey and Grassian 2010; Levard et al. 2011,
2012; Zhang et al. 2011; Gondikas et al. 2012); and
only a few studies are available in this context with
AgNP-potential transformations in soil system
(Scheckel et al. 2010; Shoults-Wilson et al. 2011).
Using X-ray absorption spectroscopy, the time-depen-
dent evolution of AgNPs in kaolin (Scheckel et al.
2010) and soil (Shoults-Wilson et al. 2011) has been
evidenced. No change was revealed in uncoated
AgNPs (mean particle diameter 100 nm) over
18 months, even in the presence of NaCl; whereas
organically coated AgNPs (mean particle diameter
148 nm) became coated with chloride when NaCl was
present. Additionally, no destabilization/dissolution of
these particles was observed during 18 months
(Scheckel et al. 2010). In another similar study,
Shoults-Wilson et al. (2011) studied the speciation of
PVP-coated AgNPs (mean particle diameter 10 and
30–50 nm) aged 28 days in soil. Most silver remained
as Ag0, while 10–17 % was present as Ag2O, indicat-
ing that AgNPs had undergone partial oxidation in
soil.
The changes in colloidal stability and their inter-
action with different environmental surfaces can
significantly control the fate of engineered NPs in
environmental systems (Abraham et al. 2013). In this
perspective, the studies on the sorption of engineered
AgNPs from stable and unstable suspensions to model
(sorbents with specific chemical functional groups)
and environmental (plant leaves and sand) surfaces
have revealed the role of classical sorption isotherms
to this end (Abraham et al. 2013). In addition, the
nonlinear nature of sorption of AgNPs from stable
suspensions was revealed. AgNPs have also been
evidenced to largely irreversibly interact in a primary
123
J Nanopart Res (2013) 15:1896
minimum associated with microscopic heterogeneity
(Liang et al. 2013). Colloidally stable AgNP suspen-
sions exhibited greater toxicity to bacterium Pseudo-
monas fluorescens (ATCC 13525) biofilms than
corresponding particle-free supernatants containing
only dissolved Ag released from the particles; whereas
this distinct NP-specific toxicity was not observed for
less stable, highly aggregated particles, suggesting
that biofilms were protected against NP-aggregate
toxicity (Wirth et al. 2012). It is important to underline
here that to date no information on the influence of
NPs on soil is available in the possibly vulnerable
ecosystems of polar-regions. In this context, however,
AgNPs (0.066 %) were evidenced highly toxic to
arctic consortia (on a high latitude, [78°N) (Kumar
et al. 2011); hence, the authors advocated more studies
need on NP’s potential toxicity, particularly in high
latitude soils.
Because ion release is an important environmental
behavior of AgNP and estimation and/or character-
ization of Ag? release in soil environment is critical
for understanding the environmental fate, transport,
bioavailability and bio-accessibility, and subsequent
biological impacts of AgNPs (Coutris et al. 2012a;
Benoit et al. 2013). Given their ability to oxidize in
soil environment (Shoults-Wilson et al. 2011; Cornelis
et al. 2012), it is not clear whether the AgNPs, Ag? or
Ag complexes are the most bioavailable species
(Benoit et al. 2013). To this end, the AgNP-bioavail-
ability (Fortin and Campbell 2001) or AgNP-toxicity
may be modulated by both Ag? (Ratte 1999) and some
of their complexes. Radniecki et al. (2011) found that
NP-specific toxicity to ammonia oxidizing bacteria—
Nitrosomonas europaea was reported negligible for
AgNPs and that dissolved Ag was responsible for the
observed AgNP-toxicity. Other studies on Ag behav-
ior in sewage sludge suggested that Ag2S was the
dominant species originating either from Ag? or
AgNPs, and that the very low solubility of Ag2S would
limit the bioavailability and adverse effects of silver in
the environment (Kim et al. 2010; Nowack 2010).
Hence, the studies aimed at evaluating the risk of the
AgNPs, and at distinguishing these particles from that
of the released free Ag and Ag-complexes should
perform speciation studies. However, very few data
are available in the literature on the partitioning of
AgNPs in soils or on the determination of the
speciation of Ag? in soils following the AgNP-
amendment (Benoit et al. 2013). Furthermore,
J Nanopart Res (2013) 15:1896
AgNPs-toxicity to microbes has been reported to be
significantly modulated by culture conditions/types
(pure culture, natural sediments), where environmen-
tal physico-chemical interactions significance in
damping NPs toxicity was reflected (Bradford et al.
2009; Colman et al. 2012). Thus, it is clear from the
above discussion that part or all of the toxicity
attributed to AgNPs may be due to the release of
Ag?. Therefore, in order to determine the relative
toxicity of Ag? with respect to AgNPs, it is essential to
precisely quantify AgNPs dissolution under the con-
ditions that are most relevant to the biological or
environmental media of interest (e.g., complex matri-
ces, low AgNP-concentrations, etc.) (Hadioui et al.
2013).
Silver nanoparticles impact on soil microbial
communities
Soil bacteria play a key role in nitrogen fixation and
the breakdown of organic matter. In addition, soil
bacteria also form symbiotic relationships with
legumes which provide a major source of fixed
nitrogen for both of them and other plants. Neverthe-
less, significant consequences for ecosystems can be
influenced by any perturbations of soil microbial
consortia which in turn could affect soil fertility, water
quality and ecosystem, and plant growth and produc-
tivity (Davidson and Janssens 2006; Throbäck et al.
2007; Yang et al. 2013). However, to date, the
majority of the toxicity studies on AgNPs have
considered mammals or aquatic species, and compar-
atively few studies have considered soil microorgan-
isms (US-EPA 2007; Christian et al. 2008; Klaine
et al. 2008; El-Temsah and Joner 2012). Moreover, the
available reports on AgNP-toxicity to bacteria have
been largely performed in laboratory settings and have
not been conducted within environmental media
(VandeVoort et al. 2012; VandeVoort and Arai
2012). In soils with low organic matter, AgNPs
exposure may cause a dramatic collapse in metabolic
abilities and the diversity of soil microbial popula-
tions (i.e., bacteria, archaea, or eukarya); whereas in
higher organic matter soils the response may be of
lesser extent where detectable and significant impli-
cations to diversity of the soil system can be envis-
aged. The implications of this collapse were expected
to be tremendous as the soil biology is critical in
controlling the environmental fate of many other
Page 9 of 26
chemicals (http://water.usgs.gov/wrri/08grants/2008
IN251B.html). Furthermore, soil exo-enzyme activi-
ties can be negatively impacted by AgNPs where
higher sensitivity of urease activity towards AgNPs
was noted (Shin et al. 2012). Hence, the potential of
AgNPs to adversely affect beneficial bacteria in the
environment, especially in soil system has become a
particular concern (http://nano.foe.org.au/node/190).
The toxic effect of AgNPs on bacteria has been
widely evidenced to disrupt denitrification processes,
with the potential to cause ecosystem-level disrup-
tion (SenJen 2007; Throbäck et al. 2007; Panyala
et al. 2008; VandeVoort and Arai 2012). Soil bacteria
exposure to 100–1,000 mg L-1 of various types of
AgNPs has been evidenced to significantly inhibit
nitrification (Choi and Hu 2008, 2009; Radniecki
et al. 2011; Arnaout and Gunsch 2012). In this
context, the AgNP-toxicity to nitrification bacteria
has been reported to be highly dependent on their
size; where AgNPs with less than 5 nm diameter
were reported to significantly inhibit the activity of
nitrification bacteria (Choi and Hu 2008). Root-
colonization by beneficial soil bacterium (Pseudo-
monas chlororaphis O6) has been evidenced to
promote plant growth and tolerance to abiotic and
pathogen stresses (Ryu et al. 2007; Cho et al. 2008).
However, the toxicity of AgNPs (10 nm spherical; 1
and 3 mg Ag L-1) to PcO6 has been reported
(Calder et al. 2012). The authors observed 1 and
3 mg Ag L-1 mediated loss in bacterial culture-
ability in sand whereas no cell death was observed in
a loam soil. In another study, Fabrega et al. (2009a, b)
evidenced partial disaggregation and stabilization of
AgNPs due to humic acids which can also reduce
AgNPs antimicrobial effects against P. fluorescens.
Moreover, the properties of solution such as pH, ionic
strength, and background electrolytes were reported
to alter the surface charge and aggregation of AgNPs
(El-Badawy et al. 2010) which in turn can lead to
altered toxicity (Jin et al. 2010; Yang et al. 2012).
Despite the clearly known AgNP-impact on benefi-
cial soil bacteria, little research has been conducted
on how nitrogen-cycling bacteria respond to AgNPs
at the molecular level and the resulting impact on the
associated metabolic pathways. Hence, the studies on
the relative sensitivity and transcriptomic response of
ecologically important microorganisms to both Ag-
NPs and Ag? would help significantly to get more
insights in the current context (Yang et al. 2013).
123
Page 10 of 26
Silver nanoparticles in plants
Accumulation
Studies have shown that NPs may undergo accumu-
lation in plants. Since plants possess a large size and
high leaf area, and are of stationary in nature they have
a greater chance of exposure to a wide range of NPs
available in their surrounding environment (Dietz and
Herth 2011). Thus, plants may significantly control
varied NP’s fate and transport in the environment by
accumulating them into their biomass (Navarro et al.
2008; Ma et al. 2010). The major pathways of
terrestrial plant’s exposure to NPs through soil were
earlier reported to include potential leaching from
nano-enabled products, intentional sub-surface release
for environmental remediation, land applications of
contaminated biosolids, or wastewater effluent dis-
charge (Pokhrel and Dubey 2013; Zhang et al. 2013).
Plant roots have been considered as the main route of
plant’s exposure to NPs which may harbor a major part
of accumulated NPs which subsequently may lead to
physical or chemical toxicity in plants. Proper hydrau-
lic conductivity has been considered essential for the
mobility and encounter of AgNPs to plant roots
and rhizobacteria (Bystrzejewska-Piotrowska et al.
2009; Fabrega et al. 2011). Cucurbita pepo shoots
contained 4.7 greater Ag-concentration under AgNPs
(10–1,000 mg L-1) exposure than did the plants from
the corresponding bulk solutions at similar concentra-
tions (Stampoulis et al. 2009). The authors considered
a greater ion release from AgNPs as the major reason
leading to a greater Ag-concentration in C. pepo
shoots. Uptake of AgNPs as large as 40 nm has been
evidenced in Arabidopsis thaliana roots, where
though the majority of AgNPs adhere to the root cap
their transport to the shoots was also observed (Ma
et al. 2010). A differential Ag-accumulation capability
of Populus deltoides 9 nigra and A. thaliana was
revealed under hydroponic exposure to AgNPs (PEG-
coated 5 and 10 nm AgNPs, and carbon-coated 25 nm
AgNPs) concentrations (0.01–100 mg L-1) (Wang
et al. 2013). In this study, Ag-distribution in shoot
organs varied between plant species, where A. thali-
ana accumulated Ag primarily in leaves (at tenfold
higher concentrations than in the stem or flower
tissues), whereas poplars accumulated Ag at similar
concentrations in leaves and stems. Moreover, within
the particle sub-inhibitory concentration range,
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J Nanopart Res (2013) 15:1896
Ag-accumulation in P. deltoides 9 nigra tissues
increased with exposure concentration and with
smaller AgNP size. However, compared to larger
AgNPs, the authors observed the faster uptake of
smaller AgNPs which impacted evapotranspiration at
lower concentrations (e.g., 1 mg L-1 of 5 nm AgNPs)
in P. deltoides 9 nigra. Sabo-Attwood et al. (2012)
reported the uptake of AgNPs by Nicotiana xanthi
seedlings as size selective, with further translocation
to cells and tissues and resulting biotoxicity. No
accumulation of Ag in any form was noted in AgNP-
exposed Brassica juncea plants (Haverkamp and
Marshall 2009); where the authors also evidenced
the bioaccumulation of the AgNPs in the B. juncea
cells as a function of the reduction potential in the
system. In context with AgNPs-cellular uptake, the
uptake mechanisms and distribution of AgNPs in cells
are still insufficiently explored, and very few studies
have addressed this question (Kokina et al. 2013). In
AgNPs-exposed Linum usitatissimum, Kokina et al.
(2013) demonstrated the uptake of AgNPs by calli
cells and regenerants where AgNPs were localized
mainly in the cytoplasm, and they did not affect
regenerant viability and also influenced the type and
frequency of flax calli regeneration. The authors
envisaged that this effect of AgNPs could be used
for the delivery of metal NPs to plant cells. Deposition
of AgNPs has been evidenced inside the root cells in
Oryza sativa (Mazumdar and Ahmed 2011). Where
the authors concluded that AgNPs can enter through
small pores of cell walls and causes damages in cell
wall and vacuoles as well. In Zea mays, the bio-uptake
concentration was 1.8 ng Ag mg-1 dry weight of
seedlings for citrate-AgNP treatments (Pokhrel and
Dubey 2013). To the other, A. thaliana exposed to
AgNP suspensions bioaccumulated higher Ag content
than plants exposed to AgNO3 solutions (Ag? repre-
sentative) (Geisler-Lee et al. 2013). Moreover, AgNPs
accumulated progressively in this sequence: border
cells, root cap, columella, and columella initials.
AgNPs were apoplastically transported in the cell wall
and found aggregated at plasmodesmata. The bio-
availability of NPs to plant-uptake can be influenced
by any difference in media with AgNPs-concentra-
tions. In this context, the bioavailability and effect of
Ag? dissolved from AgNPs were observed less in soil
than agar (Lee et al. 2012). Nevertheless, the amounts
of Ag? release from AgNPs in soil and agar media
significantly differed; where the authors noted the
J Nanopart Res (2013) 15:1896
maximum concentration of Ag? released from AgNPs
in the agar and soil samples used as: 1.3 mg L-1 and
2.7 mg kg-1, respectively. The AgNPs accumulated
in Phaseolus radiatus and Sorghum bicolor in agar
medium increased in an exposure concentration-
dependent manner where the bioaccumulation factors
of P. radiatus and S. bicolor were calculated to be 0.14
and 0.08 L kg-1, respectively. Moreover, the authors
noted AgNPs-concentration-dependent increase in
AgNP-bioaccumulation only in the roots but not in
the shoots. The bioaccumulation factors of the root of
P. radiatus and S. bicolor were 0.008 and 0.006 kg-1,
respectively; whereas the bioaccumulation factors of
the shoot of P. radiatus and S. bicolor were calculated
as 0.001 and 0.001 kg-1, respectively. As reported
also by Coutris et al. (2012a), the low bioavailability
of AgNPs may attribute to their binding to organic
substances and the low mobility. The soil media may
change the properties and dissolution of NPs hence
may affect their bioavailability. The lower AgNPs-
bioavailability was suggested to be due to a greater
aggregation in pore water and AgNP sorption onto soil
particles contributed to lower bioavailability of Ag-
NPs in soil (Lee et al. 2012). In common metallo-
phytes namely B. juncea and Medicago sativa, Ag was
stored as discrete NP, with a mean size of approxi-
mately 50 nm (Harris and Bali 2008). In Glycine max
and C. pepo exposed to 500 or 2,000 mg L-1 of bulk
or AgNP, De La Torre-Roche et al. (2013) reported
Ag-mediated significant impact on overall element
uptake, where in G. max, AgNP-exposure resulted in
1.8–6.6 times more tissue Ag than did the correspond-
ing bulk material exposure; whereas in C. pepo, this
pattern of greater NP uptake held at 500 mg L-1 but
disappeared at the higher exposure level.
Ag-mediated significant alteration in the accumula-
tion and translocation of co-contaminants in agricultural
systems has been reported where the co-contaminant
interactions varied both with Ag-particle size (NP versus
bulk) and plant species (De La Torre-Roche et al. 2013).
Nevertheless, especially in agro-ecosystems, in addition
to direct toxicity to and accumulation by crop plants, the
interaction of NPs with co-contaminants and other
chemical constituents (such as pesticides, fertilizers)
have been evidenced to impact food safety (De La Torre-
Roche et al. 2013). In G. max and C. pepo exposed to 500
or 2,000 mg L-1 of bulk or AgNP, De La Torre-Roche
et al. (2013) reported a suppressed uptake and translo-
cation of (dichlorodiphenyldichloroethylene, p,p0 -
Page 11 of 26
DDE–DDT metabolite), a widespread persistent and
estrogenic pollutant upon co-exposure to Ag; where the
authors envisaged the role of element interactions with
membrane transport proteins.
Toxicity and tolerance
In consideration of the vast use of AgNPs and their
various possible routes of entry into the environment
(Som et al. 2011; Speranza et al. 2013), there is an
urgent need to critically discuss available literature on
potential mechanisms underlying AgNP’s phytotoxic-
ity and tolerance. Nevertheless, though toxicity of the
Ag ionic form is well-understood comprehension the
toxicological impact of AgNPs is more complicated
due largely to uncertainties in the amounts of aggre-
gation or exposure (Mirzajani et al. 2013). In compar-
ison with the bacteria, there are limited toxicology
studies on the effects and mechanisms of NPs on higher
plants. Also, there is a dearth of information in the
literature on AgNP-impacts on terrestrial plant species;
where AgNPs–plant interaction-study results have
yielded both positive and negative or inconsequential
effects where merely more speculation and un-sub-
stantiation are perceptible. Though, a number of
factors related with plants (species types, seeds,
seedlings, cell suspensions), AgNPs (concentration,
size, aggregation, functionalization), and environmen-
tal/experimental conditions (temperature and time, and
method of exposure) may control AgNP-phytotoxicity
extent Navarro et al. (2008) (Table 1; Fig. 2b) but only
a few studies have considered these aspects during
AgNPs–plant interaction experiments. Figure 3 sche-
matically illustrates major sources of AgNPs to the
soil, role of soil physico-chemical characteristics in the
control of AgNPs mobility/bioavailability modulation
and their subsequent influence on the extent of plant
AgNPs-uptake/accumulation and toxicity.
In the following sub-sections, recent information
available on AgNPs-mediated toxicity to plant growth
and physiology/general biochemistry and cells will be
critically discussed. In addition, information pertain-
ing to AgNPs-accrued oxidative stress and its metab-
olism will also be appraised.
Toxicity to plant growth and physiology/biochemistry
A higher toxicity has been credited to very small size
of NPs in a number of studies in NPs-exposed plants
123
Page 12 of 26
(reviewed by Rico et al. 2011). To this end, El-Temsah
and Joner (2012) evidenced a greater toxicity in
L. usitatissimum, Hordium vulgare, and Lolium
perenne due to Ag-colloid (0.6–2 nm) when compared
to AgNPs of 5 and 20 nm. In L. usitatissimum,
H. vulgare, and L. perenne exposed to 0–100
mg L-1 Ag, El-Temsah and Joner (2012) evidenced
inhibitory effects in aqueous suspensions at 10 mg
AgNP L-1 where the authors did not achieve a
complete inhibition of germination; hence, considered
reduction in shoot growth as a more sensitive endpoint
than germination percentage. Moreover, the authors
showed no clear size dependency of the AgNP-effects.
Though AgNP (size 29 nm) may exert visible reduction
effects on the germination of C. pepo and Lactuca
sativa seeds but no toxicity effect was observed
(Barrena et al. 2009). Growth in terms of fresh weight,
root and shoot length, and vigor index of seedlings has
been reported positively affected by AgNPs concentra-
tions (0, 25, 50, 100, 200, and 400 ppm) in B. juncea
(Sharma et al. 2012). The authors noted AgNPs-
mediated increase of 326 % in root length and 133 %
in vigor index. In sand matrix culture, there is a report of
AgNPs-dose-dependent inhibition of Triticum aestivum
growth where the authors noted a dose-dependent
reduction in shoot and especially the root lengths with
amendments with AgNPs (Dimkpa et al. 2013). In
another study by Mahna et al. (2013), the lower
concentrations of AgNP (100, 250, 500, 1,000, and
2,000 ppm; exposed for 5, 10, 20, 30, and 60 min) acted
as an antimicrobial agent with no side effect on the
explant viability, and consequently, all decontaminated
seeds germinated, and leaf and cotyledon explants
survived in Lycopersicon esculentum cv. Micro-Tom,
A. thaliana and Solanum tuberosum. In a recent study, a
stimulatory effect was observed on root elongation,
fresh weight, and evapotranspiration of both plants
at a narrow range of sub-lethal concentrations
(e.g., 1 mg L-1 of 25 nm carbon-coated AgNPs for
P. deltoides 9 nigra) (Wang et al. 2013). These
authors also observed some toxicity at higher AgNP-
concentrations (e.g., 100 mg L-1 of 25 nm carbon-
coated AgNPs for P. deltoides 9 nigra, 1 mg L-1 of
5 nm AgNPs for A. thaliana) where plant susceptibility
to AgNPs increased with decreasing AgNP size. No
significant effects on seedling growth were reported in
AgNPs-exposed Ricinus communis plants even at
higher concentration of 4,000 mg L-1 (Yasur and Rani
2013), while the authors noted a decreased seed
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J Nanopart Res (2013) 15:1896
germination under the exposure of Ag in bulk form as
AgNO3. A size- and concentration-dependent citrate-
stabilized AgNPs (sizes 20, 40, and 80 nm)-toxicity (in
terms of physiological phytotoxicity, cellular accumu-
lation, and subcellular transport) in A. thaliana (Geis-
ler-Lee et al. 2013). In addition, the authors noted
inhibition in the seedling root elongation where a linear
dose–response relationship was perceptible within the
tested concentration range. The available literature on
seed germination, root elongation, and root growth
under biologically synthesized AgNPs exposure have
showed both insignificant effect (at 10 ppb and 100 ppb
AgNP; Krishnaraj et al. 2012) and significant negative
impact at very low engineered AgNPs concentration
(Ma et al. 2010; Yin et al. 2011). In P. vulgaris and Z.
mays exposed to varying AgNP-concentrations (20, 40,
60, 80, and 100 ppm), Salama (2012) reported a AgNP-
dose-dependent effect on plant growth. Where the
authors noted increase in the lengths and weights of
shoot and root and the area of leaf surface of the studied
plants with increase in AgNPs concentration up to
60 ppm; thereafter, declines in the studied parameters
were noted. The authors have given the credit of
increased plant growth up to 60 ppm AgNPs to
increased chlorophyll, carbohydrate, and protein con-
tents. In Z. mays, root hair density appeared unaffected
with citrate-coated AgNPs; where also little to no effect
on root growth was noted (Pokhrel and Dubey 2013).
The authors observed some potential of citrate-coated
AgNPs to inhibit germination in Z. mays; this inhibition
was, however, always less than 35 % even at the
highest concentration tested (73.4 lg mL-1; compared
to the control). The biologically synthesized AgNPs
resulted in an insignificant decrease in the root and
shoot length along with disappearance of air chamber in
root cortex, alteration of shape, size, and distribution of
xylem elements in the stems of Bacopa monnieri
(Krishnaraj et al. 2012). AgNP-penetration into the O.
sativa cell wall and subsequent destruction of the cell
morphology and the structural features has been
evidenced up to 60 lg mL-1 of AgNPs (Mirzajani
et al. 2013). The authors also noted a linear and
significant decline in the dry matter accumulation under
AgNPs exposure. In contrast, O. sativa plant-incubation
for 7, 14, and 21 days with the treated growth media
diminished the observed AgNPs inhibitory impact on
the plants dry weight. In this context, the authors
expected the role of AgNPs size which might have
increased during the incubation period which in turn
 Table 1 Summary of some representative recent studies on silver nanoparticles (AgNPs)-impacts in plants
Particle size/range and concentration(s) Plant species and Exposure condition and incubation Effect References
endpoints period

Plant germination, growth, and physiology/biochemistry

Size: \100 nm; concentration: Curcubita pepo 25 % Hoagland’s solution Reduced biomass and transpiration by 66–84 % when Musante
500 mg L-1 compared with bulk Ag and
White
(2012)
J Nanopart Res (2013) 15:1896

Size: 10 nm; concentration: Triticum aestivum Sand matrix Dose-dependent reduction in shoot and especially the Dimkpa
0–5 mg kg-1 root lengths with amendments with AgNPs et al.
(2013)
Size: 10 nm; concentration: T. aestivum Sand matrix Dose-dependent elevation in the accumulation of
0–5 mg kg-1 oxidized glutathione (GSSG) and induction in the
expression of a gene encoding a metallothionein
Concentration: 250 and 750 mg L-1 C. pepo Solution culture Plant biomass and transpiration decreased by Hawthorne
49–91 % compared to equivalent bulk Ag et al.
(2012)
Citrate-coated; particle size range: Phaseolus radiatus; Agar culture media (20 mL of 0.5 % No-observed-adverse-effect concentration (NOAEC): Lee et al.
5–25 nm (average 10 nm); seedling growth agar and 10 mL of 0.25 % agar); \5; the lowest-observed-adverse-effect (2012)
concentrations: 0, 0.5, 1, 5, and incubated for 2 days concentration (LOAEC): 5; median effective
10 mg L-1 concentration (EC50): 13
Sorghum bicolor; NOAEC: \5; LOAEC: 5; EC50: 26
seedling growth
Citrate-coated; particle size range: P. radiatus; shoot Soil adjusted with moisture content of NOAEC: [2,000; LOAEC: [2,000; EC50: [2,000
5–25 nm (average 10 nm); growth 40 %); controlled temperature of
concentrations: 0, 100, 200, 300, 400, 25 ± 1° C; incubated for 5 days
500, 600, and 800 mg kg-1 dry soil
P. radiatus; root NOAEC: [2,000; LOAEC: [2,000; EC50: [2,000
growth
S. bicolor: shoot NOAEC: \100; LOAEC: \100; EC50: [2,000
growth
S. bicolor: root NOAEC: 100; LOAEC: 300; EC50: [2,000
growth
Size: 2 nm; concentrations: 62, 100, and Cucumis sativus; Solvent solution and concentration: Low to zero toxicity Barrena
116 mg L-1 Lactuca sativa sodium borohydride (2.64 mM) et al.
seed germination (2009)
Page 13 of 26

123
 Table 1 continued
Particle size/range and concentration(s) Plant species and Exposure condition and incubation Effect References
endpoints period

123
Page 14 of 26

Size: 20 nm; concentrations: 20, 40, 60, Linum No effect on the germination El-Temsah
80, and 100 mg L-1 usitatissimum and Joner
Ag (colloid); size: 0.6–2 nm; AgNP- Lolium perenne Aqueous suspension (0.1 % v/v Reduced germination (20 %) (2012)
concentration: 10 mg L-1 Tween 20)
Ag (colloid); size: 0.6–2 nm; AgNP- Reduced germination (50 %)
concentration: 20 mg L-1
Ag (colloid); size: 0.6–2 nm; AgNP- L. perenne; Reduced shoot length
concentration: 10 mg L-1 L. usitatissimum
Ag (colloid); size: 0.6–2 nm; AgNP- Hordeum vulgare; L.
concentration: 20 mg L-1 perenne;
L. usitatissimum
Ag; size: 5 nm; AgNP-concentration: H. vulgare Reduced germination
10 mg L-1 L. usitatissimum; H. Reduced shoot length
vulgare
Ag; size: 20 nm; AgNP-concentration: H. vulgare Reduced germination and shoot length
10 mg L-1
Ag; size: 20 nm; AgNP-concentration: H. vulgare; Reduced shoot length
20 mg L-1 L. perenne
Ag; size: 100 nm; AgNP-concentrations: C. pepo 25 % Hoagland solution Reduced transpiration (41–79 %) Stampoulis
100, 500, and 1,000 mg L-1 et al.
Ag; size: 100 nm; AgNP-concentrations: Reduced biomass (57–71 %) (2009)
500 and 1,000 mg L-1
Gum arabic-coated AgNPs; size: 6 nm; Lolium multiflorum Seeds were soaked in 5 mL test Toxicity increased with increased AgNP- Yin et al.
concentrations: 1–40 mg L-1 solutions; incubation period: 7 days concentration; seedlings failed to develop root (2011)
hairs, had highly vacuolated and collapsed cortical
cells and broken epidermis and rootcap; root
biomass decreased from 18.6 to 4.7 mg; root length
decreased from 7 to 0.7; roots AgNP
sensitivity [ shoots
Size: 25 nm; concentration: 100 mg L-1 Populus 1/4 strength Hoagland solution; Significantly decreased evapotranspiration by 87 %; Wang et al.
deltoides 9 nigra 11 days reduced the fresh weights of roots, stems, and (2013)
leaves by 87, 42, and 81 %, respectively
Size: 25 nm; concentration: 1 mg L-1 P. deltoides 9 nigra 1/4 strength Hoagland solution; Increased poplar evapotranspiration by 42 %
11 days compared to unexposed controls; Root and stem
biomass were increased by 63 and 46 %,
respectively
J Nanopart Res (2013) 15:1896
 Table 1 continued
Particle size/range and concentration(s)
PEG-coated 10 nm AgNPs;
concentration: 0.1 mg L-1
Sizes: 5 and 10 nm; concentration:
0.05 mg L-1
Sizes: 5 and 10 nm; concentration:
1 mg L-1
Size: 5 nm; concentrations:
0.01–0.05 mg L-1
Size: 10 nm; concentrations:
0.01–0.02 mg L-1
Cellular-/geno-toxicity
Concentrations: 50, 500, and
1,000 lg mL-1
Size: 70 nm; concentrations:
0–80 mg L-1
Size: 24–55 nm; concentrations:
0–80 lg L-1
Size: \100 nm; concentration:
100 mg L-1
Size: 60 nm; concentrations: 12.5, 25,
50, and 100 mg L-1
Modified after Rico et al. (2011)
123
Plant species and Exposure condition and incubation
endpoints period
P. deltoides 9 nigra 1/4 strength Hoagland solution;
11 days
Arabidopsis thaliana 1/4 strength Hoagland solution;
11 days
A. thaliana 1/4 strength Hoagland solution;
11 days
A. thaliana 1/4 strength Hoagland solution;
11 days
A. thaliana 1/4 strength Hoagland solution;
11 days
Oryza sativa Hoagland solution; 12 days;
temperature: 25 ± 5 °C; to prevent
aggregations it was stirred with
glass rod after every 12 h.
Allium cepa 5,000 Solution culture; commercial, Sigma;
cells 2h
A. cepa 5,000 cells Biologically synthesized;
(biogenically male inflorescence of
screw pine, Pandanus odorifer); 2 h
Allium cepa Aqueous suspension; 4 h
Vicia faba root tips AgNPs were suspended directly in
deionized water
Effect References
Significantly enhanced poplar evapotranspiration by
43 %; the final fresh weight of roots, stems, and
leaves was also increased relative to the control
poplars by 48, 50, and 39 %, respectively
Moderate increases in overall rosette size and
coloration
J Nanopart Res (2013) 15:1896
Root growth rate was completely inhibited; smaller
rosette size
Increased root growth by 38 %
Increased root growth by 20 %
1,000 lg mL-1 reflected the highest toxicity where: Mazumdar
breakage of cell wall and vacuoles in root cells of and
test species described the toxicity of particles; Ahmed
depositions of silver nanoparticles inside the root (2011)
cell by smaller particles
Cytotoxicity LC50: up to 10 lg mL-1 no effects on Panda et al.
genotoxicity; Comet assay 20–40 lg mL-1; DNA (2011)
damage doses 10 lg mL-1
ROS-induced cell death and DNA damage doses Panda et al.
20 lg mL-1; up to 10 lg mL-1 no genotoxic; (2011)
concentrations \ 5 lg mL-1 were noncytotoxic,
and concentrations [80 lg L-1 were cytotoxic,
which was evident from cell death as well as
mitotic index
Decreased mitosis; disturbed metaphase; sticky Kumari
chromosome; cell wall disintegration and breaks et al.
(2009)
Dose-dependent decrease in the mitotic index but Patlolla
increase in the frequencies of chromosomal et al.
abnormalities and micronuclei (2012)
Page 15 of 26
Page 16 of 26 J Nanopart Res (2013) 15:1896

AgNP-Laden Plant-Entry to Food Chain

AgNPs-
Phytotoxicity

Biological Compounds
Extent
Modulation

AgNPs-Shoot-
Interaction
AgNPs-Plant
Uptake/Accu
mulation-
Modulation

AgNPs-Rhizosphere
Microbes Interaction

AgNPs
Mobility/Bioa
vailability
Modulation
AIR AIR

Soil Physico-Chemical
Characteristics-Mediated Control of
AgNPs Agglomeration and/or Transformation

POINT NON-POINT
SOURCES SOURCES

Environmental Factors Influence

During the AgNPs Transport to Soil

Intentional Release Accidental Release

Fig. 3 Schematic illustration of silver nanoparticles (AgNPs)-
interaction with ‘‘soil–plant systems’’ highlighting the major
pathways of AgNP-entry to the soil system, role of soil physico-
chemical characteristics in the control of AgNPs mobility/
bioavailability modulation, and their subsequent influence on
the extent of plant AgNPs-uptake/accumulation and toxicity. In
addition, AgNP-laden plant-mediated potential food chain-
contamination has also been highlighted. (Based on the
available literature including Nowack and Bucheli 2007). See
text for details

caused aggregation and agglomeration of AgNPs. O.
sativa shoots exhibited their higher susceptibility
towards AgNPs when compared to roots. Though
AgNPs treatment up to 30 lg mL-1 accelerated root
growth AgNPs at 60 lg mL-1 was able to restrict a
root’s ability to grow. Moreover, AgNPs treatment led
to an alteration of root branching systems, where the
branched root systems were enhanced through the
treatment of 60 lg mL-1 of AgNPs. The authors
considered this phenotype of a root system as a
consequence of a direct or indirect effect of AgNPs.
Between the photosynthetic pigments studied namely
chlorophyll b and carotenoids, the former was evi-
denced most susceptible to the highest concentration of
AgNPs. It was concluded that under AgNPs exposure,
O. sativa might have shifted the allocation of resources
(carbohydrate, starch) from shoot to root growth. An
improved seed yield has also been reported with
increasing concentration of AgNP from 20 to 60 ppm
in Borago officinalis (Seif et al. 2011).
It has been demonstrated that Ag? or particles
phytotoxicity could differ when soil and agar were
used as growth media. In this context, an inhibition of
the growth rates of P. radiatus and S. bicolor by 34 and
55 %, respectively, has been reported in agar media;
where the majority of adverse effects on S. bicolor
were attributed to Ag? (Lee et al. (2012). To the other,
the influence of Ag? (2.7 mg Ag? kg-1) was negli-
gible for both plants in soil medium. This study
implies that ion can be responsible for the apparent
toxicity in agar, while, the apparent toxicity observed
in soil can be attributed to particle toxicity. Consid-
ering both AgNPs and corresponding bulk counterpart
(1,000 mg L-1) in a hydroponic culture experiment

123
J Nanopart Res (2013) 15:1896
with C. pepo, Stampoulis et al. (2009) reported no
impact on seed germination. However, during a
15-day hydroponic trial, the biomass of AgNPs-
exposed C. pepo plants reduced by 75 %, respectively,
as compared to control plants and corresponding bulk
Ag powder solution. AgNPs concentrations namely
500 and 100 mg L-1 resulted in 57 and 41 %
decreases in plant biomass and transpiration, respec-
tively, as compared to controls or to plants exposed to
bulk Ag. The authors concluded that half the observed
phytotoxicity is from the elemental NPs themselves
and that germination and root elongation may not be
sensitive enough or appropriate when evaluating
nanoparticle toxicity to terrestrial plant species. Ag-
NPs of varying size rage (20–80 nm) were reported to
be toxic to A. thaliana seedlings where stunted growth
even at very low concentration (340 lg L-1) was
evidenced (Ma et al. 2010). In addition, the authors
observed a continuous decrease in the root biomass
and root length with increasing AgNP-concentrations.
A completely vacuolated and collapsed the cortical
cells have been evidenced in L. multiforum at 40 ppm
concentration of 6 nm AgNPs when compared to
25 nm size particles-effect (Yin et al. 2011). Addi-
tionally, broken epidermis and root cap were also
noted by these authors in L. multiforum. Though Ag is
known to be one of the most toxic trace metals (Ratte
1999) the mechanism involved in Ag- and AgNP-
toxicity may differ. In this context, various experi-
ments carried out with AgNPs and AgNO3 demon-
strated that the results obtained were contradictory as
nano-form had no impact on plant/seedling growth,
whereas the bulk form treatment had retarded the
growth of the R. communis exposed to different
concentrations of AgNP and AgNO3 (0, 500, 1,000,
2,000, and 4,000 mg L-1) (Yasur and Rani 2013). In
contrast, AgNPs at 250 mg L-1 decreased C. pepo
plant growth by 49 and 59 % relative to bulk Ag and
control treatments, respectively; at 750 mg L-1, the
reductions in plant mass were 55 and 64 %, respec-
tively. The presence of 100 mg L-1 humic acid
minimized AgNP-phytotoxicity at 250 mg L-1 but
at 750 mg L-1, AgNP reduced plant biomass by 70 %
(Hawthorne et al. 2012). Moreover, 500 mg L-1
AgNPs reduced C. pepo biomass and transpiration
by 66–84 % when compared with bulk Ag (Musante
and White 2012). AgNPs were reported to retard root
elongation in C. pepo seeds higher than the
Page 17 of 26
corresponding bulk form at 1,000 mg L-1 (Stampou-
lis et al. 2009). AgNP-concentrations depended
elevated toxicity (measured in terms of root length
and germination) has been reported in L. esculentum
and Z. mays which was found higher than the toxicity
caused by its equivalent Ag? concentration (Ravin-
dran et al. 2012). However, the root elongation values
in L. esculentum and Z. mays treated with 1 % bovine
serum albumin, BSA ? AgNP (20 mg L-1) were
reported similar those seedlings in control. The
coating of BSA on the surface of the AgNP may
result in a controlled release of the ions, thereby
modulating the toxic effects of the AgNP (Ravindran
et al. 2010, 2012). Using pollen culture as a model
system for AgNP-toxicity assessment in Actinidia
deliciosa var. deliciosa [(A. Chev) C.F. Liang et A.R.
Ferguson], Speranza et al. (2013) for the first time
demonstrated that AgNPs were more potent at
disrupting pollen tube elongation, while Ag? damaged
pollen membranes and inhibited pollen germination to
a larger extent. There exists also inconsistency in the
toxicity extent in different plant species caused by
different AgNPs concentrations. In this context, at one
hand, Yasur and Rani (2013) observed no significant
toxicity was observed in R. communis up to the highest
concentration (4,000 mg AgNP L-1) to the other a
reduction in biomass and transpiration by 66–84 % by
500 mg L-1 AgNPs was noted in C. pepo (Musante
and White 2012). In this perspective, the significance
of the seed coat-thickness was expected to modulate
the NPs-penetration into the seedlings (Yasur and Rani
2013). A lack of information on AgNPs potential
impact on photosynthesis and its related variables is
perceptible in the literature. To this end, growth in
terms of fresh weight, root and shoot length, and vigor
index of seedlings has been reported positively
affected by AgNPs concentrations (0, 25, 50, 100,
200, and 400 ppm) in B. juncea (Sharma et al. 2012).
The authors noted AgNPs-mediated increase of 326 %
in root length and 133 % in vigor index.
Since biochemical responses of organisms to envi-
ronmental stresses are regarded as early warning signs
of pollution in the environment (Anjum et al. 2010,
2012a, b, 2013; Gill and Tuteja 2010; Hu et al. 2012;
Gill et al. 2013), the following sections deal with the
recent information available on the AgNPs-mediated
cellular-genotoxicity and also oxidative stress and its
metabolism.
123
Page 18 of 26
Cellular- and geno-toxicity
Since plants systems have a variety of well-defined
genetic endpoints including alterations in ploidy,
chromosomal aberrations, and sister chromatid
exchanges, they have been used as indicator organ-
isms, in a wide range of studies including on
mutagenesis in higher eukaryotes (Kumari et al.
2009). In the current context, varied NPs owing to
their size can enter freely into the cells and can
interfere in cell’s normal function. Though there are a
significant number of studies on the genotoxicity and
cytotoxicity of AgNPs on mammalian and human cell
lines (Ghosh et al. 2012) only a few reports on AgNPs-
accrued cyto-genotoxicity in plant systems are avail-
able in the literature (Babu et al. 2008; Kumari et al.
2009; Ghosh et al. 2012; Patlolla et al. 2012).
Nevertheless, a paucity of knowledge pertaining to
the genotoxicity or DNA-damaging potential of AgNP
in terrestrial plants still exists in the available litera-
ture. In Allium cepa root meristems exposed to AgNPs
concentrations (10, 20, 40, and 50 ppm; for 0.5, 1, 2,
and 4 h), Babu et al. (2008) reported AgNPs concen-
trations and time intervals dependent increase in the
frequency of chromosomal aberrations and decrease in
mitotic index. In addition, the authors noted various
types of chromosomal and mitotic abnormalities such
as fragments, C-metaphase, stickiness, laggard, ana-
phasic bridge, and disturbed anaphase. In Vicia faba
root tip cells, AgNPs exposure significantly increased
the number of chromosomal aberrations, micronuclei,
and decreased the mitotic index (Patlolla et al. 2012).
The induction of chromosomal breaks and micronu-
clei by AgNPs has also been earlier reported in V. faba
root tips (Raun and Lilum 1992). A sharp decrease in
mitotic index (from 60.30 to 27.62 %) has been
evidenced in A. cepa root tip cells exposed to AgNP-
concentrations (25, 20, 75, and 100 ppm) (below
100 nm size) (Kumari et al. 2009). The authors
inferred that AgNPs penetration into plant system
lead to cell division arrest at metaphase and caused
chromatin-bridge, stickiness, disturbed metaphase,
multiple chromosomal breaks, and cell disintegration.
AgNPs also impaired cell division and caused cell
disintegration in A. cepa root tips (Kumari et al. 2009;
Stampoulis et al. 2009; Nair et al. 2010). Using A. cepa
and N. tabacum as model plant systems, Ghosh et al.
(2012) employed a genotoxic and cytotoxic approach
to elucidate the activity of AgNPs (0, 25, 50, and
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J Nanopart Res (2013) 15:1896
75 lg mL-1; for 24 h) in vitro and in vivo where the
authors observed a more pronounced AgNP-genotoxic
effect in root than shoot/leaf of the plants and also a
good correlation between the in vitro and in vivo
AgNPs’ effects. Kuriyama and Sakai (1974) reported
the ineffective mitotic spindle function as a result of
AgNPs interaction with tubulin-SH group. AgNPs
possess mitodepressive, mitoclassic, and clastogenic
properties (Tanti et al. 2012). To this end, an increase
in the frequency of chromosomal abnormalities such
as fragments, C-metaphase, stickiness, laggard, ana-
phasic bridge, chromosome divergence, spiral chro-
mosome, micronuclei, nuclear disintegration,
polyploidy, distortion of pole and unequal nuclear
distribution and decrease in mitotic index with
increase in AgNP-concentrations (25, 50, 75, and
100 ppm; for 6, 12, 18, and 24 h) were observed in A.
sativum (Tanti et al. 2012).
Oxidative stress and its metabolism
An imbalance between the generation of reactive
oxygen species (ROS) and its antioxidant defense
components-mediated scavenging causes oxidative
stress. ROS such as O- 
2 , OH , and H2O2 are strong
oxidizing agents and cause oxidative damage to
biomolecules such as proteins and lipids that weakens
membrane integrity and elevate electrolyte leakage,
and eventually cause cell death. Hence, equilibrium
between the production and elimination of ROS must
be maintained in cells if metabolic disorder or
oxidative burst is to be avoided (Gill and Tuteja
2010; Anjum et al. 2012a, b; Gill et al. 2013).
However, despite the clearly known significance of
ascorbate–glutathione pathway for the alleviation of
oxidative stress in different plant species under metal–
metalloids (Anjum et al. 2010, 2012a, b; Gill and
Tuteja 2010; Gill et al. 2013), other NPs such as
graphene oxide (Anjum et al. 2013), cerium oxide
(Rico et al. 2013), and copper oxide (Shaw and
Hossain 2013), the current literature search reflects a
clear paucity of information on this aspect in AgNPs-
exposed plant species. Nevertheless, alterations in
antioxidant defense components have recently been
considered as useful biomarkers in ecotoxicological
tests with AgNPs. Moreover, such data can be
valuable in providing information for monitoring and
forecasting early effects of exposure to AgNPs in
different scenarios (Yasur and Rani 2013). However,
J Nanopart Res (2013) 15:1896
AgNPs-toxicity studies in plants in context with
oxidative stress and its metabolism have been least
explored. Elevated generation of ROS has been
reported in O. sativa plant species under AgNPs
exposure (Mirzajani et al. 2013). However, there is no
or little information available on the adaptation of
strategies by NPs and/or AgNPs-exposed plant for the
metabolism of ROS and its reaction products. As
reported also by Mirzajani et al. (2013) in AgNPs-
exposed O. sativa plants, the induction of antioxidant
activity by elevated carotenoids levels has earlier been
confirmed to potentially reduce the toxic effects of
ROS and its reaction products (Chew and Park 2004;
He et al. 2011). Compared to AgNPs, a higher degree
of induced oxidative stress due to higher generation of
O-
2 and H2O2 was reported in A. cepa root tips under
AgNP-exposure (Panda et al. 2011). The significance
of some other factors was expected in the modulation
of ROS-mediated AgNP-toxicity in nitrifying bacteria
(Choi and Hu 2008). In contrast, in an effort to test the
phytotoxicity potential of the biologically synthesized
AgNPs in B. monnieri, Krishnaraj et al. (2012)
reported a mild stress where lower elevations
in CAT and POX activities reflected the better
B. monnieri growth with reduced toxicity compared
to the AgNO3-treated plants. Since AgNPs application
is widely used to control several plant diseases (Park
et al. 2006), Krishnaraj et al. (2012) speculated that the
mild stress due to biologically synthesized AgNPs
may be beneficial to plants in protecting them against
pathogen attacks and disease control and mandates
further study in the future. An elevated activities of
superoxide dismutase (SOD) and peroxidase have
been reported in R. communis exposed to AgNP and
AgNO3 (0, 500, 1,000, 2,000, and 4,000 mg L-1)
(Yasur and Rani 2013). The authors concluded that the
enhanced peroxidase and SOD activities are indicative
of the AgNPs-accrued increased oxidative stress
where AgNPs might have interacted with cellular
components and have caused the elevation in ROS
formation. The significance of phenols and phenolic
acids in the protection of Ag? and AgNPs-mediated
oxidative stress has been evidenced (Winkel-Shirley
2002; Krishnaraj et al. 2012; Yasur and Rani 2013).
Ag (both micro and macro forms)-mediated enhanced
accumulation of the phenolics (aromatic benzene ring
compounds with one or more hydroxyl groups) was
reported in R. communis where AgNP treatments
recorded lesser phenol content than the plants treated
Page 19 of 26
with AgNO3. The occurrence of oxidative stress in the
AgNPs-varying concentrations (0–5 mg kg-1 sand)-
exposed T. aestivum roots was assessed by measuring
levels of oxidized glutathione (GSSG) (Dimkpa et al.
2013), where AgNPs exposure caused enhanced
GSSG accumulation and also induced expression of
a gene encoding a metallothionein involved in detox-
ification by metal ion sequestration.
On the brighter side of AgNPs, since: (a) AgNPs
exhibit their ability to support electron exchange with
Fe2? and Co? 3 (the two elements that participate in
several biological redox reactions) (Mukherjee and
Mahapatra 2009) and AgNP clusters show efficient
catalytic activity in redox reactions by acting as
electron relay centers, behaving alternatively as an
acceptor and donor of electrons (Mallick et al. 2006),
AgNPs have been considered among most potential
candidates for modulating the redox status of plants
(Sharma et al. 2012). However, a little attention has
been paid to the possibility that AgNPs can possibly
help improve plant’s redox status and growth. To this
end, using B. juncea, Sharma et al. (2012) attempted to
elucidate the role of AgNP-concentrations (0, 25, 50,
100, 200, and 400 ppm) in plant growth promotion
under specified conditions. The authors noted signif-
icantly decreased levels of the two widely used
oxidative stress biomarkers namely malondialdehyde
(membrane lipid peroxidation) and hydrogen peroxide
at 25, 50, and 400 ppm AgNPs when compared to the
controls. These responses were accompanied by
significant and parallel increase in the activity of
guaiacol peroxidase (GPX; a known H2O2 metaboliz-
ing enzyme; Anjum et al. 2010, 2012a, b, 2013; Gill
and Tuteja 2010; Gill et al. 2013) and the drastic
decrease in the level of free proline (an excellent index
of the existing stress experienced by the plant;
Szabados and Savoure 2010) which the authors
considered to be responsible for improving the anti-
oxidant status and subsequently the growth of AgNPs-
exposed B. juncea.
Conclusions and perspectives
A clear imbalance between the rapid application of
AgNPs in multiple disciplines and the safety/toxicity
aspects of AgNPs in biotic systems is perceptible in
the available literature. Since metal-based NPs have
dual-toxicity of metal and NPs, their bi-toxicity and
123
Page 20 of 26
ecological risk are the hotspots in the studies of
nanotoxicology. In particular, due to their bactericidal
and viricidal properties, AgNPs have been synthesized
and widely applied and get accumulated in soil–plant
systems; hence, warrants a detail toxicological inves-
tigation to justify its safety. The effects of engineered
AgNPs on soil–plant systems are of great concern
because of their crucial interface with the environ-
ment. However, it is clearly perceptible from the
literature surveyed in the current paper that the
knowledge on the AgNP-chemistry modulation in
soils and its significance in AgNPs and Ag/Ag?
bioavailability and bio-accessibility to and subsequent
impact on soil biota in general and to plants in
particular is still in its infancy. The majority of reports
available on AgNPs interaction with soil (and/or soil
microbial community) and plants evidenced AgNP’s
negative effects. Additionally, there is still a dearth
information on: the potential mechanisms underlying
AgNP-uptake and AgNP-phytotoxicity remain largely
unknown, potential transmission of seed-harbored
AgNPs to next plant generation and their subsequent
fate within food chains is available. Because plants are
essential base component of ecosystem; as it is true
with metals–metalloids, plants may acts as a potential
pathway for AgNPs bioaccumulation and entering into
food chain. However, limited phytotoxicity studies
reported both positive and negative effects of AgNPs
on higher plants. The available AgNP-phytotoxicity
studies have revealed that AgNPs may enter the plant
system and disturb the growth and physiology/bio-
chemistry of plants by impairing mitosis causing
chromosomal abnormalities and micronuclei. The
question/concern pertaining to the AgNPs biotrans-
formation in food crops—in particular—possible
AgNPs-transmission to the next generation of Ag-
NPs-exposed plants remains wide-open unanswered.
The uptake mechanisms and distribution of AgNPs in
cells are still insufficiently explored, and very few
studies have addressed this question. In particular,
future plant toxicological research should intensify the
inclusion of different plant types while evaluating the
overall toxicological impact of the rapidly mounting
AgNPs in the environment.
As it has widely been established in different plants
under metal–metalloids exposure, the significance of
ascorbate–glutathione pathway components in the
protection of plants under AgNPs exposure against
AgNP-accrued oxidative stress, however, are so far
123
J Nanopart Res (2013) 15:1896
scarcely investigated. Molecular-genetic mechanisms
underlying AgNP-uptake across the plant cell mem-
brane, generation of reactive oxygen species, the
activation of redox-sensitive signaling cascades, and
the major cell organelle-specific responses to AgNPs
should be explored. Hence, a multi-level standard
biomarkers approach must be considered in order to
get better insights into the AgNPs potential to cause
toxicity at cytological, genetic physiological/bio-
chemical levels. It would also be imperative to
determine a relatively inexpensive and commonly
used short-term plant assay for in situ evaluation of the
potential bio-hazards of AgNPs in the environment.
Together, this approach would help understanding the
underlying AgNP-toxicity mechanisms, interpreting
molecular-genetic, and/or physiological/biochemical
data; which subsequently will complement current
toxicological screening strategies with a mechanism-
based approach. The interaction of AgNPs with other
persistent pollutants occurring at the same time should
be considered because these pollutants can both
amplify as well as alleviate the AgNP-toxicity. The
determination of AgNP’s potential transformation in
complex matrices of varied environmental compart-
ments including soil and also in biotic systems should
be worked out. Specific information on AgNP’s aging,
redox chemistry, and their light-driven transforma-
tions, including the creation of reactive sites by
photochemical pathways may yield important clues
on AgNP-environment interaction. Hence, in addition
to performing studies in laboratory settings, the
consideration of the ‘‘environmental AgNPs expo-
sure’’ will of great interest in order to further our
understanding of AgNP-fate and AgNP-impact in
terrestrial environments. Most importantly, the most
of the reports discussed herein have considered
germination and/or seedlings stage as the AgNP-
potential toxicity test system; which may not be
sensitive enough or appropriate for deciphering the
full picture of the ‘‘AgNP and/or its bulk counterpart
(Ag)-plants interaction’’ outcome. In contrast, toxicity
indicators based on biological markers, plant defense
mechanism, changes in plant integrity at cellular, or
genetic levels tested periodically during the plant’s life
cycle should be considered which were confirmed
earlier more appropriate in the current context. The
inclusion of a multidisciplinary integrated approach is
strongly recommended for future research in the
current direction aimed at unveiling quantitatively
J Nanopart Res (2013) 15:1896
and qualitatively the fate, transformation, accumula-
tion and toxicity potential of rapidly mounting
AgNPs-in ‘‘soil–plant systems,’’ and their cumulative
impact on environmental and human health.
Acknowledgments NAA (SFRH/BPD/84671/2012), ACD,
EP, and IA are grateful to the Portuguese Foundation for
Science and Technology (FCT) and the Aveiro University
Research Institute/Centre for Environmental and Marine Studies
(CESAM) for partial financial supports. SSG would like to
acknowledge the receipt of funds from CSIR and UGC, Govt. of
India, New Delhi. Authors apologize if some references related
to the main theme of the current review could not be cited due to
space constraint.
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