Environmental Chemistry Letters (2021) 19:1545–1609

https://doi.org/10.1007/s10311-020-01138-y

REVIEW

Nanoparticles in the soil–plant system: a review

Bilal Ahmed1,2 · Asfa Rizvi1 · Khursheed Ali1 · Jintae Lee2 · Almas Zaidi1 · Mohammad Saghir Khan1 ·
Javed Musarrat1,3

Received: 19 July 2020 / Accepted: 6 November 2020 / Published online: 4 January 2021
© Springer Nature Switzerland AG 2021

Abstract
Nanoparticles are increasingly used in many industrial sectors due to their unique properties, yet their introduction in eco-
systems is of concern for health and food security. In particular, the accumulation of nanoparticles in soils may disturb the
soil and plant system, possibly inducing a risk for crop production. Here, we review recent advances on nanoparticles in the
soil–plant system. We focus on sources, emission, transformation, bioavailability, interactions, phytotoxicity and plant uptake
of nanoparticles. We emphasize the genomic, metabolomic and proteomic alterations in plants caused by nanoparticles.
Besides negative impacts, benefits of nanoparticles for plant growth are discussed.

Keywords Nanoparticles · Transformation · Bioaccumulation · Phytotoxicity · Plant safety · Toxicity mechanism

Introduction metal oxides, nano-polymers, quantum dots, lipids, semicon-

ductors, dendrimers, and carbonaceous materials, with vary-
The term nanoparticle, which forms the basis of nanotech- ing morphological features such as particles, fibers, rods,
nology, is a particle having a diameter less than a 100 nm. wires, sheets, and flowers (Gentile et al. 2016; Sudha et al.
Nanoparticles have size-dependent physicochemical proper- 2018). Due to multiple properties, they are used in many
ties that are usually different from their bulk or sub-micron/ sectors from agriculture to industries (Srivastava et al. 2018;
micron-sized counterparts (Dasgupta et al. 2017). Among Yata et al. 2018).
many qualities, relatively higher surface area (S)-to-volume However, the large-scale production of nano-enabled
(V) ratio is the foremost peculiar feature of nanoparticles goods and leaching of nanoparticles either from industrial
which provides them high reactivity and physicochemical discharge (e.g., tannery effluents) or from nano-based house-
dynamicity (Mauter et al. 2018). Besides this, the distin- hold products (e.g., sewage waste) into different environ-
guish behavior of nanoparticles than their bulk materials in ments threats their sustainability, adding massive amounts
the environment is also determined by the greater surface of nanoparticles to both terrestrial and aquatic environment
energy and quantum confinement (Ma et al. 2010). Based (Ma et al. 2014; Eduok et al. 2015; Brown 2017) and other
on structure and chemical compositions, nanoparticles are biosphere (Kulizhskiy et al. 2017). The agricultural soils
categorized in different groups including zero-valent metals, generally encounter nanoparticles, incidentally, via untreated
wastewater used for irrigation or via bio-solids applied for
fertilization (Rawat et al. 2018). Since nanoparticles are
* Bilal Ahmed biologically nondestructive, they persist in soil system for
[email protected] longer durations and their alone or combined action alters
* Jintae Lee the fertility of soils, population of soil microflora, and physi-
[email protected] ology and metabolism of important plants (Fayiga 2017;
1
Department of Agricultural Microbiology, Aligarh Muslim
Pittol et al. 2017; Yanga et al. 2017). However, reports on
University, Aligarh 202002, India impact of nanoparticles on plants are conflicting. For exam-
2
School of Chemical Engineering, Yeungnam University,
ple, nanoparticles such as ­Cu2O (0–160 ppm) and ­TiO2
Gyeongsan, Republic of Korea (0.05–0.2 g ­L−1) in some studies, enhanced the growth
3
School of Biosciences and Biotechnology, Baba Ghulam
of tomato by increasing germination, root/shoot elonga-
Shah Badshah University, Rajouri, Jammu and Kashmir, tion (Ananda et al. 2019), transpiration, and chlorophyll
India

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1546 Environmental Chemistry Letters (2021) 19:1545–1609

synthesis (Qi et al. 2013). In contrast, nanoparticles when Source, emission and release
entering plant cells either via endocytosis or by other trans- of nanoparticles
port systems and accumulating inside plant tissues (Palocci
et al. 2017; Burman and Kumar 2018) have been found to The major source, which adds nanoparticles to the envi-
interact with plant molecules leading eventually to the dis- ronment, is presented in Fig. 1. Due to the increasing
tortion of morpho-anatomical features and many physiologi- applications of nanotechnology, varying range and types
cal activities of plants (García-Gómez et al. 2018a). of individual nanoparticles are fabricated each day whose
Phytotoxic nanoparticles when interacting with plants concentration in soil, water, and other ecosystem is likely
can cause mutagenic DNA lesions (Atha et al. 2012), gen- to upsurge massively in the near future.
erate reactive oxygen species, destruct cellular membranes, The production of nano-enabled goods is likely to
enhance membrane lipid peroxidation, and thus inhibit increase multiple times in near future (Boyes 2018). An
metabolism and growth of plants (Du et al. 2017b; García- estimate shows that globally, the nanotechnology indus-
Gómez et al. 2017). Moreover, the trans-generational impact try will attain a gross value of 75.8 billion USD by 2020
of nanoparticles has been reported (Hawthorne et al. 2014). (Global Nanotechnology Market Outlook 2024, 2020). The
This impact of nanoparticles on plants is determined by North American Free Trade Agreement (NAFTA) region
extent of nanoparticles’ (i) uptake, (ii) accumulation in plant shared the principal fraction from the nanotechnology
organs and (iii) subsequent translocation to various sites. market size. On the other hand, Europe and Asia espe-
These three processes also depend upon physicochemical cially Japan, India, and China are also stepping ahead very
features of nanoparticles, genotypes, and anatomy of plants dynamically. Nano-enabled products are being produced
(Landa et al. 2016; Rastogi et al. 2017). Despite the growing worldwide. Among nano-enabled products manufactur-
amount of research, the available scientific literature provid- ing countries, the USA, China, Germany, Switzerland,
ing details on nano-phytotoxicity is scattered here and there and South Korea are the top five nations, which produce a
and, hence, requires meaningful and immediate attention maximum of 2777, 719, 707, 457, and 319 nano-enabled
to better explain the inhibitory or promoting consequences products, respectively (Fig. 2a) for use in industrial divi-
of nanoparticles on crop production in a systematic man- sions such as electronics, medicine, cosmetics, construc-
ner. Realizing the gap in this area, an attempt is made in tion, textile, automotive, environment, renewable energy,
this review to provide a holistic view on how nanoparticles and food (Fig. 2b). An inventory of nano-enabled products
influence the overall performance of crops. Also, the bio- suggested that > 1814 nano-enabled products have been
transformation, bio-distribution, fate, and translocation of manufactured and are projected to increase threefold by
nanoparticles in plants are discussed. the end of 2020 (www.nanop​roduc​t.org/inven​torie​s/consu​

Fig. 1  Sources of emission and

Emission
release of nanoparticles into
the environment during: (i) raw Raw material manufacturing
materials manufacturing, (ii) Nano-enabled product manufacturing
nano-enable product manufac- A long manufacturing Use
line; during packaging;
turing, (iii) use of nano-prod- During mixing, blending; Waste management
during transfer to other
ucts, and (iv) management of equipment/facilities; embedding process; During product
nano-waste leading to nano- during machine application; during
through manufacturing
maintenance; through product wear and During waste
particle dispersion in air, soil, waste
tear; during waste treatment; during waste
process exhaust
and water. Secondary emissions disposal/sewage management; during
from humans or non-human water sewer/wastewater
species may also contribute to treatment
nanoparticles’ concentration in
the environment

Secondary Significant dispersal

emissions through air, soil, and water

Nanoparticles enter environmental

compartments

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Environmental Chemistry Letters (2021) 19:1545–1609 1547

A
No. 707
Germany
Russia
No. 210
No. 284
United Kingdom No. 303
Japan
USA
No. 2777
No. 457 Iran China
Switzerland No. 260 No. 719 No. 319
South Korea
Taiwan
No. 166
100

3000
Intensity

B
1000
Nano-enabled Products

140 South Korea

Nano-enabled Products

USA United Kingdom

800 China 120 Iran
Germany 100 Russia
Number of

Number of

600 Switzerland Taiwan

Japan 80
400 60
40
200
20
0 0
Fo y
ab Ot nt
C osm ine

En rs

od
ru s

A Te n
En om tile

nm e
C dic s

g
ro iv
st tic
M ic
Fo y
nm e
a b O t nt
En rs
ed ics
C os m ine

En m tile
A Te n

od
ru s

io

e
le he
er
g
r o iv
st tic
io

vi ot
on

ut x
ct
e
le he

on e
er
vi ot
on
C ic

ut x
ct
on e

tr
e
ec
tr

o
ec
M

El
El

ew
ew

en
en

R
R

Products in Industrial Sub-divisions Products in Industrial Sub-divisions

Fig. 2  a Number of nano-products in industrial divisions by major ://produ​ct.statn​ano.com/) and presented graphically. Accessed date
world countries. The number (No.) adjacent to a country name indi- April 02, 2020. b Number of nanotechnology products in industrial
cates the total number of nanotechnology products from that country. subdivisions. The data have been obtained from the Nanotechnol-
The scale bar represents lower (orange) to higher (red) intensity of ogy Product Database (https​://produ​ct.statn​ano.com/) and presented
nanotechnology products at a scale from 100 to 3000. The data have graphically. Accessed date April 02, 2020
been obtained from the Nanotechnology Product Database (https​

mer). However, > 8800 nanotechnology-based products are and personal care products are released when in use and
now in commercial market from 60 countries and > 2300 hence further contaminate both the surface water and soil
manufacturers. (Keller et al. 2013). The leaching speed may, however,
Among the nano-enabled products, nanoparticles used in vary among nanoparticles and depends on the manufactur-
paints, pigments, and coatings have the maximum chances ing process (Rajput et al. 2018b). For instance, dynamic
of being discharged into water, air, and soil, whereas nano- probabilistic modeling of nanoparticles emissions showed
particles used in optics and electronics are prospective to be that titanium dioxide ­(TiO2) nanoparticles had far greater
disposed of in landfills. The nanoparticles used in cosmetics concentrations in the environment than zinc oxide (ZnO)

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1548 Environmental Chemistry Letters (2021) 19:1545–1609

nanoparticles and Ag nanoparticles. In the worst case, sedi- specifically deliver their active ingredients to the target sites.
ment analysis revealed that the nanoparticles concentra- The nanoparticles which are applied for crop production
tions might range from 6.7 μg kg−1 for carbon nanotubes include nano-based fertilizers (Adisa et al. 2019), nano-fun-
to approximately 40,000 μg kg−1 for T ­ iO2 nanoparticles. gicides (Capaldi Arruda et al. 2015; Saharan et al. 2015), and
Moreover, this concentration in most cases may increase up insecticides (Wibowo et al. 2014). In agricultural systems,
to mg ­kg−1 level (Sun et al. 2016). nano-metal-based pesticides are generally applied through
Nanoparticle accumulated in soils systems may also foliar spray (Hong et al. 2015). For instance, among nano-
reach to the ground through the soil (Mahdi et al. 2018) and agrochemicals, pesticides containing nanoscale Cu(OH)2
from there can directly affect human health. Some nano- as active ingredient are in the marketplace and applied in
particles have been used for ground water remediation to agricultural fields at an increasing annual input; however, the
remove organic and inorganic pollutants (Matlochová et al. toxicity of these kind of nano-pesticides may prevent their
2013). Such nanoparticles may also be an additional source use in pest control (Zhao et al. 2016b; Zhang et al. 2019b).
of nano-pollution to ground water. Besides soil system and Once released as aerosolized sprays, waste effluents, and dry
ground water, a significant amount of engineered nanopar- powders containing aged and pristine nanoparticles, pollutes
ticles is released out to the atmosphere by various industrial soil ecosystem (Keller et al. 2013; Cornelis et al. 2014a;
activities including both point (manufacturing units, waste Ju-Nam and Lead 2016). Nanoparticles may also reach to
incineration, power plants wastewater treatment plants, dur- soils accidentally; for example, diesel fuel combustion emits
ing transportation, and landfilling) (Gottschalk and Nowack ­CeO2 nanoparticles in the atmosphere. Due to the deposition
2011) and non-point sources (vehicle emission, during of nanoparticles in soils, it becomes imperative to assess its
washing or abrasion of nano-enabled products) (Peng et al. overall impact on biotic component of soils.
2017b). In addition, accidental release of nanoparticles may
increase the magnitude of localized atmospheric concen-
tration. As per an estimate, globally, approximately 8,100
metric tons of engineered nanoparticles are emitted into the Nanoparticles and plants
atmosphere annually (Keller and Lazareva 2013) relative
to nanoparticles’ discharge in water and soil; however, the The nanoparticles prevalent in atmosphere, water and soil
atmospheric fraction of nanoparticles have a shorter dwell- interact with plants (Fig. 3). When accumulated in plants,
ing period (John et al. 2017) and ultimately get deposited in nanoparticles enter the food chain via uptake by plants
soil or water bodies (Giese et al. 2018). Also, the transfor- and decide their fate in the environment (Rai et al. 2018).
mational processes occurring in the atmosphere may influ- Atmospheric nanoparticles can easily deposit on various
ence the interactions and fate of atmospheric nanoparticles plant surfaces and hence can infiltrate into the plant system
in soil or aquatic system (Abbas et al. 2020). via wounds and stomatal apertures (Pérez-de-Luque 2017).
The increased applications of nano-enabled/nano-engi- Within soil ecosystems, the purposely applied water-borne
neered products (Villaseñor and Ríos 2018), however, are nanoparticles may also have interaction with plant tissues
likely to add enhanced concentration of nanoparticles in the (Mauter et al. 2018). The plant roots first come in contact
environment through various routes with unknown impacts with soil released nanoparticles or soil containing waste-
on water, soil, and biota (Eduok and Coulon 2017). In many water effluents applied for crop nutrition (Gottschalk et al.
cases, the nanoparticles do not remain bound to the prod- 2009; Cox et al. 2017). Considering these, the overall impact
ucts at the end of its life cycle (Cao and Liu 2016). This of nanoparticles on edible crops and plants grown for longer
can be explained by the presence of nanoparticles in landfill duration in soils contaminated with nanoparticles must be
chelates (Bolyard et al. 2013), sewage sludge (Wang et al. evaluated. For testing nanoparticles against various crop
2012b), and wastewater effluents (Brar et al. 2010). Of these, plants, in vitro approaches such as nanoparticles amend-
55% wastewater containing sewage sludge is applied as soil ment in nutrient agar media and different strengths hydro-
amendment to agricultural soils enriching soil nutrients. Due ponic solutions have been tested which are simpler providing
to these, the use of wastewater containing aged nanoparticles control over nanoparticles’ distribution in media and there-
becomes the primary source of nanoparticle to the environ- fore maximize the contact and uptake of nanoparticles with
ment (Eduok and Coulon 2017). plant system (Sharma et al. 2020; Ullah et al. 2020). As an
The use of nano-based pesticides/fertilizers in agricul- example of semi-solid plant growth media, Murashige and
ture to effectively control the growth of plant pathogenic Skoog (MS) is amended with varying concentrations of nan-
microbes and hence to optimize plant growth/yields has oparticles (Nechitailo et al. 2018; Plaksenkova et al. 2019).
also been the major source of nanoparticles in soil ecosys- Moreover, hydroponic nutrient media providing nutrients
tems (Mukherjee et al. 2016; Chhipa 2017). In agrochemi- and aeration to the growing seedlings have been tested for
cals formulation prepared with nanoparticles are aimed to more than seven days in many studies with variably shaped

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Environmental Chemistry Letters (2021) 19:1545–1609 1549

P Nanoparcles

L
A
N Entry

T
Upper Ground

Uptake
Below Ground

Nanoparcle- Nanoparcle- Nanoparcle-Soil

Plant interacon Rhizosphere interacon interacon
A Plant (species
B Soil environment affects C
type, growth Transport
stage)
Type of soil Bioavailability
Toxicity

Phytotoxicity of
nanoparcles is
Interacon Soil
governed by
mainly
three factors depends on
Major soil physicochemical properes
Experimental Size,
Time of determining fate and sorpon of NPs
(temperature,
me, and method
concentraon, Soil exposure Organic maer
and aggregaon
of exposure) of nanoparcles microflora Soil pH
Caon exchange capacity
Organic maer

Fig. 3  Interactions of nanoparticles with three components of soils aggregation, size, and concentration; environment dependent: panel
(i) plants, (ii) soil microflora, and (iii) soil itself. Plant and nanopar- B) interaction between nanoparticles and rhizosphere also determine
ticle dependent: panel A) phytotoxicity of nanoparticles is governed their impact on plants. Such interactions include biological activity
by three factors which are: (i) plant dependent: growth stage and type of indigenous soil microflora, exposure time, and soil type, and panel
of plant species, (ii) experimental: test method, time of exposure, C) physicochemical properties of soil also influence the transport of
temperature and pH of growth media, and (iii) dependent on phys- nanoparticles in soil, their bioavailability, and subsequent impact on
icochemical features of test nanoparticles, i.e., chemical composition, plants

and sized nanoparticles (Wang et al. 2012c; Sun et al. 2019a; are likely to enhance the exposure time of important crops
Li et al. 2020). which in turn affects their accumulation kinetics and toxic
Soil mixed media or soil itself is considered more practi- impact (Dev et al. 2018). For this, life cycle studies have
cal due largely to its buffering capacity that can modify the been carried out assessing the impact of C ­ eO2 nanoparti-
reactivity of test nano-species. Besides this, porous materi- cles on tomato crop for 210 days potting soil (Barrios et al.
als such as sand along with soil may also alter the available 2016), ­CeO2 and ZnO nanoparticles on soybean (Hernan-
fraction of nanoparticles to plants or affect their stability dez-Viezcas et al. 2013), and ­TiO2, ­CeO2, and Cu(OH)2 on
(Khodakovskaya et al. 2013; Gómez-Sagasti et al. 2019). elegant clarkia (Conway et al. 2015).
Therefore, to reveal the phyto-toxicological profile of a
nanoparticle, detailed and systemic phyto-toxicity studies
should be conducted keeping in view the various abiotic Plant exudates and nanoparticles
factors of soils, type of soil, simultaneous interactions with
soil microflora, time, and concentration of nanoparticle Indeed, the plant secretions strongly influence soil structure
exposure (Fig. 3). This is needed because the uncontrolled and binding of nanoparticles on plant surfaces (Fig. 4) (Sid-
disposal and persistence of nanoparticles in the environment diqi and Husen 2017a). Plant roots are known to secrete

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1550 Environmental Chemistry Letters (2021) 19:1545–1609

Fig. 4  Interactions between

plant root exudates and
nanoparticles: (i) Root exudates
(organic acids, amino acids,
and carbohydrates) induce
transformation of nanoparticles,
and (ii) nanoparticles can also
alter the root exudate pattern of
plant facilitating nanoparticle’s
transformation

Impact of exudates
on nanoparticle
uptake and
translocation

Roots
Release of
Nanoparticles metal ions

Transformation
-COOH, -SH,
of nanoparticles
-OH Exudates- organic
Mobilization / acids, amino acids
Immobilization Rhizosphere and carbohydrates

Soil Soil
microbes system Modified composition
of root exudates

exudates containing large quantities of varying molecular to plant root exudate profile of plants (Pallavi et al. 2016).
weight biomolecules and inorganic ions, which differ in On the other hand, zinc applied as ZnO nanoparticles to
composition and concentration. The root exudation pat- soybean plants was found to exist as a transformed species
tern may vary with plant species and may include variable ­(Zn2+), zinc citrate due to the influence of root exudates
amounts of high molecular weight organics like fatty acids (Hesrnandez-Viezcas et al. 2013). Root tips and root hairs
and polysaccharides, and low molecular weight substances secrete a considerable amount of a hydrated polysaccharide,
including amino and organic acids forming a nutritional the mucilage on root surface (Driouich et al. 2013; Holz
environment to a certain distance around root surface known et al. 2018). Mucilage creates an acidic environment in the
as “rhizosphere” (Bais et al. 2006). Nanoparticles applied rhizosphere and passively protects both rhizosphere and
to soils, when comes in direct contact of exudates, can eas- plant from biotic and abiotic stresses. Thus, mucilage can
ily be deposited on or adhered to root surface (Ma et al. also assist in adsorption of nanoparticles on the surface of
2013c; Zhao et al. 2016a; Gao et al. 2018). Consequently, root. The acidic environment dissolves nanoparticles and lib-
the adsorbed nanoparticles undergo extensive physicochemi- erates free metal ions which are then metabolized by plants
cal modification following specific or random interactions to other chemical forms or just deposited somewhere in plant
with root exudates, and sometimes simultaneously with tissues. For instance, Au and ZnO nanoparticles are oxidized
humic acids (Rico et al. 2011). The oxidizing and reducing due to acidic environment (Taylor et al. 2014; García-Gómez
agents secreted by plants into the soil can transform metal et al. 2018a). Furthermore, CuO nanoparticles are dissolved
containing nanoparticles of variable valance shell by per- to Cu ions under the influence of root exudate organic acids
forming various redox reactions (Wang et al. 2012a; Zhang lowering the soil pH (Shi et al. 2011).
et al. 2017). It can be inferred from nano-phyto interactions that nano-
The physicochemical modification by plant exudates particles are aggregated around roots under the influence
can therefore alter the magnitude of bioaccumulation and of single or a mixture of root exudates. Plant exudates may
ultimate fate of nanoparticles in soil or plant system. Simi- also precipitate the metal species as described for Fe and Cu
larly, nanoparticles can also change the exudation pattern which were precipitated as copper or iron hydroxides and
of plants (Dimkpa et al. 2012; Wang et al. 2013a; Lv et al. therefore were not available for uptake by plants (Dimkpa
2015) (Fig. 4). For instance, it has been suggested that Ag et al. 2015). Recently, a metabolomic study of cucumber
nanoparticles could induce a change in root exudation pat- root exudates based on 1H-NMR and GC–MS analyses has
tern of wheat, cowpea, and mustard that resulted in modified revealed that Cu nanoparticles at 10 and 20 mg ­L−1 dose
rhizosphere microbial composition which is highly specific rate-induced defense response against Cu nanoparticles

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Environmental Chemistry Letters (2021) 19:1545–1609 1551

stress (Zhao et al. 2016a). The production of amino acids, significantly affecting the aggregation of nanoparticles
ascorbic acid, and phenolic compounds increased the seques- include magnetic and hydrophobic interactions, and hydra-
tration of Cu nanoparticles/ions, combats against reactive tion force (Dwivedi et al. 2015; Sendra et al. 2017). The
oxygen species, and enhanced the antioxidant enzyme activ- agglomeration or aggregation could be of two types: (a)
ity. In contrast, citric acids were down-regulated reducing homo-aggregation—it occurs when the aggregates of similar
the mobilization of copper ions (Zhao et al. 2016a). nanoparticles are produced, and (b) hetero-aggregation—in
Soil microflora especially the fungal and bacterial popu- this process, a cocktail of other components interacts with
lation on the other hand also affects the nanoparticle’s con- nanoparticles and promotes aggregation (Fig. 5) (Xu et al.
version with the help of extracellular enzymes including 2018). Of these, hetero-aggregation is the more common
phosphatases and phytases having Zn as a co-factor (Singh phenomenon that occurs in the environment (Schultz et al.
and Satyanarayana 2011). Rhizosphere microbes secrete 2015). The aggregation of nanoparticles generally decreases
considerable amounts of phosphatases and phytases which the chemical reactivity and bioavailable concentration of
mobilize the native phosphorus and help in phosphorus nanoparticles and increases the aggregate size with increas-
acquisition by plant roots (Richardson 2001). In a study, ing time periods (Quik et al. 2014). Additionally, when
mung bean plant exposure to ZnO nanoparticles increased present in higher concentrations, the nanoparticles form
activity of phytase and phosphatase (both alkaline and acid) aggregates rapidly due to enhanced collision frequency. In
in soil due to enhanced fungal, bacterial, and actinomycetes this event, the surface energy of nanoparticles is drastically
population. The application of ZnO nanoparticles (23 nm) reduced in a thermodynamically determined progression.
increased phytase activity by 108%, alkaline phosphatase by This has been confirmed by a faster aggregation rate of
93.02%, acid phosphatase by 98.07%, and dehydrogenase by nanoparticles of ZnO (Yung et al. 2015), ­TiO2 (Botta et al.
84.21% over their bulk counterparts (Raliya et al. 2016b). 2011), and ­CeO2 (Marie et al. 2014). Furthermore, nano-
Also, the activity of dehydrogenase was increased indicating particle’s coating may also increase or decrease the rate of
higher microbial density (Raliya et al. 2016b). Moreover, aggregation in the environment (Xu et al. 2018).
the role of compounds like organic acids, carbohydrates,
proteins, and extracellular byproducts from indigenous soil Adsorption
microbial population in nanoparticle’s transformation is yet
to be explored. Nanoparticles have the tendency to adsorb to various envi-
ronmental substances such as natural organic matter. This
adsorption is governed by two factors: physicochemical
Transformation of nanoparticles

The ultimate environmental fate, extent of transport, behav- Nanoparcle suspension

ior in the environment and toxicity of nanoparticles are Hetero-aggregaon
and/or adsorpon
influenced by various transformational processes such as (A)
physical (i) agglomeration/aggregation, (ii) adsorption, and
Homo-aggregaon

Nanoparcles
(iii) deposition, (B) chemical (i) sulfidation, (ii) dissolution,
and (iii) redox reactions, and (C) interaction of nanoparti- Constuents of Deposion
environment
cles with macromolecules. Many of these transformations
may occur both in environmental and biological systems.
Hetero-aggregaon
Hence, the behavior and magnitude of these transformations
must be understood so that the strategy to contain/reduce Deposion
the environmental risks posed by nanoparticles, if any, can Homo-aggregaon Hetero-aggregaon
be devised. Surface charge Parcle size
Parcle size Reacvity
Reacvity Toxicity
Physical transformations Toxicity Bioavailability
Affects transport

Agglomeration/aggregation
Fig. 5  Homo-aggregation, hetero-aggregation and deposition of
nanoparticles in the environment. Red arrows show disaggregation
Aggregation is the process by which nanoparticles form of nanoparticles due to lower pH and the presence of natural organic
a cluster of varying sizes (Wang et al. 2016b). Aggrega- matter. Like homo-aggregation, which increases particle size and
tion of nanoparticles results majorly due to van der Waals thereby reduces surface charge, reactivity, and toxicity of nanoparti-
cles, hetero-aggregation also reduces these important physicochemi-
force and formation of electric double layer of counter ions cal parameters of nanoparticles but with the involvement of other
(Adamczyk and Weroński 1999). Some other interactions constituents of the local environment

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1552 Environmental Chemistry Letters (2021) 19:1545–1609

properties of natural organic matter and surface chemistry et al. 2015). Due to the inherent property of greater surface
of nanoparticles. If the surface functionalization of nano- area, such nanoparticles release high amount of free metal
particles is not strong, then the natural organic matter will ions over their larger counterparts (Zhang et al. 2018b). For
stabilize the nanoparticle; on the opposite site, higher N example, dissolution of ZnO nanoparticles (4–130 nm) at
and S content of natural organic matter will increase the pH 7.5 revealed that the higher S/V ratio of smaller sized
adsorption of nanoparticle (Gunsolus et al. 2015; Jorge de ZnO nanoparticles was more favorable for dissolution
Souza et al. 2019). In an earlier study, the surface adsorp- as compared to larger ones (Mudunkotuwa et al. 2012).
tion of natural organic matter either neutralizes the surface Similarly, the rate of dissolution was also found higher
charge or reverses it (Baalousha et al. 2008). Also, the natu- for smaller (7 nm) CuO nanoparticles (Chakraborty et al.
ral organic matter after adsorbing on nanoparticle surface 2018). Similar impact of nanoparticle size on dissolution
may hinder the release of ions due to natural organic matter was observed for ­Fe2O3 nanoparticles where the rate of dis-
mediated blocking of oxidation sites or reduce the already solution of 8 nm sized particles was increased up to ten-
released metal ions to their zero-valent form by fulvic and fold compared to 40 nm sized particles (Lanzl et al. 2012).
humic acids. The adsorption of nanoparticles to differ- Surface chemistry of nanoparticles may also significantly
ent surfaces is also influenced by other factors too. These increase or decrease the rate of dissolution which is other-
include environmental fluids or biomolecules. The protein wise useful for some applications. For instance, in a com-
fraction of these environmental fluids may form a corona parative dissolution study, organic coating of ZnO nanopar-
around nanoparticles known as “protein corona.” Generally, ticles delayed the rate of dissolution which reached to its
it is termed as eco-corona or corona when formed by the maxima in seven days. On the other hand, uncoated ZnO
collective adsorption of environmental constituents ranging nanoparticles showed maximum dissolution in just one hour
in size from 10 Da to 2 × 106 Da (Nasser et al. 2020). This (Gelabert et al. 2014). For various purposes, the shape and
adsorption is capable of altering the size, charge, and aggre- size of nanoparticles are tuned using surface capping/func-
gation of nanoparticles (Pinďáková et al. 2017). The process tionalizing agents; however, the use of surface modifying
of nanoparticles adsorption under different environmental agents alters the dissolution of nanoparticles in one or the
scenarios needs to be investigated further due to its impor- other way. As a classical example among metal-based nano-
tance in affecting the nanoparticle–cell interactions. particles, Ag nanoparticles (50 nm) have shown variable
dissolution when capped by citrate or polyvinylpyrrolidone
Deposition (PVP) (Kittler et al. 2010). The dissolution was 14% and
50% for citrate and PVP capped Ag nanoparticles, respec-
Deposition is the process by which nanoparticles dispersed tively, at 25 °C.
in aqueous environment tend to settle down on bottom,
which mainly occurs in the aquatic environment. The depo- Chemistry within the environmental system The dissolu-
sition, however, may differ with types, the extent of aggrega- tion of nanoparticles also depends on environmental factors
tion, and availability of natural organic materials. Overall, such as pH (Son et al. 2015), natural organic matter content
agglomeration, aggregation, and deposition are interrelated. (Jiang et al. 2015; Wang et al. 2016b), ionic strength (Yung
When aggregation increases, the deposition also increases et al. 2015; Liu et al. 2018), and temperature (Majedi et al.
which may be controlled by nanoparticles features and the 2013). Taking the example of pH mediated dissolution, dis-
physicochemical properties of the media (Amde et al. 2017). solution of ZnO and CuO nanoparticles were found higher
at acidic pH and lower at alkaline pH (Miao et al. 2010;
Chemical transformations Mohd Omar et al. 2014; Son et al. 2015; Odzak et al. 2017).
In a recent study, the dissolution behavior of CuO nanopar-
Dissolution ticles measuring the size of 7 nm and 31 nm in artificial
lysosomal fluid, simulated body fluid, artificial seawater,
The process of dissolution of nanoparticles (release of solu- and sodium nitrate (1 mM) was assessed (Chakraborty et al.
ble metal ions from nanoparticles) is dependent on both the 2018). The results revealed significant differences in the
physicochemical features of nanoparticles and chemistry of dissolution of CuO nanoparticles which was attributed to
the environmental system (Cross et al. 2015). variation in composition and concentration of media. The
dissolution was > 80% in biological media within 12–24 h,
Physicochemical features of nanoparticles Among various whereas < 15% in environmental media even after 7 days
physicochemical features, size, morphology, and surface (Chakraborty et al. 2018). In addition, the presence of
chemistry are major in controlling the dissolution of nano- natural organic matter inhibits the release of metal ions by
particles. The change in surface area-to-volume (S/V) ratio reducing them to nanoparticles through fulvic acids such
of nanoparticles affects the dissolution process (Soenen as the formation of ­Ag+-fulvic acid complex leading to the

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Environmental Chemistry Letters (2021) 19:1545–1609 1553

formation of Ag nanoparticles and thus reducing the rate of soluble proteins under aqueous condition (Gong et al. 2011).
dissolution (Tiwari et al. 2013). Similarly, significant dis- Redox reactions bring two changes which significantly affect
solution was observed for CuO and ZnO nanoparticles and the environmental fate of nanoparticles. If redox reactions
among them, ZnO nanoparticles reflected greater influence make the nanoparticle’s surface active, then the reaction of
(Liu et al. 2018). The sedimentation rates of ZnO nano- environmental constituents and nanoparticles will be facili-
particles and CuO nanoparticles in five types of water fol- tated. On the contrary, if insoluble surface is resulted due
lowed the order: tap water > wastewater > lake water > pool to redox reactions, it will increase nanoparticle’s stability,
water > rainwater (Liu et al. 2018). thus increasing the persistence of nanoparticles. Moreover,
the dissolution of nanoparticles can also be enhanced by the
Sulfidation oxidation process. Nanoparticle’s capping may also affect
the oxidation–reduction processes. As an example, silica
The presence of sulfide in the surrounding medium also coating of iron oxide (­ Fe2O4) nanoparticles was found more
influences fate of nanoparticles. In the process of sulfida- resistant than uncoated particles toward oxidation process
tion, sulfide is oxidized to sulfate and metal ions released (Cendrowski et al. 2017).
from nanoparticles reduced. For example, reduction of C ­ u2+
+
released from CuO nanoparticles to C ­ u forming copper sul- Interaction of nanoparticles with macromolecules
fate hydroxides (Ma et al. 2013b). Moreover, after dissolu-
tion of nanoparticles such as CuO and Cu nanoparticles, The nanoparticles have been reported to interact with mac-
the sulfidation process could compete with the high disso- romolecules such as proteins, polysaccharides, surfactants,
lution (Kent and Vikesland 2016). The process of nanopar- and varying types of natural organic matter modifying their
ticle sulfidation is dependent of the total concentration of surface and physicochemical features (Ansari et al. 2014;
sulfides in the media. Sometimes, excess presence of sulfide Wang et al. 2016b; Schwaminger et al. 2017). This interac-
results in the 100% sulfidation of nanoparticles in a solution tion between the nanoparticle and macromolecules depends
(Ma et al. 2013b). For example, low concentration of sulfide on the concentration, type of molecules/nanoparticles, pH,
(< 1 mg ­L−1) could initiate release of A
­ g+ ions from Ag nan- and binding affinity (Philippe and Schaumann 2014; Yu et al.
oparticles which then form silver sulfide ­(Ag2S) nano-link- 2018). These interactions include electrostatic, H-bonding,
ages with adjacent nanoparticles by reacting with sulfide. On hydrophobic, bridging between macromolecules and nano-
the other hand, when the sulfide concentration is between 1 particles, van der Waals force, ligand exchange reaction, and
and 100 mg ­L−1, the formation of ­Ag2S is direct following chelation (Fig. 6). Furthermore, the macromolecules by one
the oxy-sulfidation pathway (Liu et al. 2011). Similarly, zinc or multiple interactions with nanoparticles can cause co-
sulfide (ZnS) was detected as a result of ZnO nanoparticle aggregation or provide electrostatic/steric stability reduc-
transformation in the presence of sulfide with the total ZnS ing the aggregation and thus deposition of nanoparticles
yield of up to 90% (Brunetti et al. 2015). (Huangfu et al. 2014; Sheng et al. 2016; Chen et al. 2018).
Besides these, other chemical processes including surface
Reduction–oxidation reactions oxidation, reactive oxygen species generation, and degrada-
tion of coat material can influence the nanoparticle–plant
These reactions include oxidation and reduction transfer- interactions either in a positive or negative way (Amde et al.
ring the electrons from one species to another. This is of 2017).
importance because nanoparticles also have various surface
constituents which may be influenced by redox reactions.
Moreover, these reactions transforming nanoparticles may Transformation of nanoparticles
vary depending upon the type of environment. For example, in the atmosphere
oxidation is predominant in aerated soils and waters, while
reduction occurs mainly in groundwaters and carbon-rich Annually, a small amount of engineered nanoparticles is
sediments (Cendrowski et al. 2017). In the aquatic envi- emitted into the atmosphere as compared to other environ-
ronment, natural organic matter may hinder the oxidation mental compartments (Keller and Lazareva 2013). Despite
reduction process due to its ability to inhibit the electron having a shorter span in the atmosphere (John et al. 2017),
transfer. Biological constituents of the environment by redox the nanoparticles undergo atmospheric physical and chemi-
reactions may alter the oxidation of metal component of cal transformations impacted by physicochemical features of
nanoparticles. For example, interaction of ­CeO2 nanoparti- nanoparticles, atmospheric gases, and weather-related condi-
cles with environmental media disturbs ratio of Ce III/IV in tions (Kumar and Al-Dabbous 2016). Interaction of nano-
­CeO2 nanoparticles (Baalousha et al. 2010). Similarly, NiO particles with atmospheric gases such as ­CO2 can poten-
nanoparticles were also found reduced to zero valent Ni by tially change nanoparticle’s features as well as their rate of

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1554 Environmental Chemistry Letters (2021) 19:1545–1609

Fig. 6  Forces controlling nano-

particle–macromolecule interac-
tions, including (i) hydrophobic
interaction, (ii) ligand exchange
reaction, (iii) electrostatic
attraction, (iv) bridging between
nanoparticles and other mol-
ecules, (v) hydrogen bonding,
(vi) nanoparticle chelation by
chelating agents such as amino/
organic/fatty acids, proteins, and
sugars, and (vii) van der Waals
force

dissolution after deposition in aqueous media. In a study, atmosphere (Tiwari and Marr 2010; Han et al. 2015). The
reaction of CuO and ZnO nanoparticles with ­CO2 at varying size of nanoparticles can also be increased by their conden-
levels of relative humidity (­ H2O) was performed (Gankanda sation with atmospheric inorganic (­ NH3, ­NO3−, and ­SO42−)
et al. 2016). Results revealed that surface adsorbed hydroxyl or organic moieties or both (Baalousha et al. 2016). Other
groups of both the nanoparticle reacted with ­CO2 which led factors altering the size and morphology of nanoparticles
the formation of surface adsorbed bicarbonates. On the other include turbulence, temperature, UV radiation, and free radi-
hand, reaction of C ­ O2 with nanoparticles surface defects cals (Zhang et al. 2016b).
and lattice oxygen resulted in surface adsorbed carboxylate
and mono- and bi-dentate carbonates. Progressing to high Transformation of nanoparticles in soil
humidity conditions (0–70%) showed water solvated surface
adsorbed carbonate. Overall, the change in surface chemistry Generally, nanoparticles persist for longer duration in sedi-
was limited to near surface region enhancing the dissolution ments and terrestrial locations where nanoparticles and their
of nanoparticles in liquid media. metal ions respond differently in soils and depend upon the
Both types of aggregation (homo and hetero) of nano- aging process and soil properties (Peijnenburg et al. 2016;
particles also occur in the atmosphere subject to Brownian Romero-Freire et al. 2017). Nanoparticle’s transformation in
motion and surface area of nanoparticles reducing the num- soil systems has been studied in greater detail recently. In a
ber of particles in the air while increasing its size. In the study, it is reported that the extractable amount of Cu from
atmosphere, hetero-aggregation is more common due to the soils exposed to CuO nanoparticles or Cu (­ NO3)2 in differ-
occurrence of natural air-borne nanoparticles and this new ent sets of experiments changed over time which was influ-
formation (binding of nanoparticles with airborne particles enced by source and concentration of Cu used (Gao et al.
such as particulate matter) may travel long distances in the 2017). Similarly, CuO nanoparticles may be transformed in

13
Environmental Chemistry Letters (2021) 19:1545–1609 1555

soil upon weathering which in turn affect the availability et al. 2013; Cui et al. 2014). The transformation of nano-
of Cu both in soil, uptake by lettuce plant, and Cu trans- particles in plant system may also occur in a way that nano-
port to higher trophic level (Servin et al. 2017). However, particle’s size is increased in plant organs. For example, Ag
the aging of CuO nanoparticles did not significantly affect nanoparticles taken up by tomato roots were found in large
the chlorophyll and carotenoid synthesis by lettuce plants. clusters ranging from 100 to 200 nm as compared to the
This could be due to the above discussed hetero-aggregation size in water suspension (1–10 nm). Also, some spherical
of nanoparticles which is more common in soil (Cornelis clusters of S­ nO2 nanoparticles were detected (Vittori Anti-
et al. 2014b). Nanoparticle’s aggregation in soil system also sari et al. 2015a). These and other studies are suggestive of
prevents their uptake by plants (Dimkpa et al. 2013). For extensive processing of nanoparticles in plant cell environ-
example, hetero-aggregation of ZnO nanoparticles with soil ment following their uptake, modifying its original form.
granules hindered their diffusion (Zhao et al. 2012b; Milani Some evidences are shown in Fig. 7.
et al. 2015). The organic substances of soil also influence The plant-mediated transformation in turn may reduce
the adsorption of nanoparticles on to soil surface and hence or enhance the phytotoxicity of nanoparticles. For instance,
enhance the stability of nanoparticles (Ju-Nam and Lead nano-CuO (copper II oxide) was found reduced to ­Cu2O and
2016). ­Cu2S (copper I oxide) in maize plants with symptoms of
The nanoparticles are also dissolved in soils by soil pore growth reduction (Wang et al. 2012c; Servin et al. 2017).
water. The released ions are more bioavailable than corre- Similar transformation of nano-CuO from Cu (II) → Cu (I)
sponding nanoparticles, where dissolution largely depends Cl is evident from the enhancement of degree of saturation
on the type and physicochemical properties of soil, besides in fatty acids (Yuan et al. 2016a). Copper may be partially
the application mode of nanoparticles in the soil such as biotransformed from Cu (II) to Cu (I) by interacting with
powder or solution forms. For instance, the ZnO nanopar- root secreted citrate from bean (Dimkpa et al. 2015). In a
ticles have been reported to undergo dissolution in soils to micro-X-ray fluorescence analysis of plant roots, the deposi-
an extent that the nanoparticles were not detected in nano- tion of Cu nanoparticles was restricted to the outer region of
particles spiked soil (Wang et al. 2013a). Likewise, the dis- root tissues, most likely due to intracellular transformation
solution of citrate coated ­CeO2 nanoparticles (8 nm) was of nano-Cu which limits its movement to other part of root
found considerably high in acidic media at pH 4.0 (Cornelis tissue (Servin et al. 2017). Similarly, cucumber-mediated
et al. 2011). A similar mechanism for enhanced dissolution transformation of nano-ytterbium oxide ­(Yb2O3) and nano-
of metal oxide nanoparticles by plants has been suggested lanthanum oxide ­(La2O3) has been documented (Ma et al.
which could be assigned to organic acids and siderophores 2011; Zhang et al. 2012b). Phosphate salts and organic
present in rhizosphere soils (Dimkpa et al. 2013; Schwabe acid from cucumber roots played a role in the solubiliza-
et al. 2015). The dissolution of CuO and ZnO nanoparticles tion of ­Yb2O3 and ­La2O3 and biotransformed them into their
was enhanced by wheat roots from less than 0.3 to 1 and 0.6 respective phosphates. Similarly, following the adsorption
to 1–2.2 mg kg−1, respectively. In contrast to higher disso- of ­Fe2O3 nanoparticles on various regions of root such as
lution, some metal–oxide nanoparticles such as ­TiO2 nano- hairs, tips, and meristematic zone and uptake inside the root
particles exhibit little dissolution in soils (Du et al. 2011). cells, ­Fe2O3 nanoparticles were bio-mineralized under the
root phytochemical influence (Shankramma et al. 2016).
Plant‑mediated transformation of nanoparticles A scheme for biotransformation of nanoparticles by plant
secretion and the internal environment of plants and their
The nanoparticles present in a different environment can impact is shown in Fig. 7I.
also be influenced or modified by biotic factors. For exam-
ple, nanoparticles prepared from CuO and ZnO were found
accumulated as copper–sulfur complexes and zinc phosphate Bioavailability of nanoparticles to plants
in wheat shoots, respectively, that was likely be due to the
dissolution of CuO and ZnO nanoparticles followed by their The bioavailability of nanoparticles to plants is a stability-
uptake and transformation inside the plant (Dimkpa et al. dependent factor (Von Moos et al. 2014). The more stable
2013). Nanoparticles also undergo various other transforma- the nanoparticles are in the environment, the lesser will be
tions in the plant physiological environment. In this context, their bioavailability, and hence, the nanoparticles exhibit low
a study revealed that ­CeO2 nanoparticles were influenced by toxicity (Auffan et al. 2009). For instance, the reduction of
structural and chemical changes occurring within the plants Ce from Ce(IV) to relatively more stable Ce (III) within the
(Zhang et al. 2012a). In a similar study, the use of X-ray- soil resulted in decreased bioavailability of ­CeO2 nanopar-
based fluorescence and absorption techniques confirmed ticles to plants (Cui et al. 2014). In contrast, enzymes and
various transformations in the chemical status of ZnO and other chelating agents released by soil organisms cause the
­CeO2 nanoparticles in plant system (Hernandez-Viezcas transformation of nanoparticles and make it more available

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1556 Environmental Chemistry Letters (2021) 19:1545–1609

A B E F

Intensity (a.u.)
Yb2 O3 G
YbAc3
YbPO4

C D G H
Intensity (a.u.)

Yb2 O3

YbAc3
YbPO4

I
CuO Cu2S/Cu2O
plant exudates:
La2O3, Yb2O3 mucilage, sugars, amino Phosphac forms in roots
Ni(OH)2 acids etc.; Internal plant Accumulated as Ni in ssues
environment
Cu (II) Cu (I), parally

Nanoparcles
Detoxificaon Biotransformaon
of plant system Toxicity

Plant mediated
dissoluon
NPs Ions High dissoluon
(ZnO, CuO) (Zn2+, Cu2+)

Direct uptake
Co-factor for phytase, phosphatase, and dehydrogenase
(low dissoluon)

Fig. 7  Plant-mediated transformation of nanoparticles: Ytterbium green and blue also indicate signals for CuCl and CuO, respectively.
component color maps of cucumber roots treated with 2000 mg L ­ −1 Adapted with permission from (Yuan et al. 2016b). Panel H shows
­Yb2O3–nanoparticles (panel A) and and 200 mg ­L−1 ­YbCl3 (panel XANES Ce LIII-edge spectra lettuce roots grown with C ­ eO2 nano-
C) derived from scanning transmission X-ray microscopy. Red, yel- particles (2000 mg ­L−1) and spectra of reference compounds. The
low, and blue regions show high, low, and zero Yb containing zones, dotted and dashed lines are for Ce (IV) and Ce (III) containing com-
respectively. Panels B and D represent 3D spectra of Yb component pounds, respectively. There are three peaks A, B, and C in panel H.
from panels A and C, respectively. In panels B and D, the 3D Yb Peak A is the characteristic of Ce (II), which comes from three Ce
spectra of root samples are comparatively analyzed with reference Yb compounds such as and C ­ e2(C2O4)3, Ce(CH3COO)3, and C ­ ePO4.
compounds such as Y ­ bPO4, ­Yb2O3, and Yb (Ac)3. Analysis showed Peaks B and C represent Ce(IV) of C ­ eO2 nanoparticles (NPs) accu-
that the compound present in roots treated with ­Yb2O3–nanoparticles mulated in lettuce roots. Comparative analysis of sample with refer-
can be inferred to be ­YbPO4. Adapted with permission from (Zhang ence Ce compounds revealed that there were two oxidation states of
et al. 2012b). Transmission electron microscopy (TEM) (panel E) and Ce present in roots, Ce(III) and Ce(IV). Quantitative analysis showed
high-resolution (HR) TEM (panels F and G) images of CuO nanopar- 78.3% root Ce was present as C ­ eO2, while 21.7% was from carbox-
ticles exposed A. thaliana roots after 10 days of exposure. Panels G ylates of Ce as a fraction of applied ­CeO2 nanoparticles underwent
and F are magnified pictures of deposit G (high electron dense depos- plant-mediated transformation. Adapted with permission from (Cui
its) and F (loosely dispersed flocci). Fast Fourier transform (FFT) et al. 2014). Panel I depicts plant mediated transformation of nano-
analysis (inset) was done of the regions indicated in white rectangles. particles under the influence of plant secretion and the internal envi-
Interplanar crystal spacing data from FFT confirm the signal (-111) ronment of plants
for CuO and signals (111) and (220) for CuCl. Regions encircled in

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Environmental Chemistry Letters (2021) 19:1545–1609 1557

to plants (Schwabe et al. 2015). Moreover, the other factors nanoparticles also accumulate in fruits with help of phloem.
like the use of coating materials, size of nanoparticles, and As an example, tomato plants-accumulated cerium dioxide
homo/hetero-aggregation are also crucial in determining the ­(CeO2) nanoparticles in not only shoots, but also a frac-
bioavailability of nanoparticles and hence should be moni- tion of it was stored in tomato fruits (Wang et al. 2012c).
tored cautiously (Zhang et al. 2015; Máté et al. 2016). This suggests that nanoparticles with specific size are able
Furthermore, proteins, humic acids, fulvic acids, and to cross and travel in phloem tissues, the only channel enter-
polysaccharides are also responsible for the surface adsorp- ing fruit tissues. In yet other experiments, soybean raised
tion of nanoparticles and their intracellular uptake (Khan with metal and metal–oxide nanoparticles in hydroponic
et al. 2015; Amde et al. 2017). In a study, Lv et al. reported solution had nanoparticles accumulated in roots, nodules,
the presence of ZnO nanoparticles within the roots of maize stems, and pods (Priester et al. 2012, 2017). However, dif-
plants; however, ZnO nanoparticles were not detected in ferent nanoparticles behave differently in plant system and
maize shoots possibly due to dissolution of ZnO nanopar- most of them are largely accumulated in plant root tissues.
ticles in plant tissues and hence showed their differential For instance, ­CeO2 nanoparticles were found deposited in
availability to various plant parts (Lv et al. 2015). It has root system of three cereal plants, rice, barley, and wheat
been established that nanoparticles are easily bioavailable without showing any visible change in germination and elon-
to plants after dissolution. For instance, ZnO nanoparticles gation of roots (Zhao et al. 2012b; Rico et al. 2015b); how-
are reported to become frequently bioavailable primarily in ever, some molecular changes were observed in rice plants
its ionic or dissolved form which is indicative of rapid dis- (Rico et al. 2013b). Similar kind of impact of corn roots was
solution of ZnO nanoparticles (Du et al. 2011). Further, it exerted on fluorescently labeled ZnO nanoparticles, where
has been reported that ZnO nanoparticles–wheat interactions ZnO nanoparticles were just deposited in root’s stele with nil
result in Zn–phosphate accumulation in shoots which could transportation to upper ground organs (Zhao et al. 2012b).
be due to dissolution of ZnO nanoparticles and internali- However, Cu nanoparticles when internalized in root tissues
zation of ­Zn2+ ions (Dimkpa et al. 2013). Similarly, equal of cucumber plant as higher as 10–20-fold over untreated
bioavailability of Z­ n2+ dissolved from ZnO nanoparticles control inhibited the root expansion (Arif et al. 2018).
and zinc chloride ­(ZnCl2) to cowpea plants further sup-
ported the role of dissolution in the uptake of nanoparticles
(Wang et al. 2013a). Identical results were also obtained Mechanisms of nanoparticle uptake
with Solanum lycopersicon, Zea mays (Lv et al. 2015), Pha- by plants
seolus vulgaris (García-Gómez et al. 2017), Glycine max
(Hernandez-Viezcas et al. 2013), and Prosopis juliflora-velu- When taken up from external environment into plant tis-
tina (Hernandez-Viezcas et al. 2011) plants. In a study, not sues, nanoparticles can penetrate plant cells through various
the ZnO nanoparticles, but modified Zn forms resembling mechanisms including (i) ion channel transport, (ii) passive
Zn–citrate and Zn–phosphate were observed indicating the transport, (iii) transport along with water molecules by aqua-
transformation of ZnO nanoparticles (Hernandez-Viezcas porins, (iv) with the help of carrier proteins, (v) endocy-
et al. 2013; Lv et al. 2015). tosis, (vi) by creating new pores, and (vii) by associating
with organic matter (Hillaireau 2016; Jha and Pudake 2016;
Yanga et al. 2017). Among crops where maximum uptake,
Accumulation and deposition accumulation and toxicity of nanoparticles have been
of nanoparticles at subcellular sites reported include onion (Rajeshwari et al. 2015), wheat (Gao
et al. 2018), cucumber (García-Gómez et al. 2018b), tomato
Once internalized in the plant system, nanoparticles either (Raliya et al. 2015), zucchini/pumpkin (De La Torre Roche
accumulate at various sub-cellular locations like cellular et al. 2018), soybean (Rezaei et al. 2015), lettuce (Margenot
membranes, walls, tonoplast, vacuoles, endodermis, peri- et al. 2018), and rice (Da Costa and Sharma 2016). Of these,
cycle, cortex, cytoplasm, mitochondria, chloroplast, and cucumber and zucchini/pumpkin are considered preferred
nucleus or travel to various plants organs, for example, crops for evaluating the uptake and translocation of nanopar-
stem nodes, foliage, flowers, and fruits (Yanga et al. 2017; ticles due largely to higher water uptake by these plants and
Rajput et al. 2018b). In general, though the accumulation comparatively larger sized vascular bundles (Baas 2006).
of nanoparticles occurs at various sites (Fig. 8) (Lv et al. Here, the routes/modes through which nanoparticles can
2019), vascular bundle among plant tissues serves an impor- enter plant systems are briefly discussed.
tant role in nanoparticle transportation through plant organs
(Fig. 9) (Pradas Del Real et al. 2017). Once nanoparticles
reach the vascular system or tissues like xylem, their move-
ment toward aerial parts of the plant becomes rapid. The

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1558 Environmental Chemistry Letters (2021) 19:1545–1609

Fig. 8  Bioaccumulation and A C D

subcellular deposition of
nanoparticles (NPs): micropho-
tograph of split-root exposure
hydroponic system (a). Treated
side (TS) and blank side (BS)
CeO2-NPs
indicate the treated (with ­CeO2
nanoparticles) and blank side
of cucumber roots, respectively.
Adapted with permission from
reference (Ma et al. 2017).
Treatment of Cucurbita maxima
seedlings with iron oxide B
nanoparticles in the hydroponic E F
system (b). Adapted with per-
mission from reference (Li et al.
2018a). Panels C–F show the
presence of ­CeO2 nanoparticles
(2000 mg ­L−1) at various sites
of cucumber roots as analyzed
by TEM: root surface of treated
side (c), internal structure of Fe2 O3
treated side root (D), and root γ-Fe2 O 3 NPs NPs
surface of blank sized (e, f).
α-Fe2 O 3 NPs Fe
3+

Inset pictures in panels C–F

represent greater magnifica-
tion of selected regions (scale G H I
bar = 200 nm for each inset).
Panels G-K represent TEM
micrographs of C. maxima
ultrathin root sections as control
(g), roots treated with 50 mg
­L−1 each of γ-Fe2O3 nanopar-
ticles (h, i), α-Fe2O3 nanopar-
ticles (j, k), and bare ­Fe3O4
nanoparticles (l) for 10 days

J K L

Root‑mediated uptake of nanoparticles nanoparticles by plant root cells have been reported (Li et al.
2016; Raliya et al. 2016a; Vithanage et al. 2017; Ahmed
Roots are in direct contact with nanoparticles and hence et al. 2018b). The transpiration may facilitate the uptake of
can absorb nanoparticles from soils and transport them to nanoparticles (Zhai et al. 2014) with positive correlation
various plant tissues. This uptake is facilitated by perme- between rate of water absorbed and nanoparticle’s uptake
able and more thinner cuticle of roots and cell wall of root (Rico et al. 2013a). For instance, along with water uptake
hairs (Galway 2006). Uptake and accumulation of various through the xylem, the CuO nanoparticles also travel from

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Environmental Chemistry Letters (2021) 19:1545–1609 1559

Fig. 9  Examples of distribution of nanoparticles in plants. Panels untreated (e), treated with 75 mg ­L−1 each of ­CuCl2 (f) and CuO
A-D show Ag nanoparticle’s distribution in wheat roots. Tricolor nanoparticles (NPs) (g). Fluorescence of lignin present in periderm
maps of wheat root captured through micro-X-ray fluorescence is shown (e) where arrows point the cellular structure of cortex and
(μ-XRF) technique (a), cross section of root (b), a magnified picture periderm, while opaque region represents cortex only. The inset pic-
of endodermis (c), and cortex (d). Arrows in red indicate preferential ture in panel F corresponds to aqueous solution of ­CuCl2 showing no
deposition locations of Ag nanoparticles, while white arrows indicate fluorescence. However, panel G indicates lignin fluorescence in peri-
the points of root tissues where μ-XANES analysis was performed. derm. Yellow rectangle in panel G confirms the fluorescence of CuO
Abbreviations Ep, Cx, Ed, Pe, and Xy stand for epidermis, cortex, nanoparticles present in the cortex which is also visible in aqueous
endodermis, pericycle, and xylem, respectively. Adapted with per- suspension of CuO nanoparticles in inset of panel G. Adapted with
mission from reference (Pradas Del Real et al. 2017). Panels E–G permission from reference (Bonilla-Bird et al. 2018)
represent the two-photon microscopic analysis of sweet potato roots:

roots to shoot of maize (a cereal crop) as viewed under TEM influences nanoparticle’s internalization. As an example, the
and energy-dispersive X-ray (EDX) of xylem sap (Fig. 10) pore diameter (6.6 nm) of maize primary roots selectively
(Wang et al. 2012c). Furthermore, root pore size also allows the uptake of smaller sized ­CeO2 nanoparticles in root

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1560 Environmental Chemistry Letters (2021) 19:1545–1609

Fig. 10  Uptake of CuO nanoparticles (NPs) by maize plants and its internalized CuO nanoparticles in intracellular spaces and within the
visualization by TEM after 15 days of growth in hydroponic nutri- cortical cells of maize root. Panels E and F are enlarged views of
ent solution. Magnified view of panel A shows transverse cut in encircled and squared area shown in panel C. Panel G reveals trans-
maize stem with xylem sap coming of it. TEM analysis of xylem location of CuO nanoparticles across cell wall of epidermis, and the
sap revealed the presence of CuO nanoparticles aggregates being presence of CuO nanoparticles like aggregates at the interface of
transported through xylem vessels. Panels B and C represent CuO cell membrane and cell wall. In addition, the endocytosis-like struc-
nanoparticles entrapped in epidermal cell walls, while panel C is the ture was observed in the cells (H, I). Adapted with permission from
magnified view of square drawn in panel B. Panels D, E, and F show (Wang et al. 2012c)

cells with subsequent transmission to aerial parts (Zhao et al. nanoparticle’s uptake varies between cereal and vegetable
2012a). On the other hand, ­CeO2 nanoparticles of > 7 nm in crops and even among vegetable crops based on nanoparti-
diameter can be taken up by other crops including alfalfa, cle’s and root pore diameter. Also, nanoparticles with size
tomato, cucumber, and corn (López-Moreno et al. 2010). greater than those mentioned above have been found to flow
The ­CeO2 nanoparticles having a diameter of more than in the epidermal cells, across the cortex, and vascular system
seven nm up to 25 nm are taken up by cucumber roots and (Aubert et al. 2012).
travel to its shoots. These studies suggest that the mode of

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Environmental Chemistry Letters (2021) 19:1545–1609 1561

Foliar uptake In an experiment, leaf pore size in three dicot plants has
been reported to be more than 100 nm based on the uptake
Foliar application has been found useful in understanding efficiency of C­ 13 and N­ 15 (Eichert and Goldbach 2008).
the mode of uptake and distribution of nanoparticles from Sometimes, the stomata are clogged during the uptake of
leaves to shoot and then to belowground regions, and hence, individual nanoparticles or nano-sized aggregates (Hussain
the toxicity of nanoparticles on plants is resulted (Fig. 11). et al. 2013) resulting in reduced rate of water transpiration
Engineered nanoparticles, similar to those of naturally and elevation in foliage temperature ultimately retarding the
occurring atmospheric particles, are in direct surface con- production of photosynthetic pigments (Hirano et al. 1990).
tact with exposed organs like (i) stomatal apertures, (ii) To validate this, an experiment was conducted, where an
leaf hydathodes, and (iii) trichomes (Fig. 11). Nanoparti- aerosol-based spray of ­TiO2 and ZnO nanoparticles at the
cles, when applied foliarly as suspension or aerosol-based concentration range of 0–1000 mg kg−1 on 14 days grown
spray, are deposited on foliar surfaces and able to directly tomato plants. The plant height was increased by both nano-
penetrate inside the plant system largely due to nanoscale particles up to 250 mg kg−1. Of the two nanoparticles, the
size and along with gaseous uptake by plants (Wang et al. ­TiO2 significantly toxified tomato roots at all test concen-
2013b). During foliar applications, nanoparticles with an trations except 1000 mg kg−1 (Raliya et al. 2015). Besides
average size of approximately < 100 nm can easily be taken stomata, nanoparticles can also be taken up or excreted
up through stomatal openings typically ~ 100 nm in size with the help of leaf tip hydathodes (Hong et al. 2014) more
(Schwabe et al. 2015). effectively after guttation when small droplets of water are
If the nanoparticles have a coating of polar material, hooked on leaf (Huang 1986). In a study, the inside entry
then their uptake is highly likely due to enhanced perme- of insoluble radioactive 141CeO2 nanoparticles through
ability of stomata for polar substances (Schreiber 2005).

Leaf ssue
NPs
H2O, O2
CO2 Stomata
NPs
NPs

Long distance transloca
on

Companion
cell

Sieve plate

Lower
epidermis

Spongy
mesophyll
Phloem vein
Xylem vein
Upper epidermis

Phloem Xylem

Root ssue

Fig. 11  Major sites (root and leaf) of nanoparticles (NPs) access to (black arrows). Blue arrow in xylem vessel indicates long distance
intracellular environment of plants and subsequent translocation to transport of nanoparticles to aerial parts. Small black arrows in root
various sites. Two types of nanoparticle’s movement are depicted: cell walls are showing the movement of nanoparticles from one cell
(i) apoplastic movement (red arrows) and (ii) symplastic movement to another via plasmodesmata

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1562 Environmental Chemistry Letters (2021) 19:1545–1609

141
hydathodes of cucumber plants was observed as Ce of hydro-minerals and nutrients carrying more nanoparticles
(Zhang et al. 2011). inside the plant (Castiglione et al. 2011).
In some cases, even the larger sized nanoparticles, for
example, ZnO nanoparticles > 40 nm, have, however, also
Role of plant cell wall and membrane in root been found to increase root cell permeability by forming
or foliar uptake variable sized holes (Lin and Xing 2008). This mode of
nanoparticle’s uptake is unlike the assumption of restricted
The cell wall-mediated uptake of nanoparticles generally size (only ≤ 20 nm) entry of nanoparticles through cell walls
depends both on (i) nanoparticle’s diameter and (ii) cell wall (Ma et al. 2010). In yet other experiment assessing the cell
structure—thickness of cell wall (which varies from 100 nm wall dependency of nanoparticle’s uptake, it was revealed
to several µm), pore size, and biochemical composition (cel- that zero-valent iron nanoparticles can enhance the loosen-
lulose, hemicellulose, and pectin) (Glenn et al. 2012; Bid- ing of cell wall in radical-induced manner (Kim et al. 2014).
hendi and Geitmann 2016; Kumar et al. 2018). The pore size This occurred in two steps: (i) enhanced hydrogen peroxide
of the cell walls mostly remains constant acting as a selective level due to strong oxidizing potential of zero-valent iron
barrier for nanoparticles. Research has revealed the dyna- nanoparticles followed by (ii) hydroxyl radical formation,
micity in porosity of pectin (a component of cell wall) due to which induced loosening of A. thaliana root cell wall by
structural heterogeneity of cell wall (Willats et al. 2001; Fry creating asymmetrical distribution of tensional strength due
2011). A study revealed the spaces in hemicellulose struc- to hydroxyl radicals. It also stimulated endocytosis-medi-
ture of an average size of ~ 100 nm (McCann et al. 1990). ated uptake of nanoparticles. In contrast to ionic counter-
Due to this, nanoparticles of approximately 50 nm traversed part ­(Zn2+), ZnO nanoparticles also induced endocytosis in
across and along the cell wall with consequent internaliza- roots of A. thaliana grown on agar-based medium contain-
tion in cell matrix (Lee et al. 2008). Similarly, nanoparti- ing ½ strength MS medium (Wan et al. 2019). To confirm
cles ranging between 5 and 20 nm were also able to cross this, actin-binding domain 2 (ABD2)/GFP transgenic line
the plant cell wall (Navarro et al. 2008; Ma et al. 2010). was used. ZnO nanoparticles caused actin microfilament
For instance, the uptake and movement of Au nanoparticles rearrangement in epidermal cells of root elongation zone
with ≤ 20 nm have been confirmed in watermelon plants repressing the growth of primary roots (Fig. 12).
(Raliya et al. 2016a). Moreover, the smaller sized nanopar- Following penetration, nanoparticles can move across the
ticles encourage creation of new pores in cell envelope due cellular membrane through various mechanisms as depicted
to higher surface reactivity which perhaps enhances influx in Fig. 13. The cell membrane due to its polar nature acts as

An epidermal cell of root transion zone

Acn

Intermediate filament

Microtubule

ZnO-NPs ZnO-NPs induces changes

in acn microfilament
modulate endocytosis

Changed organizaon
and orientaon of
microfilaments

Fig. 12  a Endocytosis of ZnO nanoparticles (NPs) in root cells of A. filaments of epidermal cells. Emission of green fluorescent protein
thaliana. Five-day-old seedlings were exposed to (i) ZnO nanoparti- (GFP) from the roots of ABD2::ABD2-GFP seedlings of A. thaliana
cles for 6 h or 3 days at 100 mg L ­ −1, (ii) Z
­ n2+ for 3 days at 200 mg exposed for three days to 200 and 100 mg ­L−1 of ­Zn2+ and ZnO nano-
­L−1, and (iii) brefeldin A for 3 h at 25 μM and then stained with red particles, respectively. Animation shows rearrangement of micro-
fluorescence emitting FM4-64 fluorescent dye. b ZnO nanoparticles filaments under ZnO nanoparticle stress. Adapted and recreated with
rearranged microfilaments such as actin, microtubules, and other permission from (Wan et al. 2019)

13
Environmental Chemistry Letters (2021) 19:1545–1609 1563

transformaon
NPs ions Key
Physical clogging
of cell wall pore Integral protein

Peripheral protein

Carrier protein
Ion
New pore channel Low Aquaporin
formaon Facilitated transport transpiraon
entry Cell membrane receptor
Endocytosis

NP bound with organic ma†er

Passive
diffusion Bare nanoparcle

~70-120 nm
Coated nanoparcle
Nanotubes

Plasma Clathrin molecule

Concentraon membrane
gradient Cell wall Ion channel

Plasmodesmata
Desmotubule Widest point Cell 1 Clathrin coated vesicle
~ 40-60 nm
containing nanomaterial
Neck region
Apoplasc ~ 20-40 nm Cell 2
Symplasc
movement
movement
Smooth ER

Fig. 13  A model of nanoparticles (NPs) entry into plant cell, across organic matter, passive diffusion, and through new pore formation by
the plant cell wall and membrane followed by their apoplastic and carbon nanotubes or surface reactivity of smaller size nanoparticles.
symplastic movement. Nanoparticles are taken up by facilitated trans- During the process of cellular uptake, nanoparticles may clog the cell
port of coated nanoparticles, ion channel transport (after dissolution wall’s pores and aquaporins present in membrane
of nanoparticles), through endocytosis of nanoparticles bound to

a selective channel for the across movement of solutes and of lipid bilayer entrapping the surface adsorbed nanoparticle
substances. As per the surface and morphological features followed by its dissociation but inside the cell by tightly
of nanoparticles, the cell membrane can regulate the inside controlled cell signals (Karami Mehrian and De Lima 2016).
passage of nanoparticles by facilitated uptake or passive dif- The endocytosis may occur as receptor independent or
fusion. The entry passage of nanoparticles in cells critically dependent (Schwabe et al. 2015). In the latter one, nanopar-
depends on many physicochemical and physiological factors ticles first adsorbed to a membrane bound macromolecule,
including: (i) nanoparticle-dependent factors such as chemi- which could be a carbohydrate, protein, or lipid followed
cal composition, size, morphology, surface charge, hydro- by cellular internalization of the formed vesicle (Karami
phobicity, or hydrophilicity and (ii) membrane-dependent Mehrian and De Lima 2016). Charge nanoparticles are taken
factors like composition of lipids, fluidity of cell membrane, up via a clathrin-dependent and receptor-mediated endocy-
and the presence of molecular species and membrane- tosis (Onelli et al. 2008). Clathrin molecules are cellular
embedded ligands (Karami Mehrian and De Lima 2016). coat proteins producing endocytic vesicles of size ranging
Selectively permeable channel proteins limit the influx between 70 and 120 nm (Robinson 2015; Faisal et al. 2018).
of polar and large molecules such as ions dissolved from This size of vesicles may therefore limit the entry of bigger
nanoparticles or polar, negative, or positive nanoparticles sized nanoparticles into the vesicle such as carbon nanotubes
(Schwabe et al. 2015). (Fig. 14).
The nanoparticles are also taken up while entrapped in For the uptake of carbon nanotubes through cell mem-
endocytic vesicles, which can be of two types either depend- branes, a non-specific mode of uptake has been proposed
ent of endocytosis or independent of endocytosis (Fig. 14). (Liu et al. 2009b). Endocytosis can differentiate nanoparti-
Endocytosis is a natural process that allows communica- cles based on their charge; for example, positively charged
tion among cells, helps in cellular signaling and nutrient Au nanoparticles are internalized in plant cells through
transfer, and induces defense response against xenobiotics. nonspecific fluid phase endocytosis more effectively than
The very first event in the endocytosis in the invagination negatively charged Au nanoparticles (Onelli et al. 2008).

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1564 Environmental Chemistry Letters (2021) 19:1545–1609

Fig. 14  Uptake of nanoparticles Invaginaon of lipid

in plant cells through endocyto- bilayer
sis of clathrin-coated vesicles, Nanoparcles
uncoated vesicles, and receptor
independent vesicles. Lipid bilayer Nanotubes

Dissociaon of Cell surface receptors

(receptor dependent)
formed vesicle Non-specific receptor
independent endocytosis
Clathrin

Nucleus
Clathrin coated vesicle
(clathrin dependent
endocytosis)
Cytoplasm
Endocytosis dependent uptake

Enhanced uptake of nanoparticles may also alter the gene in phloem vessels (Zangi and Filella 2012). In symplastic
expression for aquaporin channels (Rico et al. 2011) of movement, microscopic channels called plasmodesmata are
cell membrane in an inversely proportional manner, i.e., key because it is the only connection adjoining two plant
higher uptake of nanoparticles clogs the aquaporins, and cells regulating the transfer of different molecules and nano-
in response, cell starts to down-regulated the expression of particles from one cell to another across the plant (Corredor
aquaporin genes (Lü et al. 2010; Taylor et al. 2014). Aqua- et al. 2009). The apoplastic route is more preferred due to
porins also serve as non-selective passage for the uptake of the fact that it is a non-selective passage of least resistance,
non-ionic solutes or substances less than one nanometer in thereby translocating many non-essential metal complexes
size (Zangi and Filella 2012) and assist to switch over the and nutrients (Sattelmacher and Horst 2007). If there is any
symplastic or apoplastic movement (Schwabe et al. 2015). blockage of apoplastic way due to the presence of caspar-
ian strip, nanoparticles choose to traverse the protoplast of
endodermal cells and gain access to vascular tissues (Lin and
In Planta translocation of nanoparticles Xing 2008) as nanoparticles have been detected in xylem
vessels (Zhang and Zhang 2020).
Translocation of nanoparticles from one organ to other parts In a recent study, when A. thaliana was treated with dif-
of plant occurs via xylem and phloem tissues. However, ferentially charged (positive and negative) Au nanoparticles,
translocation differs from nanoparticle to nanoparticle. For two different modes of nanoparticles uptake and translo-
example, ­TiO2 nanoparticles in cucumber roots are translo- cation were detected based on the charge on nanoparticle
cated to leaves and fruits without their bioconversion (Servin surface (Avellan et al. 2017). The data recorded through
et al. 2012). In contrast, nano-ceria is first dissolved and then two highly sophisticated microscopy techniques: (i) X-ray
liberate cerium ions which then interacts with plant organics computed nanotomography (nano-CT) and (ii) dark-field
inside the plant system (Gui et al. 2015). The translocation microscopy combined with hyperspectral imaging (DF-
of nanoparticles is generally dependent of four factors: (i) HSI), revealed that the detachment of border-like cells from
size of nanoparticle, (ii) surface chemistry and charge, (iii) root cap and secreted mucilage could adsorb and entrap the
growth phase of plant, and (iv) inside environment of plant Au nanoparticles regardless of their surface charge. In con-
cell. Broadly, the nanoparticles translocation occurs through trast, the behavior of root cap border cells toward Au nano-
symplastic or apoplastic pathways as depicted in Fig. 13. In particles depends on particle charge. Positively charged Au
the apoplastic pathway, the nanoparticles move either by nanoparticles enhanced the secretion of mucilage and sub-
one of the following ways or simultaneously via longitudinal sequently are trapped in it, which in turn prevents their accu-
channels in cell wall, intercellular spaces, and xylem vessels mulation and transposition in root tissue. On the other hand,
(Sattelmacher et al. 1998; Geisler-Lee et al. 2013); how- negatively charged Au nanoparticles bypassing the mucilage
ever, when travelling symplastically, nanoparticles cross cell adsorption could get entered the root tissue and were trans-
membrane reaching to next adjacent cell through plasmodes- located in apoplast (Fig. 15a). In a different study, C ­ eO2
mata (Figs. 10 and 13) or move via sieve tissues present nanoparticles when applied on leaves of Cucumis sativus,

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Environmental Chemistry Letters (2021) 19:1545–1609 1565

approximately 3% of the total amount of nanoparticles was to only 5.45% fraction of low soluble ­TiO2 nanoparticles
found in roots suggesting that the nanoparticles were trans- (Wang et al. 2013b). However, T ­ iO2 nanoparticles with low
located from leaf to root via phloem (Hong et al. 2014) with solubility were able to penetrate leaves and translocated to
subsequent adsorption of up to 81% of C ­ eO2 nanoparticles vascular supply and roots (Larue et al. 2014). In a hydro-
on outer surface of leaf. Numerous studies have shown that ponic nutrient solution, soybean plants accumulated and
nanoparticles can travel through plant cell walls and are distributed nanoparticles of Zn/ZnO and ­CeO2, and their
localized within cell organelles or cytosol. For instance, the corresponding metal ions in various tissues (López-Moreno
presence of T­ iO2 nanoparticles was observed using EDX et al. 2010). However, a distinctive mode of translocation
on the rice chloroplast membrane when treated with 1000 of ZnO and C ­ eO2 nanoparticles has been suggested, where
­mgTiO2 nanoparticles ­L−1 (Ji et al. 2017). In a study, ­TiO2 ­CeO2 nanoparticles remained bio-accumulated in root nod-
nanoparticles were translocated to leaf trichomes and fruits ules causing a substantial reduction in ­N2 fixation, while
of cucumber as reveled by micro-X-ray near edge spectros- ZnO nanoparticles were able to pierce into leaves and beans
copy (µ-XANES) analysis of cucumber tissues (Servin et al. (Priester et al. 2012). In a recent study, ZnO nanoparticles
2012, 2013). In a similar study, C ­ eO2 nanoparticles have and ­ZnSO4 were foliarly applied on the winter wheat under
also been detected in vacuole, chloroplast, and plasma mem- field conditions and after the growth, analysis of grain by
brane of cotton plants grown under hydroponic environment µ-XRF microscopy and XANES showed that ZnO transloca-
(Nhan et al. 2015). tion somewhat increased the zinc content of grain endosperm
Among various factors, the solubility of nanoparticles (Zhang et al. 2018a). Zinc was also distributed in the crease
profoundly affects their translocation; for example, up to of grain and aleurone layer (Fig. 15b, c). Besides these, the
26.14% of total applied concentration of highly soluble MgO translocation of nanoparticles also varies with growth con-
nanoparticles was translocated from leaf to root compared ditions. To prove this, studies on copper-based nanoparticle

Fig. 15  Panel A shows trans-

location of Au nanoparticles
(NPs) in A. thaliana roots
detected through: (i) Nano-CT
and (ii) DF-HSI. Negatively
(−) or positively (+) charged
Au nanoparticles were stabi-
lized by polyethylenimine or
citrate coating. Adapted with
permission from (Avellan et al.
2017). Panel B shows a section
of wheat grain under light
microscopy which were picked
from foliarly applied ZnO
nanoparticles exposed wheat
plants. Examination of zinc
distribution in grain section by
synchrotron X-ray fluorescence
microscopy: panel CK, FZnO,
and FZn represent control, treat-
ment of ZnO nanoparticles, and
zinc sulfate, respectively, while
panel C shows XANES spectra
of control and each test Zn
species. The vertical dotted line
in panel C corresponds to 9.671
keV for ZnO (9.671 keV) which
confirms the translocation of
ZnO nanoparticles to wheat
grain. Adapted with permission
from (Zhang et al. 2018a)

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1566 Environmental Chemistry Letters (2021) 19:1545–1609

and plant interactions are discussed as an example. When of nanoparticles in the environment and their interactions
nano-forms of three copper materials, namely Cu, CuO, and with plants induce toxicity (Fig. 16). Irrespective of the
Cu(OH)2, were tested on cilantro, lettuce, and alfalfa, copper routes, bioaccumulation, transport, and effects of nanopar-
was mostly found accumulated in roots approximately more ticles on plant’s performance depend upon three factors: (A)
than 87% with some translocation to stem but not to leaves [Plants]—(i) genotypes, (ii) growth stage, and (iii) physi-
(Hong et al. 2015; Zuverza-Mena et al. 2015). However, ological and metabolic activities; (B) [Nanoparticles] (i) size
copper from Cu nanoparticles translocated to only to stems and shape, (ii) surface functionalization and chemical com-
leaves but also accumulated in fruits of tomato and cucum- position, (iii) stability of nanoparticles, and (iv) duration of
ber raised in soil (Zhang et al. 2016a; Rajput et al. 2018c). exposure; and (C) [Soils] (i) physicochemical properties and
In one of our previous studies on comparative analysis of (ii) microbiological composition (Rico et al. 2011; Raliya
CuO nanoparticle translocation in hydroponically and soil et al. 2015; Carrière and Larue 2016; Zhao et al. 2016a;
grown tomato plants, the CuO nanoparticles translocated to Gao et al. 2018). The lethality of nanoparticles (Table 1) on
every plant organ but uptake were low in soil raised plants different growth stages/physiological processes of numer-
as compared to hydroponic culture (Ahmed et al. 2018a). ous plant species is reviewed and discussed briefly in the
The limited internalization and hence translocation of CuO following sections.
nanoparticles could be due to the above discussed hetero-
aggregation of nanoparticles which is more common in soil Seed germination and growth of seedlings
system. under nanoparticle stress

Phytotoxic impact of nanoparticles Nano-phytotoxic impacts on plants starting from seed ger-
mination and on both seedling (Kasana et al. 2017) and adult
Prolong persistence, low biodegradability, and massive stage have been studied (Chichiriccò and Poma 2015). Of
increase in environmental deposition of nanoparticles built these, seed germination, considered an important process of
additional survival pressure on edible crops. The prevalence plant (Bewley 1997), is tightly regulated and a well-protected

Fig. 16  Toxic impacts of nanoparticles on the plant through reactive eration, chromosomal anomalies, and altering miRNA gene expres-
oxygen species production, membrane lipid peroxidation, destruc- sion (Box-III). Disruptive impacts of nanoparticles on plants include
tion of chloroplasts, and mitochondria (Box-I). Intracellular oxidative reduced biomass and water transpiration with up-regulation of heat
stress causes imbalance in antioxidant enzymes such as superoxide shock proteins (Box-IV). Nanoparticle interaction with plant cells
dismutase (SOD), catalase (CAT), and peroxidase (POD) (Box-II); results in apoptosis, necrosis, and overall change in proteome and
interaction of nanoparticles with genetic material of plant cells causes metabolome (Box-V), and oxidative stress, which ultimately lead to
genotoxicity via disruption of normal cell cycle, micronuclei gen- plant cell death

13
 Table 1  Toxic responses of nanoparticles to agriculturally important plants
Nanoparticle Size (nm) Test crop(s) Dose rate Activity/toxicity References

Ag 10 Lycopersicon esculentum 10–50 mg kg−1 Ag nanoparticles’ uptake induced reactive oxi- Das et al. (2018)
dative stress that reduced photosynthesis, C­ O2
assimilation and fruit yield
10 Allium cepa, Raphanus sativus 0.001–10,000 mg ­L−1 Root growth was inhibited Pittol et al. (2017)
17 Triticum aestivum 20–60 ppm Generation of oxidative stress was evident, Barbasz et al. (2016)
antioxidants’ level was enhanced, and Ag
nanoparticles induced cell deformation
20 Vigna radiata 5–50 mg ­L−1 Ag nanoparticles induced formation of reactive Nair and Chung (2015)
oxygen species and reduced overall yield
20, 51, 73 Vicia faba 100 mg ­L−1 Ag nanoparticles induced excessive production Falco et al. (2020)
of oxidative stress, reduced C
­ O2 assimilation
and stomatal conductance, inhibitory impact
Ag nanoparticles increased with increasing
Environmental Chemistry Letters (2021) 19:1545–1609

diameter
CuO 20–100 Lactuca sativa, Brassica oleracea var. sabel- 34.4 g/m2 on leaf surface Foliar application: highest amounts of CuO Keller et al. (2018)
lica and B. oleracea var. viridis nanoparticles were accumulated on lettuce
leaf surface followed by collard green and kale
16 L. sativa, Daucus carota 0.8–798.9 mg ­L−1 Water transport and growth assessment was Margenot et al. (2018)
done following 10 days of growth. Dose
related increase in root diameter of lettuce by
52% and carrot by 26% seedlings relative to
control
40–80 Zea mays, Oryza sativa 500, 1000, 2000 mg L
­ −1 At 2000 mg L ­ −1, 95% and 97% inhibition in Yang et al. (2015)
root length of maize and rice
10–100 Coriandrum sativum 0–80 mg kg−1 soil Nanoparticle solutions were mixed with com- Zuverza-Mena et al. (2015)
mercial potting mix. Cu accumulation caused
approximately 50% inhibition of germination,
depression in micro and macro nutrient ele-
ment accumulation
38 T. aestivum 500 mg kg−1 Fresh and aged mixture of CuO nanoparticles Gao et al. (2018)
and loamy sand soil were tested. Compro-
mised root growth and aged CuO nanoparti-
cles further aggravate the toxicity
25–55 B. rapa 50–500 mg ­L−1 Seedlings exposed to CuO nanoparticles for Chung et al. (2019b)
15 days in a growth room. Synthesis of pho-
tosynthetic pigments and sugar was decreased
with simultaneous enhancement in proline
level, generation of reactive oxygen spe-
cies, malondialdehyde, and H ­ 2O2; decreased
amount of glucosinolate and phenols

13
1567
 Table 1  (continued)
1568

Nanoparticle Size (nm) Test crop(s) Dose rate Activity/toxicity References

13
< 50 Hordeum vulgare 50–1000 mg kg−1 Soil–nanoparticle mixture of pH 4.8 and 5.8 Qiu and Smolders (2017)
before and after aging. Soil aging increased
CuO nanoparticles toxicity; root elongation
was suppressed
43 O. sativa 50–1000 mg kg−1 Low water uptake by root and aerial parts; grain Peng et al. (2017a)
production was considerably reduced
< 50 T. aestivum 3–300 mg kg−1 Reduction in root elongation and zone of cell Adams et al. (2017)
division was shortened
< 50 Cucumis sativus 50–200 mg ­L−1 Foliar application on soil grown plants. Inhibi- Hong et al. 2016)
tion of leaf transpiration, net photosynthesis,
reduction in fruit firmness and molybdenum
of fruits
25–55 D. carota 1–1000 mg ­L−1 Plants were treated in coarse sand mixed with Ebbs et al. (2016)
CuO nanoparticles for 13 weeks. The CuO
nanoparticles dose dependently decreased
plant biomass, Cu accumulation in taproot
was limited to the periderm, radial penetration
of Cu into the taproot, and subsequent translo-
cation to shoots was observed
< 50 O. sativa 2.5–1000 mg ­L−1 Accumulation of CuO nanoparticles in Da Costa and Sharma (2016)
chloroplast, reduced transpiration, stomatal
conductance, photosynthesis, enhanced activ-
ity of ascorbate peroxidase and superoxide
dismutase
40 T. aestivum Freshly added and 28 days Aging of CuO nanoparticles further reduced Gao et al. (2018)
aged CuO nanoparticles at root growth, wheat root system had some-
500 mg kg−1 soil what compensatory effects on nanoparticles
dissolution, plant activity enhanced the pH by
0.4 and 0.6 units by fresh and aged CuO nano-
particles, root exudates enhanced Cu content
in pore water
ZnO < 100 Pisum sativum, T. aestivum, Z. mays, R. sati- 20–900 mg kg−1 soil Accumulation and toxicity of ZnO nanoparticles García-Gómez et al. (2018c)
vus, L. sativa, Solanum lycopersicum, Beta varied with plant species; interaction of ZnO
vulgaris, and C. sativus nanoparticles with calcareous soil reduced
Zn availability and thus toxicity to biomass
accumulation by cucumber, beet, and wheat;
in acidic soil, pea, wheat, and maize showed
resistance
< 50 Glycine max 500 ppm Effect on seedlings was studied. Inhibition of Hossain et al. (2016)
root elongation, cell viability, and biomass,
generation of superoxides, reduced biomass of
foliage, alteration of gene expression
Environmental Chemistry Letters (2021) 19:1545–1609
 Table 1  (continued)
Nanoparticle Size (nm) Test crop(s) Dose rate Activity/toxicity References

90 Z. mays 400–32,000 mg kg−1 Plants were grown in soil for 56 days. Increased Wang et al. (2016a)
production of superoxide anions and super-
oxide dismutase activity decreased mineral
nutrient acquisition, decreased photosynthesis
and root activity, dose-dependent enhance-
ment in Zn bio-uptake
15 S. lycopersicon, T. aestivum 50–1600 mg ­L−1 Seed germination in Petri dishes; plants were Amooaghaie et al. (2017)
exposed in vermiculite receiving hydro-
ponic nutrient medium. Lower doses of ZnO
nanoparticles increased seed germination and
growth attributes, while higher doses showed
toxicity to germination, growth attributes,
photosynthetic pigments, enhanced bio-uptake
Environmental Chemistry Letters (2021) 19:1545–1609

of Zn, 200 mg ­L−1 concentration increased

hydrogen peroxide and malondialdehyde pro-
duction; overall, S. lycopersicon experienced
more toxicity than T. aestivum
10 G. max 0.05, 0.1, 0.5 g kg−1 soil Seed protein, chlorophyll, reactive oxygen Priester et al. (2017)
species, lipid peroxidation, genotoxicity were
taken as toxicity end points. Leaf damage,
genotoxicity appeared at 0.5 g kg−1
15 T. aestivum 100, 200 µM Hydroponic exposure to plants. Reduced photo- Tripathi et al. (2017)
synthesis, production of ­H2O2, lipid peroxida-
tion, nitric oxide ameliorated the toxicity
< 100 P. vulgaris, S 3, 20, 225 mg kg−1 Plants were raised with ZnO nanoparticles García-Gómez et al. (2017)
Lycopersicon at pH 5.4 and 8.3 in acidic and calcareous.
Reduced photosynthesis, enhanced oxidative
stress, reactive oxygen species generation,
higher toxicity were observed in acidic soil for
P. vulgaris and opposite for S. lycopersicon
30–40 Z. mays 0.02–2 g ­L−1 Petri dish assay to assess germination and Fellmann and Eichert (2017)
seedling growth. Negative effect on seed ger-
mination at 0.02 g L ­ −1 after 24 h; root length
increased after 68 h at 0.02 and 0.2 g L­ −1
< 100 S. lycopersicum 300, 600, 1000 mg kg−1 Plants were grown in soil for 90 days. Root Akanbi-Gada et al. (2019)
uptake of ZnO nanoparticles, generation of
­H2O2, and oxidative stress in leaves; enhanced
superoxide dismutase activity, total flavo-
noids, phenols, lycopene, and β-carotene were
significantly reduced
90 Z. mays 800 mg kg−1 Reduced growth and inhibition of arbuscular Wang et al. (2016a)
mycorrhiza fungi
10 Medicago sativa 250, 500, 750 mg kg−1 Reduced root biomass up to 80% Bandyopadhyay et al. (2015)

13
1569
 Table 1  (continued)
1570

Nanoparticle Size (nm) Test crop(s) Dose rate Activity/toxicity References

13
64 and 80 Vigna angularis 20–200 µg mL−1 ZnO nanoparticles readily accumulated in roots, Jahan et al. (2018)
disrupted plant physiology of plant, enhanced
oxidative stress, and reduced photosynthetic
pigment
TiO2 20 ± 5 O. sativa 50 and 200 mg L
­ −1 Reduced grain yield and biomass, enhanced Du et al. (2017a)
Mg, Ca, Zn, P, and Ti in grains
25 C. sativus, B. oleracea var. capitata, Avena 250–1000 mg ­L−1 Inhibition of root growth of oat, corn, cabbage, Andersen et al. (2016)
sativa, oat, lettuce, and reduction of soybean and
D. carota, Z. mays, cucumber germination
L. sativa, A. cepa,
Lolium perenne, S. lycopersicum
< 25 S. lycopersicum 100–1000 mg kg−1 Plants were raised in nanoparticles amended Raliya et al. (2015)
soil. Root elongation, plant height, and
biomass increased at 250 ­mgTiO2 nano-
particles ­kg−1, 100 ­mgTiO2 nanoparticles
­kg−1 enhanced the lycopene and fruit yield,
photosynthetic pigment increased up to
750 mg kg−1
5–15 Z. mays 0.02–2 g ­L−1 Inhibition of germination, root and shoot growth Fellmann and Eichert (2017)
8 Spirodela polyrrhiza 0.05–10 mg ­L−1 Exposure was given in specific nutrient solu- Movafeghi et al. (2018)
tion. Significant decrease in biological attrib-
utes, peroxidase activity, increased superoxide
dismutase activity
< 20 T. aestivum 20–100 mg kg−1 soil 60 days exposure in soil (sandy loam, pH 7.6). Rafique et al. (2018)
Root, shoot elongation and P uptake were
lower at 80 and 100 mg kg−1, 11.1% less
chlorophyll at 100 mg kg−1
20 O. sativa 100–500 mg ­L−1 Plants were exposed in hydroponics. Decreased Wu et al. (2017a)
production of glucose-6-PO42−, glucose-1-
­PO42−, Reduced biomass and altered antioxi-
dant defense, dose-dependent accumulation of
Ti in root and shoot
Environmental Chemistry Letters (2021) 19:1545–1609
 Table 1  (continued)
Nanoparticle Size (nm) Test crop(s) Dose rate Activity/toxicity References

Al2O3 13 Z. mays, O. sativa 2000 mg ­L−1 Roots were exposed in deionized water for Yang et al. (2015)
5 days (Z. mays) and 7 days (O. sativa). No
effect on seed germination; low phytotoxicity
of ­Al2O3 nanoparticles was observed in maize
only
< 50 Sinapis alba 10–1000 mg ­L−1 Effects on germinating seeds were observed. Landa et al. (2016)
At all concentrations, seed germination was
affected negatively
< 50 A. cepa, Z. mays 0.1, 1 and 10 g L
­ −1 Plants were cultivated in liquid nutrient media. Asztemborska et al. (2015)
Highest Al accumulation in roots; high-
est translocation factors were recorded for
Zea mays grown in liquid medium; results
suggested that ­Al2O3 nanoparticles sediment
Environmental Chemistry Letters (2021) 19:1545–1609

certainly but are available for bio-uptake

13 T. aestivum 5, 25, 50 mg mL−1 Time (24–96 h) and dose dependent effects Yanlk and Vardar (2015b)
were observed. Reduction in root elonga-
tion by 40.2%, 50.6%, and 54.5% at 5, 25,
50 mg mL−1 after 96 h; callose deposition,
lignin accumulation and cellular damage in
roots cortex, enhanced peroxidase, A ­ l2O3
nanoparticles induced DNA fragmentation
13 T. aestivum 5, 25, 50 mg mL−1 Effects on seedlings were observed for 96 h. Yanık and Vardar (2018)
Increased ­H2O2 content, superoxide dismutase
activity, lipid peroxidation; reduced produc-
tion of photosynthetic pigment and anthocya-
nin
α-Fe2O3, 30, 20 and 20 Citrus maxima 50 mg ­L−1 Nanoparticles were accumulated in plant roots; Li et al. (2018a)
γ-Fe2O3 and at 50 mg ­L−1, nanoparticles were still in Fe
­Fe3O4 deficiency state; chloroplast was very sensitive
to nanoparticles, enhanced ferric reductase
activity
Fe3O4 6 R. sativus, 0.67 mg mL−1 Inhibition of seed germination García et al. (2011)
C. sativus, Spinacia oleracea,
S. lycopersicon
Cr2O3 50 nm G. max 0.01, 0.05, 0.1 and 0.5 g L
­ −1 Reduction of 46.3% and 9.9% in biomass of root Li et al. (2018b)
and shoot, respectively, inhibition of photo-
synthesis, RUBISCO activity

13
1571
 1572 Environmental Chemistry Letters (2021) 19:1545–1609

stage against different stresses. However, soon after absorp-

tion (imbibition) of water and concurrent onset of vegeta-
tive developmental processes, they become sensitive to all
forms (physical, biotic and molecular) of stresses (Srivastava
Salehi et al. (2018)

2002). On the contrary, seeds have certain sensing mecha-

nisms, which enable them to germinate even under nanopar-
References

ticle stressed environment (Singh 2016). When exposed to

nanoparticles, germination and development of many edible
crops have been found to be adversely affected (Yan and
Stomatal morphology, photosynthesis, osmotic,

Chen 2019). As compared to germination, root growth is,

and redox balance were impaired; electrolyte
leakage increased with increasing concentra-

transport chain biochemical machinery and

however, more sensitive to contamination (Rees et al. 2016)

tions of nanoparticles and altered electron

and inhibition of root elongation is linked with alteration in

root architecture and morphology. As an example, ­Fe3O4
nanoparticles at 0.5–5 mg mL−1 reduce germination and
development of Cucumis sativus roots (Mushtaq 2011).
Similarly, Ag nanoparticles and ZnO nanoparticles signifi-
cantly inhibited seed germination and root development of
B. oleracea and Z. mays relative to corresponding free metal
photosynthesis
Activity/toxicity

species (Pokhrel and Dubey 2013). Other nanoparticles like

CuO, ZnO, ­Al2O3, and ­TiO2 considerably inhibited germi-
nation and seedling growth of radish, tomato, wheat, and
maize at the concentration range of 10–1000 mg L ­ −1 (Atha
−1
et al. 2012), 50–1600 mg ­L (Amooaghaie et al. 2017),
5–50 mg mL−1 (Yanlk and Vardar 2015a) and 0.02–2 g L ­ −1
(Fellmann and Eichert 2017), respectively.

Toxicity to cell envelope and intracellular oxidative

250–2000 mg ­L−1

stress
Dose rate

Plant cell wall is the first site that is exposed to nanoparti-

cles. The nanoparticles or their metal ions dissolved from
nanoparticles enter into the cell wall of root tissues forming
a complex with the –COOH groups of pectin (Jian et al.
2008). This binding may alter the symplastic or apoplastic
mode of solute transport across the cell wall and membrane
which leads to inhibition of root elongation (Horst et al.
2010). Moreover, the duration of exposure and metal con-
centration may also influence the cell wall rigidity (Kopittke
et al. 2008). In a study, Fe nanoparticles appeared to be
harmful to the plants and the majority of Fe nanoparticles
Phaseolus vulgaris

were found to be aggregated into cell walls of Capsicum

annum roots and then transported via apoplastic pathway
Test crop(s)

potentially blocking the transfer of iron nutrients (Yuan et al.

2018). The plasma membrane is yet another target to which
nanoparticles can bind and disrupt its physiological func-
tions (Contini et al. 2018).
10–30 nm
Size (nm)

Depending on chemical composition, size, and charge

of nanoparticles, the changes in membrane occur due to
Table 1  (continued)

absorption and permeation by nanoparticles leading even-

tually to complete disruption of membrane permeability
Nanoparticle

(Contini et al. 2018). Variation in physiological functions of

biological membranes due to stressor molecules often causes
CeO2

structural alterations in the composition of membrane lipids

13
Environmental Chemistry Letters (2021) 19:1545–1609 1573

and their peroxidation (Nasim and Dhir 2010; Meisrimler sharply. For example, higher production of malondialde-
et al. 2011). The uptake of nanoparticles begins with initial hyde by onion roots under ZnO nanoparticles and Z ­ n2+ ions
adhesion onto cells and subsequent interactions with cell amended hydroponic nutrient solution could be attributed
membrane stuff as described above. The internalization and to enhanced intracellular reactive oxygen species genera-
translocation are then followed in an energy driven mode tion leading to membrane lipid peroxidation and mitochon-
(Lesniak et al. 2013) ending sometimes in lysosomal accu- drial swelling (Kumari et al. 2011; Ahmed et al. 2017). In
mulation (Salvati et al. 2011). Variation in the local stabil- a study, even though the malondialdehyde was not detected
ity of membranes (Wang et al. 2011b), membrane fluidity in tissues of rice plants exposed to ­CeO2 nanoparticles at
(Liu et al. 2009b), disruption of electron transport chain 0–500 mg ­L−1, ions were leaked due to instability of cell
(Jhanzab et al. 2019), and dissipation of proton motive force membrane (Rico et al. 2013a). ­Fe3O4 nanoparticles induced
(Mirzajani et al. 2014) are some of the toxic consequences considerably high amount of membrane lipid peroxidation
of nanoparticles in plants. Among different nanoparticles, in seedlings of ryegrass and pumpkin as 248% and 210%,
­Fe3O4 nanoparticles, for example, when absorbed by pump- respectively, over control plants. Also, F
­ e3O4 nanoparticles
kin roots, caused local instability of the cell wall and/or blocked aquaporin channels inhibiting cellular respiration of
membrane and thus produced oxidative stress (Wang et al. roots linked to lipid peroxidation (Wang et al. 2011a). The
2011a). Whole rice plant metabolomic analysis by 2-DE reactive oxygen species as a prime cause of lipid peroxida-
and NanoLC/FT-ICR MS analysis after exposure with Ag tion induced by ­Al2O3, CuO, and ­Co3O4 nanoparticles has
nanoparticles revealed protein precursor accumulation which also been recorded in various tissues of tomato and rape
was indicative of membrane proton motive force dissipa- (Faisal et al. 2016; Ahmed et al. 2018a) (Fig. 17).
tion (Mirzajani et al. 2014). Further, gel-free/label-free pro-
teomic analysis of whole wheat plants under chemo-blended Impact on photosynthesis
Ag nanoparticles showed that proteins related to cell signal-
ing, cell wall, and electron transport chain were decreased Among other metabolic activities, photosynthesis is one
(Jhanzab et al. 2019). Among others, CuO nanoparticles also of the significant physiological process of plants which is
modify the lipid composition of wheat cell membranes in an negatively affected by nanoparticles (Fig. 16) (Jampílek
adverse manner (Sharma and Uttam 2017). and Kráľová 2019). The toxic nanoparticles attack dif-
Among stressors, metals have also been found to induce ferent photosynthetic apparatus (Sardoiwala et al. 2018),
the intracellular production of reactive oxygen species which leads to the following: (i) undesired deposition and
including hydrogen peroxide, hydroxyl, and superoxide distribution of nanoparticles leaf tissue such as mesophyll
radicals (Reddy et al. 2005; Hayyan et al. 2016). The over- (Xiong et al. 2017), (ii) altered membrane physiology of
production of reactive oxygen species due to add on pres- photosynthetic apparatus (Rajput et al. 2018a), (iii) reduc-
sure of nanoparticle is, however, common among edible crop tion in the formation of photosynthetic pigments (Rajput
plants, which further interact with many important plant bio- et al. 2019), (iv) variation in cytosolic enzymes and organics
molecules such as lipids, proteins, and cellular organelles. (Tighe-Neira et al. 2018), (v) changes in the functioning of
This reaction in turn induces membrane lipid peroxidation photosystem (Fig. 18). Among nanoparticles, CuO nano-
leading eventually to ion leakage, damage to photosynthetic particles have been reported to reduce chlorophyll content
apparatus, and consequently plant cell death (Sharma and in green gram (Gopalakrishnan Nair et al. 2014), field mus-
Dietz 2009; Das and Roychoudhury 2014) (Fig. 5). The tard (Chung et al. 2019a), and decreased net photosynthesis
enhanced peroxidation of membrane lipids can serve as a rate in cucumber (Hong et al. 2016) and rice (Da Costa and
biomarker for oxidative stress and also make changes in Sharma 2016).
physiological properties of membranes. Three major among Similarly, photosynthetic pigment content in cowpea
them are permeability, fluidity, and activity of membrane- (Jahan et al. 2018), maize (Wang et al. 2016a), tomato
bound ATPase (ATP synthase) (Shewfelt and Erickson (Amooaghaie et al. 2017), and wheat (Tripathi et al. 2017)
1991). Due to extremely short half-life, direct measurement was reduced by ZnO nanoparticles. Besides, nanoparticles
of reactive oxygen species is not feasible; however, other of ZnO, CuO, ­Al2O3 (Yanık and Vardar 2018) and ­TiO2
by-products produced as a result of reactive oxygen species (Rafique et al. 2018) also caused a significant reduction in
damage such as thiobarbituric acid reactive species are eval- chlorophyll production by wheat foliage. Also, exposure of
uated (Pryor 1991). The ultimate product of membrane lipid Lemna gibba plants to CuO nanoparticles for 45 h resulted
peroxidation is malondialdehyde, whose amount is directly in the inactivation of photosystem-II reaction center and
related to oxidation of polyunsaturated fatty acids (PUFAs) increased dissipation of thermal energy (Perreault et al.
(Song et al. 2016). When plant system becomes inefficient 2014). Similarly, the photosynthesis of soybean exposed to
to scavenge the reactive oxygen species due to nanoparticle- 0.01, 0.05, 0.1, and 0.5 g L ­ −1 of C
­ r2O3 nanoparticles sus-
mediated oxidative stress, malondialdehyde level increases pensions was inhibited. The maximum quantum yield of

13
1574 Environmental Chemistry Letters (2021) 19:1545–1609

photosystem-II (Fv/Fm) decreased up to 22% which indi- could be due to the physical blockage of root pores, thus
cates the destruction of photosynthetic apparatus by C ­ r2O 3 considerably reducing water and nutrient uptake (Ma et al.
nanoparticles (Li et al. 2018b). In a study, Cu nanoparti- 2013d; Martínez-Fernández et al. 2015). Similarly, reduced
cles maximally decreased chlorophyll-a content by 33%, activity of ascorbate peroxidase was recorded under C ­ eO2
whereas Ni nanoparticles decreased chlorophyll-b content nanoparticle (800 mg kg−1) treatment with a concurrent
by 68% in wheat seedlings after 2 days of exposure (Korot- decline in ­H2O2. These studies suggest that anti-oxidant
kova et al. 2017). Similarly, Ag nanoparticles also reduced enzymes activities are decreased (Mukherjee et al. 2014)
photosynthesis in S. polyrhiza by inhibiting the photopro- or increased (Kim et al. 2011) in plant cells based upon the
tective capacity of photosystem-II and RUBISCO activity exposure, plant organ, and concentration of test nanoparti-
which resulted in reduced ­CO2 assimilation associated with cles. Taking another example, Amooaghaie et al. assessed
a decrease in solar energy consumption (Jiang et al. 2017). the impact of varying concentrations of Zn and ZnO nano-
Likewise, ­CeO2 nanoparticles notably reduced total chloro- particles on tomato and wheat plants (Amooaghaie et al.
phyll in tomato plants grown for 210 days in pot soils mixed 2017). At 100 mg L ­ –1, both nanoparticles slightly enhanced
with 250 mg kg−1 of citric acid coated C­ eO2 nanoparticles the activity of three enzymes peroxidase, ascorbate peroxi-
(Barrios et al. 2016). dase, and catalase in both test crops, whereas, at 200 mg
­L–1, both nanoparticles significantly enhanced the superox-
Nanoparticle‑mediated enhancement in antioxidant ide dismutase level, only in wheat foliage.
enzyme activity
Mutations, chromosomal anomalies,
Nanoparticle-induced intracellular oxidative stress in plants and destruction of genetic material
leads to enhanced antioxidant activity, and their measure-
ment serves as a toxicity bio-indicator (Sardoiwala et al. In addition to the physiological impacts, nanoparticles can
2018). This system comprises the single or combined role also induce genotoxic effects either directly or indirectly in
of antioxidant enzymes such as peroxidases (glutathione plants (Table 2). Of these, physical interactions between
peroxidase, ascorbate peroxidase, and guaiacol peroxidase), DNA and nanoparticles cause direct genotoxic impact
superoxide dismutase, and catalase. Moreover, low molecu- altering or modifying (i) phosphorylation, (ii) DNA stacks
lar weight compounds including phenolic compounds, vari- among DNA bases, (iii) gene regulation/expression, and
ous carotenoids, ascorbate, glutathione, α-tocopherols, and (iv) trigger adduct formation. The later one can result from
proline are also produced in higher amounts by plant sys- altered gene expression due to inhibition of DNA repair
tem in response to the damaging impact of reactive oxygen mechanisms (Karami Mehrian and De Lima 2016; Ghosh
species under nanoparticles stress (Das and Roychoudhury et al. 2019). Plant cell with low number of chromosomes can
2014; Getnet et al. 2015; Ozyigit et al. 2016). These are the help to visualize the genotoxic impact of nanoparticles and
candidates which either independently or simultaneously act hence is incorporated in genotoxic studies as a testing model.
to decrease the elevated level of oxidative destruction. As an While assessing the genotoxic impact of nanoparticles, the
example, catalase and superoxide dismutase synergistically following toxicological endpoints are considered: appear-
convert first superoxide ions [O‒O]2− to hydrogen perox- ance of aberrant chromosomes during mitosis or meiosis,
ide ­(H2O2) and then to H­ 2O and ­O2 with additional role of change in ploidy levels, exchange between sister chromatids,
reduction of hydroxyl radicals (·OH), whereas peroxidases DNA lesions, and genetic mutations (Pakrashi et al. 2014;
act as scavenger of reactive oxygen species. Ghosh et al. 2015).
Plant–nanoparticles interactions have also shown Some examples of chromosomal aberrations, genotoxic-
increased production of these enzymes in a concentra- ity and DNA damage are shown in Fig. 19. In this context,
tion dependent manner. As an example, ZnO nanoparti- A. cepa chromosomal aberration bioassay has been used for
cles enhanced the secretion of non-enzymatic antioxidant genotoxicity assessment in several studies. By using A. cepa
molecules and thus anti-oxidative response at a concen- model, chromosomal aberrations like broken chromosomes,
tration range of 500–1500 µg L ­ −1 in black mustard (Zafar bridges, stickiness, laggings, disorientation during anaphase,
­ eO2 nanoparticles at 400 mg kg−1
et al. 2016). Similarly, C disturbed metaphase, and one or many micronucleus by nan-
caused a 39-fold increase in catalase activity of shoot as oparticles of ­Al2O3 (Rajeshwari et al. 2015), Ag (Cvjetko
compared to control; however, catalase activity was declined et al. 2017), Zn (Taranath et al. 2015), ZnO (Sun et al.
by 30-fold at 800 mg kg−1. In a likewise study, ­Fe3O4 nano- 2019b), bismuth (III) oxide (Liman 2013), ­TiO2 (Pakrashi
particles induced the higher production of two major anti- et al. 2014), and Cu (Nagaonkar et al. 2015) have been doc-
oxidant enzymes (catalase and superoxide dismutase) over umented in A. cepa root cells. Moreover, metaphasic and
bulk material of F
­ e3O4 without travelling from roots to aerial anaphasic disorientation in root meristem cells of Vicia faba
parts (Wang et al. 2011a). The enhanced enzyme activity seedlings after 72 and 120 h exposure of Ag nanoparticles

13
Environmental Chemistry Letters (2021) 19:1545–1609 1575

B C

Fig. 17  Nanoparticles induced reactive oxygen generation in plants: rectangles, while arrowheads point toward root tip. Adapted with
confocal laser scanning microscopic analysis of tomato roots and leaf permission from (Ahmed et al. 2018a). Panel C shows the reactive
reveals tissue wide localization of enhanced intracellular reactive oxygen species generation in roots of eggplant after exposure with
oxygen species following the exposure to A­ l2O3 and CuO nanoparti- Co3O4-nanoparticles. As in tomato roots, green fluorescence speci-
cles (NPs) compared to controls. Generation of intracellular oxidative fies reactive oxygen species production at varying concentrations of
stress is shown in panels A2−A4 for CuO nanoparticles treatment ­Co3O4-nanoparticles. Adapted with permission from (Faisal et al.
and panel A5−A7 for Al2O3 nanoparticles treatment over untreated 2016). Panel D shows the pathways for the induction of intracellular
control of leaf (panel A1). Panel B depicts reactive oxygen species reactive oxygen species mediated primarily by hydrogen peroxide,
localization in tomato roots. Two physiologically distinct root zones superoxide, and hydroxyl radicals
as elongation and meristematic zone are denoted by yellow and blue

13
1576 Environmental Chemistry Letters (2021) 19:1545–1609

Deposition of nanoparticles in leaf

Synthesis of photosynthec pigments

Funconing of PS-I and PS-II
Photo-protecve ability of PS-II
Maximum quantum yield (Fv/Fm)
Chloroplast Photochemical quenching (qP) H+
RUBISCO acvity NADP NADPH
H+ ADP ATP
Light Pi
Thylakoid lumen
H+ Cytochrome Fd FNR
P-680 P-700
Alteraon of
e- e-
membrane PQ
physiology
PS-II
PQH2
b6 f PS-I
Plastoquinone
PC ATP synthase
Plastocyanin
e-
Oxygen evolving complex Nanoparticles
H+
H+
H2O O2 H+

Stroma

Fig. 18  Nanoparticles induced reactive oxygen generation in plants: rectangles, while arrowheads point toward root tip. Adapted with
Confocal laser scanning microscopic analysis of tomato roots and permission from (Ahmed et al. 2018a). Panel C shows the reactive
leaf reveals tissue wide localization of enhanced intracellular reactive oxygen species generation in roots of eggplant after exposure with
oxygen species following the exposure to ­Al2O3 and CuO nanopar- Co3O4-nanoparticles. As in tomato roots, green fluorescence speci-
ticles (NPs) compared to controls. Generation of intracellular oxida- fies reactive oxygen species production at varying concentrations of
tive stress is shown in panels A2–A4 for CuO nanoparticles treatment ­Co3O4-nanoparticles. Adapted with permission from (Faisal et al.
and panel A5–A7 for ­Al2O3 nanoparticles treatment over untreated 2016). Panel D shows the pathways for the induction of intracellular
control of leaf (panel A1). Panel B depicts reactive oxygen species reactive oxygen species mediated primarily by hydrogen peroxide,
localization in tomato roots. Two physiologically distinct root zones superoxide, and hydroxyl radicals
as elongation and meristematic zone are denoted by yellow and blue

is evident (Abou-Zeid and Moustafa 2014). Genotoxicity of attempts have been made to evaluate the impact of nano-
­TiO2 nanoparticles has been confirmed by evaluating DNA particles on proteome and metabolome of various cereal,
comets and ladders. The formation of micronucleus and legume, and vegetable crops including wheat, rice, beans,
other chromosomal anomalies validated the genetic manipu- and cucumber. The impact of nanoparticles on gene expres-
lation by nanoparticles in preceding cell cycle (Rico et al. sions employing DNA microarrays for A. thaliana (Landa
2011). In a study, Xi et al. reported that ­TiO2 nanoparticles et al. 2012; García-Sánchez et al. 2015) while exposing roots
caused purine oxidation which may cause abrupt DNA rep- to nanoparticles prepared from Ag and ­TiO2 for 7 days has
lication (Xi et al. 2004). Atha et al. reported DNA lesions shown that nanoparticles suppressed the transcriptional
caused by CuO nanoparticles in grasses and radish plants response which is generally needed for resisting and combat-
(Atha et al. 2012). Considerable accumulation of oxidatively ing the colonization of microbial pathogens. Gene transcrip-
modified three mutagenic DNA base lesions was recorded tion required in phosphorus starvation and for development
using GC–MS along with isotope dilution method. of roots was inhibited. Likewise, the microarray analysis
of A. thaliana roots grown with fullerene, ZnO, and T ­ iO2
Impact on gene expression, miRNA, proteome nanoparticles revealed that genes for both abiotic and biotic
and metabolome stress response factors such as oxidative stress and wound-
ing were up-regulated, while gene expression essential for
The nanoparticles have been reported to alter the gene maintaining cellular organization and biogenesis was signifi-
expression (Table 3), proteome (Table 4), miRNA expres- cantly inhibited due to ZnO nanoparticles stress (Landa et al.
sion, and metabolome (Table 5) of various crops. Most of 2012). In another study, the expression of genes associated
the gene expression and miRNA profiling studies have, how- with glutathione biosynthesis and sulfur assimilation was
ever, been focused on assessing the impact of nanoparticles altered causing eventually the genotoxicity to A. thaliana
on A. thaliana gene expression and N. tabacum miRNA, raised with 50–500 ­mgCeO2 nanoparticles ­L−1 of C ­ eO2 (Ma
both of which are not essentially food crops. Still, several et al. 2013a). In an identical experiment, it was reported that

13
 Table 2  Genotoxicity of nanoparticles to crop plants
Type of nanoparticle Characteristics of Crop Concentrations tested Exposure conditions Toxicity markers Toxic effect References
nanoparticles

TiO2 Size: spheri- T. aestivum 20–100 mg kg−1 soil 60 days exposure in MN 53.65% at 80 mg kg−1 Rafique et al. (2018)
cal < 20 nm by SEM, soil (sandy loam, and 62.5% at
Dispersion: in deion- pH 7.6) 100 mg kg−1
ized water, sonica-
tion for 30 min
Zero valent ­Fe0 (nZVI) Size: nZVI-1 (49 nm), A. cepa 125, 250, 500 mg L
­ −1 Exposure in hydro- MI, MN, CA, NA, Significant reduc- Ghosh et al. (2017)
nZVI-2 (57 nm), ponic environment DNA comets tion in MI from
Dispersion: in for 24 h at 25 ± 2 °C 14.62 ± 1.79%
ultrapure water (at in control to
40 W for 15 min), 9.63 ± 0.05%
Size by DLS: 211 and by nZVI-1 and
254 nm 10.2 ± 1.16% by
Environmental Chemistry Letters (2021) 19:1545–1609

ZP:—18.76 nZVI-2,
to—35.7 mV Increase in MN by
1.3% under nZVI-1
and 0.4% under
nZVI-2 exposure,
Significant increase
in CAs from
0.19 ± 0.1% in con-
trol to 12.67 ± 0.32%
by nZVI-1 and
4.24 ± 0.37% by
nZVI-2,
Significant increase in
NA from 0.09% in
control to 6.02% by
nZVI-1 and 3.23%
by nZVI-2,
Comet assay revealed
increased DNA
damage by 35% by
nZVI-1 and 20.35%
by nZVI-2 compared
to control (3–4%)
Fe2O3 Size: 22.3 ± 3.1 nm R. sativus 0.25–2 mg mL−1 Seeds were exposed DNA comets Concentration depend- Saquib et al. (2016)
by TEM, and for 2 h in rotatory ent increase in DNA
271 ± 2.4 nm by shaker followed by strand breaks
DLS with ZP of transfer on Petri dish
4.1 ± 0.9 mV and incubation for
Dispersion: in 4 days at 25 ± 2 °C
ultrapure water (at
40 W for 15 min)

13
1577
 Table 2  (continued)
1578

Type of nanoparticle Characteristics of Crop Concentrations tested Exposure conditions Toxicity markers Toxic effect References
nanoparticles

13
NiO Size: 1100–1250 nm Seeds of A. cepa, A 0–500 mg ­L−1 Seeds were exposed MI, CA, MN Significant reduction Manna and Bandyo-
by DLS as compared porrum, A. sativum, A. for 6 h in rotatory in MI from 70% in padhyay (2017)
to 33.65 nm recorded fistulosum shaker followed by control to 20% in
by TEM with ZP of seeds, A. schoenopra- washing and transfer treatment,
8.42 ± 3.77 mV dis- sum on Petri dish and Chromosomal breaks
persed in ultrapure incubated for 7 days as 0.4% in control
water and sonicated at 23 ± 1 °C and 1.6% in treat-
at 60 W, 40 kHz for ment,
45 min MN as 3% in control
and 7% in treatment
Al2O3 Size: 121–479 nm A. cepa 0–5 µM Onion bulbs were MI, MN, CA, Comet Significant reduction De et al. (2016)
as recorded by exposed in hydro- analysis in MI from 15.22%
DLS with ZP of ponic solutions for in control to 4.06%
-16.5 ± 6.12 mV, 24 h at 28 ± 0.5 °C by ­Al2O3 nanopar-
dispersed in Milli-Q ticles
water, sonicated at Increase in MN by
130 W for 30 min 2.24,
Significant increase
in CAs
Comet assay revealed
increased DNA
damage by A ­ l2O3
nanoparticles as 10%
compared to control
(2%)
ZnO Size: 100 nm and V. faba seeds, A. cepa 0.2–0.8 g ­L−1 Exposure was given MI, MN, CA, Comet MI: A. cepa control Ghosh et al. (2016)
285–317 nm as roots, and N. taba- in hydroponic for analysis 6.78%, treated 0.62%
recorded by TEM cum seedlings 24–48 h at 25 ± 1 °C V. faba control 4.91%,
and DLS, dispersed treated 0.38%
in Milli-Q water, MN: 4.9% and 19.3%
sonicated at 100 W, increase in A. cepa
30 kHz for 30 min and V. faba, respec-
tively
CA: 0.18% and 0.19%
increase in A. cepa
and V. faba, respec-
tively
Comet: A. cepa con-
trol 4%, treated 24%
N. tabacum control
4%, treated 9.5%
Environmental Chemistry Letters (2021) 19:1545–1609
 Environmental Chemistry Letters (2021) 19:1545–1609 1579

the two genes ORF31 (152u) and BIP3 (005u) were consist-

TEM: transmission electron microscopy; DLS: dynamic light scattering; ZP: zeta potential; MI: mitotic index; MN: micronucleus index; CA: chromosomal aberration; and NA: nuclear aberra-
Cvjetko et al. (2017)
ently modulated by C ­ eO2 nanoparticles, CuO nanoparticles,
and ­La2O3 nanoparticles (Pagano et al. 2016) suggesting that
References

these genes can be considered as potential biomarker for

identifying the toxicity of nanoparticles to Cucurbita pepo
and Solanum lycopersicum.
The micro-RNA gene expression analysis of A. thaliana

nanoparticles > PVP-

Ag-ions > CTAB-Ag
cantly compared to

(Nair and Chung 2014) and N. tabacum (Burklew et al.

increased signifi-
Number of comets

cles > citrate-Ag

following order

2012) after nanoparticle exposure is reported. The miRNA

Ag nanoparti-

nanoparticles
control in the

can be defined as the small non-coding RNA typically rang-

Toxic effect

ing between 22 and 25 nucleotides (Ahmad et al. 2013),

acting as an endogenous post-transcriptional regulator of
gene expression either by (i) inhibiting or (ii) degrading
messenger RNAs (mRNAs) preventing their translation.
The miRNAs also control plant response to abiotic stress by
Toxicity markers

mediating expression of related genes. Since nanoparticles

alter the gene expression in non-edible plants like tobacco
and A. thaliana, it is expected that they can also influence
Exposure was given in Comet

the genetic expression in edible crop plants. As an exam-

ple, carbon nanoparticles stimulated production of aqua-
porin proteins and enhanced water uptake in tobacco cells
hydroponic for 72 h
Concentrations tested Exposure conditions

(Khodakovskaya et al. 2012). In a study, ­Al2O3 nanoparticles

up-regulated the expression of miRNA genes, which helped
in the survival of tobacco plants. To substantiate this, N.
at 25 °C

tabacum plant was exposed to 0–1% concentration of ­Al2O3

nanoparticles. As the concentration of ­Al2O3 nanoparticles
increased, the biological attributes such as biomass accu-
mulation, root volume, and number of leaves were signifi-
cantly decreased. Studies on gene expression of at least nine
miRNAs with known functions of reducing abiotic stress
0–100 µM

in plants showed that increasing concentrations of ­Al2O3

nanoparticles considerably up-regulated the miRNAs gene
expression (Burklew et al. 2012). In a similar study, two
miRNA genes (miR399 and miR395) of tobacco plant under
0.1% and 1% ­TiO2 nanoparticle’s exposure caused a drastic
change in gene expression as 143- and 285-fold, respec-
tively, suggesting the adverse impact of T­ iO2 nanoparticles
on plant growth and development (Frazier et al. 2014).
A. cepa
Crop

Programmed cell death induced by nanoparticles

Size ranged between 5
and 50 nm, Disper-

Apoptosis or programmed cell death is another cytotoxic

sion: in distilled
Characteristics of

outcome of nanoparticle’s interaction with plant cells. How-

nanoparticles

ever, there are very few reports on nanoparticles induced

apoptosis. In this regard, four pioneer studies have reported
water

apoptosis by nanoparticles of NiO and ­Co3O4, single- and

multi-walled carbon nanotubes. In a comet assay and flow
cytometry-based analysis of apoptosis in tomato roots,
Ag (surface function-
Type of nanoparticle

citrate and CTAB)

Table 2  (continued)

alized with PVP,

a significant increase in dead cells due to emergence of

apoptotic (21.8%) and necrotic (24%) cell population was
observed when roots were exposed to 2 mgNiO nanopar-
ticles ­mL−1 (Faisal et al. 2013) compared to negative con-
tion.

trol (Fig. 20A–D). Data recorded through flow cytometric

13
1580 Environmental Chemistry Letters (2021) 19:1545–1609

Fig. 19  Genotoxicity and DNA A C

B
damage induced by nanopar- Chromosome break Disturbed
ticles. Chromosomal anoma- nucleus
lies after exposure to TiO2
nanoparticles in A. cepa root
meristem cells: panels A and B Nuclear notch
show two types of anomalies in Chromosome
chromosome fragments, while bridge forma on
panels B–D represent nuclear
damage and formation of
micronuclei. Panel F indicates D E F
metaphasic stickiness during the
arrangement of chromosomes Micronucleus forma on
at metaphasic plate. Adapted Budding nucleus
with permission from (Pakrashi S cky
et al. 2014). Panels G shows metaphase
formation multi-walled carbon
nanotubes (MWCNTs) induced
formation of DNA tail in root
nuclei of A. cepa. Comet data
at 10 μg multi-walled carbon
nanotubes ­mL−1 were signifi-
G H M WCNTs (μg/ml)
Control 5 10
cant at P < 0.05 over untreated
control. Micrographs at the bot-
tom of bar diagram show repre-
sentative comets with varying
degree of DNA tail formation.
Panel H is for DNA laddering of
DNA incubated with or without
multi walled carbon nanotubes.
Bands highlighted in in agarose
gel in red correspond to internu-
cleosomal fragments. Adapted
with permission from (Ghosh
et al. 2015)

experiments revealed a 65.7% increase in dead cells and through flow cytometry exhibited 73.2% more apoptotic
more than twofold higher activity of caspase-3-like proteases cells as compared to negative control (Faisal et al. 2016).
activity at 2 mgNiO nanoparticles ­mL−1. The apoptosis and In a different study, single-walled carbon nanotubes caused
necrosis are two different events, which follow some major condensation of chromatin fibers with simultaneous pro-
steps of cytotoxicity illustrated in Fig. 20. Two pathways for duction of enhanced intracellular oxidative stress in rice
apoptosis are widely known intrinsic and extrinsic. cell suspensions (Shen et al. 2010). Besides, single-walled
In the study of NiO nanoparticles and tomato root carbon nanotubes-induced apoptosis was also noticed at
interaction, mitochondrial-dependent intrinsic pathway 25 μg single-walled carbon nanotubes ­mL−1. It has also
has been suggested which could be assigned to release been reported that multi-walled carbon nanotubes in an
of ­N i 2+ ions in the solution from NiO nanoparticles identical manner can damage rice cells in suspension (Tan
(Faisal et al. 2013). It has also been reported that apop- et al. 2009) which could probably be mediated by apopto-
tosis-mediated toxicity in some vegetables, for example, sis at low concentration. On the other hand, higher dose
eggplant occurred, when it was exposed to ­Co3O4 nano- of nanoparticles can inhibit plant growth by induction of
particles (Faisal et al. 2016). Exposure of eggplants to necrosis as revealed by alteration of cell membrane perme-
cogrowth enhancing impact as depicted O ­ 4 nanoparticles ability leading to the leakage of cytoplasmic fluid. As an
(1 mg mL−1) revealed approximately 2.4-fold greater DNA alternative way of protecting the large population of cells,
damage using comet assay, while cell cycle measurement rice cells when treated in suspension can precipitate a

13
 Table 3  Transcriptomic studies of nanoparticle–plant interaction
Nanoparticle Size (nm) Plant Plant organ Dose rate Total age Exposure Observation Overall References
of plant at time impact
treatment
TiO2 10, 20 and A. thaliana Both roots and aerial part 20 mg ­L−1 21 days 2 days No effect TiO2 nano- García-
40 particles Sánchez
exposure et al. (2015)
showed
almost
similar
gene
expression
pattern
among the
treatments,
the impact
Environmental Chemistry Letters (2021) 19:1545–1609

was very
low as
compared
to salinity,
drought,
and
wounding
stress

13
1581
 Table 3  (continued)
1582

Nanoparticle Size (nm) Plant Plant organ Dose rate Total age Exposure Observation Overall References
of plant at time impact

13
treatment
TiO2 33 A. thaliana Both roots and aerial part 500 mg ­L−1 Seeds 12 days Positive RT-qPCR Tumburu et al.
effect analysis (2015)
showed
altered
expres-
sion of
204 genes,
which
include
the genes
associated
with oxida-
tive stress,
salt stress,
transport
of water,
and
respira-
tory burst.
Addition-
ally, a
range of
metabolic
processes
was
affected
Environmental Chemistry Letters (2021) 19:1545–1609
 Table 3  (continued)
Nanoparticle Size (nm) Plant Plant organ Dose rate Total age Exposure Observation Overall References
of plant at time impact
treatment
TiO2 33 A. thaliana Both roots and aerial part 500 mg ­L−1 Seeds 29 days Nil impact Microarray Tumburu et al.
analyses (2017)
showed
alteration
in tran-
scriptomes
of rosette
leaves with
large num-
ber of dif-
ferentially
expressed
Environmental Chemistry Letters (2021) 19:1545–1609

genes
(DEGs),
­TiO2 nano-
particles
affected
photo-
synthesis
associated
genes,
more
DEGs
were
altered
in rosette
leaves than
those in
roots

13
1583
 Table 3  (continued)
1584

Nanoparticle Size (nm) Plant Plant organ Dose rate Total age Exposure Observation Overall References
of plant at time impact

13
treatment

CuO 25–55 Brassica rapa Whole seedlings 50–500 mg Seeds 15 days Negative RT-PCR Chung et al.
­L−1 effect analysis (2019b)
revealed
transcrip-
tional
alteration
of genes
associ-
ated with
biosyn-
thesis of
phenolics
and oxida-
tive stress,
significant
up regula-
tion of
antioxidant
genes was
noticed
ZnO 20 A. thaliana Col-0 Roots 4 mg ­L−1 28 days 7 days Negative Microarray Landa et al.
effect analyses (2015)
exhibited
up-regu-
lation of
416 genes
includ-
ing stress
response
genes and
down-reg-
ulation of
961 genes
including
nucleic
acid
metabo-
lism,
biogenesis,
and cell
organiza-
tion
Environmental Chemistry Letters (2021) 19:1545–1609
 Environmental Chemistry Letters (2021) 19:1545–1609 1585

fraction of cell population with test nanoparticles thus safe

References guarding others. This is an indirect mode of self-defense

Microarray Tang et al.

minimizing the nanoparticle’s risk (Rico et al. 2011).

(2016)

expression,

genes were
Plausible mechanism of nanoparticles’ toxicity
able gene

genes, 47

regulated

ated with
oxidative
were up-
of those
showed

associ-
to crops

found
Overall

stress
impact

vari-

From the literature reviewed and the experimental results

obtained so far on the toxic behavior of nanoparticles begin-
Observation

ning with absorption by leaves and roots to translocation and

Negative
effect

accumulation in various organs of actively growing plants,

the phytotoxic events leading to the death of plants (Fig. 21)
can be categorized into the following steps: (i) Adsorption:
Exposure

nanoparticles are adsorbed onto the surface of leaf and root

due to repulsive and attractive forces; (ii) uptake: the uptake
time

2h

of nanoparticles inside the cells depends largely on the pore

size of cell wall and size of nanoparticles. However, the
of plant at
treatment

nanoparticles have been observed to increase the porosity

Total age

15 days

of plant cell membrane. (iii) Internalization: after successful

adsorption, the infiltration (internalization) of nanoparticles
inside the cell occurs which are then deposited onto various
10 mg ­L−1
Dose rate

cellular organelles such as the tonoplast of vacuoles; (iv)

Translocation: translocation of nanoparticles proceeds via
vascular tissues (e.g., xylem) to different plant organs. Cell-
to-cell movement of nanoparticles occurs through intracel-
lular junctions. Nanoparticles start disrupting cellular home-
ostasis with their sequestration on the nuclear membrane,
degenerate nuclear constituents, and dissipate mitochondrial
membrane potential (ΔΨm) and sometimes the appearance
Plant organ

of swollen mitochondria; (v) disruption of homeostasis; (vi)

genotoxicity: nanoparticles also exhibit genotoxic effect and
Roots

cause DNA damage as revealed by disruption of mitosis

(mitotic index) and induction of chromosomal aberrations.
Also, nanoparticles induce caspase-dependent degradation
of nuclear DNA (sub-G1 phase) which indicates apoptosis;
A. thaliana Bay-0

(vii) lipid peroxidation and antioxidant generation: nanopar-

ticles increase lipid peroxidation (malondialdehyde content)
and generation of intracellular reactive oxygen species ­(O2·‾,
­OH·, and H ­ 2O2) which are responsible for alteration in ΔΨm;
Plant

(viii) destruction of physiological and metabolic functions

leading to reduction in biological attributes and yield of
plants; and (ix) death of plants due to one or simultaneous
Size (nm)

activity of nanoparticles. Conclusively, when composition,

30–50

concentration, size, morphology, and surface adsorbing abil-

ity of nanoparticles differ, the toxic impact of nanoparticles
is very likely to change dramatically. Hence, the phytotoxic-
ity mechanism of nanoparticles requires further elaborative
Table 3  (continued)

research. In this regard, a few cutting-edge molecular strate-

gies such as proteomics and genomics are likely to enhance
Nanoparticle

the understanding on phytotoxicity of nanoparticles.

CuO

13
 Table 4  Proteomic studies of nanoparticle–plant interaction
1586

Nanoparticle Size (nm) Plant Plant organ Dose rate Total age Exposure Observation Overall impact References
of plant at time

13
treatment
Ag 18.3 O. sativa Whole plant 30 and 60 mg ­L−1 10 days 20 days Negative The Ag Mirzajani
effect nanoparti- et al. (2014)
cles resulted
in protein
precursor
accumulation
indicative of
proton motive
force dissipa-
tion, proteins
measured
were involved
in ­Ca2+
regulation,
cell signaling,
transcription,
oxidative
stress mitiga-
tion, cell divi-
sion, protein
degradation,
cell wall and
apoptosis
Environmental Chemistry Letters (2021) 19:1545–1609
 Table 4  (continued)
Nanoparticle Size (nm) Plant Plant organ Dose rate Total age Exposure Observation Overall impact References
of plant at time
treatment

PVP-Ag 10 T. aestivum Roots and shoots 10 mg ­L−1 Seeds 5 days Negative 2-DE based Vannini et al.
effect proteomic (2013)
analysis
revealed
relatively low
amount of
differentially
expressed
proteins
(DEPs), expo-
sure induced
changes in
Environmental Chemistry Letters (2021) 19:1545–1609

redox regula-
tion, sulfur
metabolism,
change in
protein syn-
thesis associ-
ated with
endoplasmic
reticulum and
vacuoles
CeO2 8 P. vulgaris Seeds 62.5–500 mg kg−1 Seeds 102 days No effect Proteomic Majumdar
analysis et al. (2015)
showed up
regulation of
stress related
proteins at
62.5 and
125 mg kg−1,
major proteins
associated
with nutrient
storage (pha-
seolin) and
carbohydrate
metabolism
(lectins) were
down-regu-
lated

13
1587
 Table 4  (continued)
1588

Nanoparticle Size (nm) Plant Plant organ Dose rate Total age Exposure Observation Overall impact References
of plant at time

13
treatment

Al2O3 30–60 G. max Root including 5–500 ppm 2 days 1–3 days Positive effect Using gel-free Hossain et al.
hypocotyl (nano-LC (2016)
MS/MS),
proteins that
were signifi-
cantly altered
by ­Al2O3
nanoparticles
were mainly
associated
with energy
metabolism,
hierarchical
clustering
analysis,
proteins asso-
ciated with
glycolysis
exhibited
major changes
in abundance,
among all
responsive
proteins,
major popula-
tion was
found related
to protein
synthesis or
degradation,
lipid metabo-
lism and
glycolysis
Al2O3 30–60 G. max Root 5–500 ppm 2 days 2–4 days Positive effect 211 proteins Yasmeen et al.
of cell wall, (2016)
protein syn-
thesis, stress
and signal-
ing were up
regulated
Environmental Chemistry Letters (2021) 19:1545–1609
 Table 4  (continued)
Nanoparticle Size (nm) Plant Plant organ Dose rate Total age Exposure Observation Overall impact References
of plant at time
treatment

Chemo blended-Ag 15–20 T. aestivum Whole plant 6 days 11 days Positive effect Gel-free/ Jhanzab et al.
label-free pro- (2019)
teomic analy-
sis showed
that proteins
related to
photo- and
protein syn-
thesis were
increased,
whereas cell
signaling, gly-
Environmental Chemistry Letters (2021) 19:1545–1609

colysis, cell
wall, redox,
mitochon-
drial electron
transport
chain related
proteins were
decreased

13
1589
 1590

13
Table 5  Metabolomic and micro-RNA profiling studies of nanoparticle–plant interaction
Nanoparticle Size (nm) Plant Plant Dose rate Targeted Expo- Obser- Overall impact References
organ organ sure vation
time

micro-RNA (miRNA) profiling studies

Al2O3 Not specified N. tabacum Whole 0.1%, 0.5% Seeds 21 days Nega- Four micro-RNAs related to plant stress management showed Burklew et al. (2012)
plant and 1% tive remarkable enhanced expression when plants were exposed to
effect 1% w/v ­Al2O3 nanoparticles
TiO2 < 25 N. tabacum Whole 0.1% and Seeds 21 days Nega- TiO2 nanoparticles greatly enhanced the expression of miR399 Frazier et al. (2014)
plant 1% tive and miR395 by 143 and 285, respectively
effect
Metabolomic studies
CeO2 10–30 P. vulgaris Whole 250– Leaves 15 days Nega- Foliar application of ­CeO2 nanoparticles enhanced the bio- Salehi et al. (2018)
plants 2000 mg sprayed tive uptake of Ce, which caused production of proline up to
­L−1 for effect 0.65 mg g−1, production of phyto-siderophores like mugine-
14 days ate and muconate was found increased by more than 16-fold,
on translation of folding related proteins was also increased
leaves
or
added
in soil
after
every
48 h
1
Cu 40 C. sativus Mixture 10–20 mg Exudates 21 days H-NMR, GC–MS and ICP-MS revealed interference of Cu Zhao et al. (2016a)
of ­L−1 from nanoparticles with the accumulation of micro- and macro-
exu- root and elements including P, Mo, Na, Fe, Zn, and S, some metabolic
dates leaves alterations were also noticed in exudation pattern of roots and
leaves, Cu nanoparticles caused up-regulation of ascorbic
acid, amino acids, and phenolic compounds related gene,
however, genes associated with citric acid were down-regu-
lated
Environmental Chemistry Letters (2021) 19:1545–1609
Environmental Chemistry Letters (2021) 19:1545–1609 1591

Nanoparticles of dehydrogenase enzyme indicating microbial metabolic

A activity, which produces organic acids and thus increases the
Healthy cell
available forms of phosphorus in soil for subsequent plant
Swelling of ER and
uptake. The rhizospheric microbial population regulates soil
Release of cytochrome C
mitochondria fertility by performing essential biogeochemical cycling of
Caspase 9
Membrane blebbing
nutrients (Raliya et al. 2016b). In another study, dissolution
Caspase 3 Progressive B of ­Zn2+ ions from ZnO nanoparticles and their internaliza-
Chromatin condensation
injury tion in plant cells was found beneficial for the activity of
Breakdown of plasma
Cellular fragmentation membrane, organelles
carbonic anhydrase mediating more carbon dioxide fixation
and nucleus into carbohydrates. The combination of nanoparticles such
as ­SiO2 with ­TiO2 has also been found to increase the nitrate
reductase activity which catalyzes nitrate ­(NO3−) to nitrite
­(NO2−) and intensifies the absorption capacity of plants,
Apoptosis Necrosis
which in effect enhances the uptake of soil nutrients and
C D water (Rico et al. 2011). Some metallic and metal–oxide
nanoparticles tested against tomato plants increased Ca
content of root and shoot of tomato plants up to 69.8% (Vit-
tori Antisari et al. 2015b). Similarly, nanoparticles those
prepared from ceria and carbon also facilitate growth and
improve the yield of edible crops such as bitter melon,
Fig. 20  Apoptosis and cell death induced by nanoparticles: sequence wheat, and tomato (Raliya et al. 2015). One possibility is
of events starting from the interaction of nanoparticles with plant that if nanoparticles at some concentrations dependent on
cells ending in cell death by either apoptosis or necrosis. Panels A various factors increase the biomass accumulation of plant
and B show untreated cell (negative control) and ethylmethane sul-
fonate (2 mM) treated cell (positive control) of tomato roots. Nickel tissues and fruits with nil toxicity, then they can also be used
oxide nanoparticles at 2 mg ­mL−1 caused apoptosis (panel C) and in synergy with bio-fertilizers, thus optimizing benefits and
necrosis (panel D) in nuclei of tomato roots. Figures in panels A–D producing organic crops.
are adapted with permission from (Faisal et al. 2013)
Improvement in whole plant biomass, length,
Beneficial impacts of nanoparticles on plants and volume

Nanoparticles exhibit negative effects on physiology, mor- When present exposure media, nanoparticles have also
phology, overall plant development, and yield of many agri- shown growth stimulatory influence on edible crop plants
culturally important crops, yet they have also been found while growing under both soil-less media and in natural
exhibiting plant growth enhancing impact as depicted in soil environment (Table 6; Fig. 22). For example, 1–10
Fig. 22. The beneficial impacts also vary with growth stage ­mgCeO2 nanoparticles m ­ L−1 though marginally increased
of plants, test species of nanoparticle and plants, exposure shoot length; however, it substantially enhanced the total
concentration and condition, and duration of treatment. weight of tomato fruits at highest test concentration (10 mg
Some examples are summarized in Table 6. The positive ­L−1) (Wang et al. 2012a). In a different study, 500 ­mgCeO2
impact of nanoparticles on major growth parameters leading nanoparticles ­kg−1 of soil caused rapid elongation of stem
to enhancement in yield of some useful crops is explained in length and also increased the dry matter accumulation in
the following sections. barley by 331% over control but declined the grain produc-
tion considerably. On the contrary, C ­ eO2 nanoparticles at
Enhancement of nutrient absorption and water 125 and 250 mg kg−1 added to soil stimulated grain yield
uptake with concurrent accumulation of high amounts of cerium in
leaves and grains (Rico et al. 2015a). Likewise, the impact
Some nanoparticles may positively affect the nutrient uptake of varying concentrations of ­CeO2 nanoparticles on root
and water absorption from soils as reported in few studies. growth of cucumber, alfalfa, maize, and tomato was incon-
For instance, ZnO nanoparticles significantly affect three sistent, but on shoot elongation, it was consistent for all four-
major growth factors in mung bean rhizosphere including plant species (Chichiriccò and Poma 2015).
the availability of soluble form of phosphorus, root coloniza- Certain concentrations of nanoparticles may also detox-
tion by growth promoting microbes, and increased root sur- ify plant system by reducing overall intracellular oxidative
face area (Raliya et al. 2016b). The overall increased growth stress increasing biomass; for example, Zn acting as a co-
of mung bean plants has been attributed to enhanced activity factor of two antioxidant enzymes, namely catalase and

13
1592 Environmental Chemistry Letters (2021) 19:1545–1609

Fig. 21  Genotoxicity and DNA damage induced by nanoparticles. formation of DNA tail in root nuclei of A. cepa. Comet data at 10
Chromosomal anomalies after exposure to T ­ iO2 nanoparticles in A. μg multi-walled carbon nanotubes m­ L-1 were significant at P < 0.05
cepa root meristem cells: panels A and B show two types of anoma- over untreated control. Micrographs at the bottom of bar diagram
lies in chromosome fragments, while panels B-D represent nuclear show representative comets with varying degree of DNA tail forma-
damage and formation of micronuclei. Panel F indicates metaphasic tion. Panel H is for DNA laddering of DNA incubated with or with-
stickiness during the arrangement of chromosomes at metaphasic out multi-walled carbon nanotubes. Bands highlighted in in agarose
plate. Adapted with permission from (Pakrashi et al. 2014). Panel G gel in red correspond to internucleosomal fragments. Adapted with
shows formation multi-walled carbon nanotubes (MWCNTs)-induced permission from (Ghosh et al. 2015)

superoxide dismutase, may help to mitigate oxidative dam- and 20%, respectively, compared to negative control (Kole
age to plants. Moreover, the foliar application of ZnO nano- et al. 2013). Some better performance of mustard has been
particles has been reported to augment the growth and bio- obtained with 2.3 µg mL−1 of oxidized multi-walled carbon
mass of tomato (Mikkelsen 2018) and rice (Bala et al. 2019) nanotubes (Mondal et al. 2011).
suggesting that ZnO nanoparticles could be used as a future
nano-fertilizer. The exposure of iron oxide nanoparticles Enhanced photosynthetic rate
has been reported to increase the dry biomass of leaf and
pods of soybean. Also, iron oxide nanoparticles acted as iron Nanoparticles, in general, have been observed to have a
facilitators assisting in transfer of photosynthates to peanut positive impact on many physiological activities includ-
leaves. This could be due to the dissolution of iron from ing photosynthesis of plants (Fig. 22). In this category,
nanoparticles followed by its uptake by plant roots, which nanoparticles of ­TiO2, ­CeO2, and ZnO are significant. As
also enhanced root growth (Rico et al. 2011). In a similar an example, the ­TiO2 nanoparticles substantially improved
experiment, iron oxide nanoparticles have been found to pro- spinach growth (i) by improving light absorbance, (ii) by
mote substantially the growth and biomass of tomato plants enhancing the production of RUBISCO enzyme, and (iii)
(Siddiqi and Husen 2017b). Among carbon nanoparticles, by reducing the UV radiation mediated oxidative stress in
fullerene at 4.72 and 47.2 nM increased the production of chloroplast (Yang et al. 2007; Umeyama et al. 2015). A
bitter melon by 128 to 112%, respectively, when seeds were ­TiO2 nanoparticle has one of the three crystalline phases:
grown in a supplemented medium. Also, the synthesis of (a) brookite, (b) rutile, and (c) anatase. Mechanistically,
some important molecules such as cucurbitacin-B, lycopene, ­TiO2 nanoparticles in anatase phase show highest cata-
insulin, and charantin was also promoted by 74%, 82%, 91%, lytic activity than two other forms (Yan and Chen 2012),

13
Environmental Chemistry Letters (2021) 19:1545–1609 1593

Table 6  Nanoparticles-mediated growth enhancement of food crops

Nanoparticle Size (nm) Test crop Dose rate Activity/impact References

ZnO 1.2–6.8 Cyamopsis tetragonoloba 10 mg ­L−1 Significant improve- Raliya and Tarafdar (2013)
ment in plant length,
biomass accumulation,
surface area of roots,
photosynthesis, and
soluble protein
20 T. aestivum 2 g ­L−1 (foliar appli- Synchrotron X-ray Zhang et al. (2018a)
cation) at a rate of absorption spectros-
1.2 kg ha−1 copy and X-ray fluo-
rescence microscopy
revealed enhancement
in Zn concentration in
grain
Not specified V. radiate 20 ppm (foliar spray) Increased biomass Dhoke et al. (2013)
18 T. aestivum 6 mg kg−1 soil 15% decrease in grain Dimkpa et al. (2018)
yield with simultane-
ous internalization of
Zn in grain by 229%
and 186% under fresh
and weathered ZnO
nanoparticle exposure
18 Sorghum bicolor 6 mg kg−1 Enhanced accumula- Dimkpa et al. (2017)
tion of nitrogen and
potassium by sorghum
plants
TiO2 conjugated 30–50 S. lycopersicon 0–0.5 g ­L−1 Enhanced percent seed Singh et al. (2016)
with activated germination with less
carbon germination time
TiO2 Not specified G. max 0, 0.01, 0.03, 0.05% Enhancement in dry mat- Rezaei et al. (2015)
ter accumulation and
plant height
20 O. sativa 25–750 mg ­L−1 Enhanced accumulation Zahra et al. (2017)
of palmitic acid, amino
acids and glycerol in
rice grain, improved
shoot growth, and
phosphorus concentra-
tion in whole plant and
grains
32–171 T. aestivum ­ −1
10, 100, 1000 mg L Enhanced growth of lat- Zhang et al. (2019a)
eral roots and biomass
with concurrent uptake
of titanium
27 C. sativus 250, 500, Increased potassium Servin et al. (2013)
750 mg kg−1 and phosphorus in
cucumber fruits, ­TiO2
nanoparticles induced
oxidative defense
response as shown by
catalase activity in
other organs
16.04 S. lycopersicon 0.05–0.2 g ­L−1 Transpiration, photosyn- Qi et al. (2013)
thesis, and conduct-
ance to H­ 2O in tomato
leaves was improved
Fe3O4 13.9 P. vulgaris 1–1000 mg ­L−1 Fe3O4-PEG at 1000 mg Duran et al. (2018)
­L−1 increased radicle
growth
Not specified G. max 500–750 mg ­L−1 Quality and yield Sheykhbaglou et al. (2010)

13
1594 Environmental Chemistry Letters (2021) 19:1545–1609

Table 6  (continued)
Nanoparticle Size (nm) Test crop Dose rate Activity/impact References

SiO2 4–10 O. sativa 5 mM SiO2 nanoparticles Liu et al. (2009a)

increased grain yield
and weight
CuO Not specified T. aestivum 0.5 g kg−1 (sand culture) Enhanced biomass accu- Dimkpa et al. (2012)
mulation
Cu 50 S. lycopersicon 50–500 mg ­L−1 Cu nanoparticles López-Vargas et al. (2018)
enhanced lycopene,
vitamin-C in tomato
fruits, number of fruits,
and fruit firmness
Cu2O Not specified S. lycopersicon 0–160 ppm Highest percent germina- Ananda et al. (2019)
tion, increased leaf
pigment and increased
root/shoot elongation at
20 ppm

Fig. 22  A model illustrating the beneficial impacts of nanoparticles on plants including enhanced photosynthesis, increased root volume, nutri-
ent uptake, enhanced soil enzyme activities, increased plant biomass, number of flowers and fruits, and fruit mass

13
Environmental Chemistry Letters (2021) 19:1545–1609 1595

which promotes chlorophyll and carotene formation, as et al. 2008). Some studies report the genetic transmission of
reported in C. sativus. The ­TiO2 nanoparticles facilitate nanoparticles to progeny (Lin et al. 2009; Rico et al. 2011).
photosynthetic activity in spinach leaf by enhancing light For example, in a trans-generational study, the bean and rice
absorption rate by chlorophyll-a molecules, evolution of in their second generation revealed the presence of ZnO nan-
molecular oxygen, and rate of electron transfer (Xuming oparticles and fullerene which, however, varied greatly with
et al. 2008; Lyu et al. 2017). Similar to anatase, nano- age and organs of plants (Lin et al. 2009; Medina-Velo et al.
TiO2 having rutile crystal structure can prevent the gen- 2018). In a study with ZnO nanoparticles, P. vulgaris plants
eration of intracellular reactive oxygen species and thus were raised in soil artificially contaminated with two types
protect chloroplast membrane from the action of free of ZnO nanoparticles (i) coated with triethoxycaprylylsilane
radicals (Hong et al. 2005; Iswarya et al. 2015). Also, an and (ii) bare surface ZnO nanoparticles at a concentration
aerosol-based foliar spray of 500 m ­ gTiO2 nanoparticles range of 125–500 mg kg−1 soil. Seeds of first generation
­kg−1 soil brought an increase by 227.42% in chlorophyll (S1) accumulated ZnO nanoparticles, which were sown,
synthesis by tomato foliage, while the soil application of and seedlings were grown in soil without the amendment
750 ­mgTiO2 nanoparticles k­ g−1 increased the chlorophyll of ZnO nanoparticles followed by evaluation of trans-gen-
content maximally by 216.29% (Raliya et al. 2015). erational Zn accumulation in second generation seeds (S2)
When applied in soil, ­TiO2 nanoparticles enhance pho- and its impact. Results revealed that ZnO nanoparticles had
tosynthetic pigment content with simultaneous increase low residual trans-generational impact on seed composi-
in antioxidant activities in T. aestivum (Feizi et al. 2012). tion, which could be beneficial in agricultural production
Some other nanoparticles like ZnO nanoparticles have (Fig. 24) (Medina-Velo et al. 2018). The uptake followed by
shown a considerable increase in total soluble protein by subsequent transport to higher organism can be driven by the
25% and photosynthetic pigment production by 34.5% of solubility of nanoparticles (Uddin et al. 2020). The capillary
green gram plants grown in nanoparticles amended soils movement through which nanoparticles can travel to broader
(Raliya et al. 2016b). Foliarly applied ZnO nanoparticles channel locations can also influence the transport.
increased biomass accumulation, leaf protein, and chlo- ­ eO2 nanoparticle’s
Scientists have also tried to explain C
rophyll synthesis (Raliya and Tarafdar 2013; Raliya et al. transmission via food chain in detail (Hawthorne et al. 2014;
2015). In A. thaliana chloroplasts, exposure of negatively Majumdar et al. 2016). In one of such studies, Hawthorne
charged poly (acrylic acid) C­ eO2 nanoparticles (PNC) aug- et al. grew zucchini plants in soil amended with 1228 μg g−1
mented reactive oxygen species scavenging and enhanced ­CeO2 nanoparticles and, after 28 days, observed that leaf
photosynthesis (Wu et al. 2017b). ­CeO2 nanoparticles via tissues which were used to feed crickets had significant
a non-endocytic pathway and through the electrochemical amount of Ce (Hawthorne et al. 2014). The crickets were
gradient of membrane potential enter into chloroplasts. analyzed after 14 days for Ce uptake and also fed to wolf
PNC with a low ­C e 3+/Ce 4+ ratio of about 35% reduced spiders. Crickets fed on zucchini leaves contained a sig-
leaf reactive oxygen species (­ O2− + H2O2 + OH·) levels by nificant amount of Ce (33.6 ng g−1) which was higher than
52% and increased up to 19% of quantum yield in photo- control. Feces of crickets contained 1010 ng g−1 of Ce. Spi-
system-II, up to 67% of carbon assimilation and 61% of ders that consumed crickets from the nanoparticle-exposed
RUBISCO carboxylation rate over untreated control. The group accumulated 5.49 ng g−1 of Ce (Fig. 24). Similarly,
possible mechanism of enhanced photosynthetic rate in A. Phaseolus vulgaris grown in C ­ eO2 nanoparticles mixed soil
thaliana chloroplast is depicted in Fig. 23. at a concentration range of 1000–2000 mg kg−1 were fed
to Mexican bean beetles which were then eaten by spined
soldier bugs (Majumdar et al. 2016). Following 36 days of
Transmission of nanoparticles to progeny growth with 1000 m ­ gCeO2 nanoparticles k­ g−1, 1.02 μg g−1
and higher trophic level Ce was translocated to the upper ground parts. The beetle
larvae when fed on ­CeO2 nanoparticles treated leaves con-
The accumulation of nanoparticles in grains/fruits or con- tained low Ce concentration; meanwhile, 98% of Ce was
sumable parts of plants paves a way for their transfer to prog- excreted. However, accumulation of Ce in adults was higher
eny and to higher trophic level consumers via food web (Zhu than excreted Ce. Moreover, the bio-magnification of Ce

13
1596 Environmental Chemistry Letters (2021) 19:1545–1609

A B C arbohydrate fixation
S u gars
Leaf mesophyll cell

C O 2 +H2O

Stroma

CeO2-NPs CeO2-NPs

Extracellular
air space

Abaxial epidermis

CeO2-NPs Thylakoid membrane

Fig. 23  Transport of C ­eO2 nanoparticles (NPs) into chloroplast or forms malondialdehyde (MDA) and H ­ 2O through the reaction with
(panel A) and reactive oxygen species scavenging by C ­ eO2 nano- AsA catalyzed by enzyme ascorbate peroxidase (APX). Alternatively,
particles (panel B) in the following steps: (i) incident light leads to it is transformed to hydroxyl radical (­ OH·) via Fenton reaction. In the
electron transfer via fd (ferredoxin) to molecular oxygen which forms presence of C ­ eO2 nanoparticles, O­ 2−, ­H2O2, and ­OH· are catalyzed to
superoxide radicals (­O2−); (ii) superoxide dismutase (SOD) enzyme ­O2, ­H2O, and O ­ H–, respectively. Adapted and modified with permis-
catalyzes the transformation of ­O2− to H ­ 2O2. ­H2O2 by reacting with sion from (Wu et al. 2017b)
ascorbate (AsA) which is either converted to ­H2O and ­O2 by catalase

content was observed by a factor of 5.3 from plants to Mexi- that make nanoparticles so special and so powerful could
can bean beetles and then to spined soldier bugs (Fig. 24) damage agricultural crops and human health through trophic
(Majumdar et al. 2016). In another study, lettuce was treated transfer. Nanoparticles taken up by plants (through stomata
in soil with weathered/un-weathered CuO nanoparticles for and roots) bio-accumulate or are translocated to subcellu-
70 days and crickets fed on its leaves for 15 days followed lar compartments and various plant organs including fruits/
by consumption of crickets by lizards (Servin et al. 2017). grains. Inside the plant cells, due to multiple action sites,
The XANES and µ-XRF analysis showed that weathered nanoparticles can destruct cellular organelles and morphol-
CuO nanoparticles were transformed into ­Cu2O and ­Cu2S ogy, alter physiological and metabolic reactions of plants,
which were mainly localized in main and secondary roots; and modify gene expression, proteome and metabolome.
however, un-weathered CuO nanoparticles were present as Besides harmful effect, some nanoparticles can modulate
CuO in roots. CuO nanoparticles taken up in shoots were growth, development, and yield of crops, which makes them
transferred to crickets and then to lizards through trophic prospective candidates to be included in agricultural prac-
levels where they were found in crickets’ abdomen and head, tices. However, the biologically nondestructive properties
intestine and body of lizards. and ability of nanoparticles to persist indefinitely in the
environment are still questionable and require urgent atten-
tion. Also, nanoparticles can find their way to animals and
Conclusion humans through the consumption of nanoparticles enriched
foods and feeder via levels of the food chain. Considering
The massive production and unrestricted use of nanopar- these, the safe-by-design approaches need to be adopted
ticles in nano-enabled products and their unregulated dis- to produce nanoparticles/nano-products, which should be
posal in ecosystems have raised serious concerns over crop attractive and target specific but has little or nil inhibitory
yields. Due to nano-size, greater surface area, reactivity, and impacts on plant cells. Furthermore, scientists, industries,
surface charge, the nanoparticles when present in soils can and environmental agencies need to work hand in hand to
enter easily and rapidly into the intracellular environment of regulate its safe disposal into the environment to avoid the
plant system. Following entry, the nano-specific properties nanoparticle toxicity to plants and humans/animal.

13
Environmental Chemistry Letters (2021) 19:1545–1609 1597

Panel I
S2
Bean plant
No significant
S1 persistence of Zn
content in S2 seeds as
Increased Zn compared to control
content in S1
S0 seeds as compared ZnO nanoparticles reduced
Not
to control Ni content
amended
Seeds No change in yield, starch,
sugar and protein content
(i) Bare ZnO nanoparticles while no effect on P, K, S,
(ii) Triethoxycaprylysilane Fe, Mg, Mn, Mo, B and Cu
coated ZnO nanoparticles amount

Panel II
A B C D G H

Ce+
CeO2
nanoparticles Ce+++
Kidney bean plant Mexican bean
beetles larvae
E F

Ce++

Spined soldier bugs

Panel III
Transfer of CeO2 Transfer of CeO2
nanoparticles to nanoparticles to
crickets wolf spider

CeO2
nanoparticles
Zuchhini plant
Excretion of CeO2
nanoparticles

Fig. 24  Transmission of nanoparticles to the next trophic level. Panel collected to feed next consumer; f consumption of Mexican bean bee-
I shows the trans-generational flow of ZnO nanoparticles in bean tles by spined soldier bugs; g Mexican bean beetle larvae metamor-
plants raised in soil contaminated with coated and bare ZnO nanopar- phose into pupae (dormant phase); picture was taken after 25 days of
ticles. ZnO nanoparticles were taken up and transmitted to progeny treatment; and ­H– Mexican bean beetle adults feeding on plant leaf.
without showing trans-generational effects in nutrient composition (Picture was taken after 36 days of treatment.) Adapted and modi-
of seeds. Adapted and modified with permission from (Medina-Velo fied with permission from (Majumdar et al. 2016). Scheme (Panel III)
et al. 2018). Panel II shows a scheme assessing the trophic movement showing the trophic transfer of ­CeO2 nanoparticles (NPs) taken up by
of ­CeO2 nanoparticles: a Treatment of kidney bean plants with ­CeO2 zucchini plants followed by their accumulation in crickets and then to
nanoparticles; b infestation of plants with larvae of Mexican bean wolf spider or excretion of some fraction of ­CeO2 nanoparticles from
beetle; c and d leaf eating by Mexican bean beetles larvae (picture crickets. Adapted and modified with permission from (Hawthorne
was taken after 22 days of treatment); e Mexican bean beetles were et al. 2014)

Acknowledgements This work was supported by the Priority Research References

Centers Program through the National Research Foundation of Korea
funded by the Ministry of Education (2014R1A6A1031189).
Abbas Q, Yousaf B, Amina, et al (2020) Transformation pathways and
fate of engineered nanoparticles (ENPs) in distinct interactive
environmental compartments: a review. Environ Int 138:105646.
https​://doi.org/10.1016/j.envin​t.2020.10564​6
Abou-Zeid HM, Moustafa Y (2014) Physiological and cytogenetic
responses of wheat and barley to silver nanopriming treatment.
Int J Appl Biol Pharm Technol 5:150–163

13
1598 Environmental Chemistry Letters (2021) 19:1545–1609

Adamczyk Z, Weroński P (1999) Application of the DLVO theory for Auffan M, Rose J, Wiesner MR, Bottero JY (2009) Chemical stability
particle deposition problems. Adv Colloid Interface Sci 83:137– of metallic nanoparticles: a parameter controlling their potential
226. https​://doi.org/10.1016/S0001​-8686(99)00009​-3 cellular toxicity in vitro. Environ Pollut 157:1127–1133
Adams J, Wright M, Wagner H et al (2017) Cu from dissolution of Avellan A, Schwab F, Masion A et al (2017) Nanoparticle uptake
CuO nanoparticles signals changes in root morphology. Plant in plants: gold nanomaterial localized in roots of Arabidopsis
Physiol Biochem 110:108–117. https​://doi.org/10.1016/j.plaph​ thaliana by X-ray Computed Nanotomography and hyperspec-
y.2016.08.005 tral imaging. Environ Sci Technol 51:8682–8691. https​://doi.
Adisa IO, Pullagurala VLR, Peralta-Videa JR et al (2019) Recent org/10.1021/acs.est.7b011​33
advances in nano-enabled fertilizers and pesticides: a critical Baalousha M, Le Coustumer P, Jones I, Lead JR (2010) Characterisa-
review of mechanisms of action. Environ Sci Nano 6:2002–2030. tion of structural and surface speciation of representative com-
https​://doi.org/10.1039/c9en0​0265k​ mercially available cerium oxide nanoparticles. Environ Chem
Ahmad J, Hasnain SE, Siddiqui MA et al (2013) MicroRNA in car- 7(4):377–385. https​://doi.org/10.1071/EN100​03
cinogenesis & cancer diagnostics: a new paradigm. Indian J Med Baalousha M, Manciulea A, Cumberland S et al (2008) Aggrega-
Res 137:680–694 tion and surface properties of iron oxide nanoparticles: Influ-
Ahmed B, Dwivedi S, Abdin MZ et al (2017) Mitochondrial and chro- ence of pH and natural organic matter. Environ Toxicol Chem
mosomal damage induced by oxidative stress in Z ­ n2+ Ions, ZnO- 27(9):1875–1882. https​://doi.org/10.1897/07-559.1
Bulk and ZnO-NPs treated Allium cepa roots. Sci Rep 7:40685. Baalousha M, Yang Y, Vance ME et al (2016) Outdoor urban nanoma-
https​://doi.org/10.1038/srep4​0685 terials: the emergence of a new, integrated, and critical field of
Ahmed B, Khan MS, Musarrat J (2018) Toxicity assessment of metal study. Sci Tot Environ 557:740–753. https​://doi.org/10.1016/j.
oxide nano-pollutants on tomato (Solanum lycopersicon): A scito​tenv.2016.03.132
study on growth dynamics and plant cell death. Environ Pollut Baas P (2006) Vascular organization of angiosperms. A new vision
240:802–816. https​://doi.org/10.1016/j.envpo​l.2018.05.015 André J.-P. 2005. Enfield, New Hampshire: Science Publishers,
Ahmed B, Khan MS, Saquib Q et al (2018) Interplay between engi- Inc. $59.50 (hardback), $39.0 (paperback). 140 pp. Ann Bot
neered nanomaterials (ENMS) and edible plants: a current per- 97:1157–1157. https​://doi.org/10.1093/aob/mcl07​4
spective. Phytotox Nanopart. https:​ //doi.org/10.1007/978-3-319- Bais HP, Weir TL, Perry LG et al (2006) The role of root exudates
76708​-6_2 in rhizosphere interactions with plants and other organisms.
Akanbi-Gada MA, Ogunkunle CO, Vishwakarma V et al (2019) Phy- Annu Rev Plant Biol 57:233–266. https​://doi.org/10.1146/annur​
totoxicity of nano-zinc oxide to tomato plant (Solanum lycoper- ev.arpla​nt.57.03290​5.10515​9
sicum L.): Zn uptake, stress enzymes response and influence on Bala R, Kalia A, Dhaliwal SS (2019) Evaluation of efficacy of ZnO
non-enzymatic antioxidants in fruits. Environ Technol Innov nanoparticles as remedial zinc nanofertilizer for rice. J Soil Sci
14:100325. https​://doi.org/10.1016/j.eti.2019.10032​5 Plant Nutr 19:379–389. https​://doi.org/10.1007/s4272​9-019-
Amde M, Liu J, Tan ZQ, Bekana D (2017) Transformation and bio- 00040​-z
availability of metal oxide nanoparticles in aquatic and terrestrial Bandyopadhyay S, Plascencia-Villa G, Mukherjee A et al (2015) Com-
environments a review. . Environ Pollut 230:250–267. https:​ //doi. parative phytotoxicity of ZnO NPs, bulk ZnO, and ionic zinc onto
org/10.1016/j.envpo​l.2017.06.064 the alfalfa plants symbiotically associated with Sinorhizobium
Amooaghaie R, Norouzi M, Saeri M (2017) Impact of zinc and zinc meliloti in soil. Sci Total Environ 515–516:60–69. https​://doi.
oxide nanoparticles on the physiological and biochemical pro- org/10.1016/j.scito​tenv.2015.02.014
cesses in tomato and wheat. Botany 95:441–455. https​://doi. Barbasz A, Kreczmer B, Oćwieja M (2016) Effects of exposure of
org/10.1139/cjb-2016-0194 callus cells of two wheat varieties to silver nanoparticles and
Ananda S, Shobha G, Shashidhara KS, Mahadimane V (2019) Nano- silver salt (AgNO3). Acta Physiol Plant 38(3):76. https​://doi.
cuprous oxide enhances seed germination and seedling growth in org/10.1007/s1173​8-016-2092-z
Lycopersicum esculentum plants. J Drug Deliv Ther 9:296–302. Barrios AC, Rico CM, Trujillo-Reyes J et al (2016) Effects of uncoated
https​://doi.org/10.22270​/jddt.v9i2.2554 and citric acid coated cerium oxide nanoparticles, bulk cerium
Andersen CP, King G, Plocher M et al (2016) Germination and early oxide, cerium acetate, and citric acid on tomato plants. Sci
plant development of ten plant species exposed to titanium Total Environ 563–564:956–964. https​://doi.org/10.1016/j.scito​
dioxide and cerium oxide nanoparticles. Environ Toxicol Chem tenv.2015.11.143
35:2223–2229. https​://doi.org/10.1002/etc.3374 Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055–
Ansari MA, Khan HM, Khan AA et al (2014) Interaction of silver nan- 1066. https​://doi.org/10.1105/tpc.9.7.1055
oparticles with Escherichia coli and their cell envelope biomol- Bidhendi AJ, Geitmann A (2016) Relating the mechanics of the pri-
ecules. J Basic Microbiol 54:905–915. https​://doi.org/10.1002/ mary plant cell wall to morphogenesis. J Exp Bot 67:449–461.
jobm.20130​0457 https​://doi.org/10.1093/jxb/erv53​5
Arif N, Yadav V, Singh S et al (2018) Interaction of copper oxide Bolyard SC, Reinhart DR, Santra S (2013) Behavior of engineered
nanoparticles with plants: uptake, accumulation, and toxicity. nanoparticles in landfill leachate. Environ Sci Technol 47:8114–
Nanomater Plants Algae Microorgan. https​://doi.org/10.1016/ 8122. https​://doi.org/10.1021/es305​175e
B978-0-12-81148​7-2.00013​-X Bonilla-Bird NJ, Paez A, Reyes A et al (2018) Two-photon microscopy
Asztemborska M, Steborowski R, Kowalska J, Bystrzejewska- and spectroscopy studies to determine the mechanism of copper
Piotrowska G (2015) Accumulation of aluminium by plants oxide nanoparticle uptake by sweetpotato roots during posthar-
exposed to nano-and microsized particles of Al2O3. Int J Environ vest treatment. Environ Sci Technol 52:9954–9963. https​://doi.
Res 9:109–116. https​://doi.org/10.22059​/ijer.2015.880 org/10.1021/acs.est.8b027​94
Atha DH, Wang H, Petersen EJ et al (2012) Copper oxide nanoparticle Botta C, Labille J, Auffan M et al (2011) TiO2-based nanoparticles
mediated DNA damage in terrestrial plant models. Environ Sci released in water from commercialized sunscreens in a life-cycle
Technol 46:1819–1827. https​://doi.org/10.1021/es202​660k perspective: Structures and quantities. Environ Pollut 159:1543–
Aubert T, Burel A, Esnault MA et al (2012) Root uptake and phyto- 1550. https​://doi.org/10.1016/j.envpo​l.2011.03.003
toxicity of nanosized molybdenum octahedral clusters. J Haz- Boyes WK (2018) Safety assessment of nanotechnology products
ard Mater 219–220:111–118. https​://doi.org/10.1016/j.jhazm​ comprehensive toxicology, 3rd Edition. Elesiver, Amsterdam, pp
at.2012.03.058

13
Environmental Chemistry Letters (2021) 19:1545–1609 1599

34–43. Doi: https:​ //doi.org/10.1016/B978-0-12-801238​ -3.99179​ Contini C, Schneemilch M, Gaisford S, Quirke N (2018) Nanoparti-
-7 cle–membrane interactions. J Exp Nanosci 13:62–81. https:​ //doi.
Brar SK, Verma M, Tyagi RD, Surampalli RY (2010) Engineered nano- org/10.1080/17458​080.2017.14132​53
particles in wastewater and wastewater sludge - Evidence and Conway JR, Beaulieu AL, Beaulieu NL et al (2015) Environmental
impacts. Waste Manag 30:504–520. https​://doi.org/10.1016/j. stresses increase photosynthetic disruption by metal oxide nano-
wasma​n.2009.10.012 materials in a soil-grown plant. ACS Nano 9:11737–11749. https​
Brown J (2017) Impact of silver nanoparticles on wastewater treat- ://doi.org/10.1021/acsna​no.5b030​91
ment. Giusy L, Giovanni L, Jeanette B (2017) Nanotechnologies Cornelis G, Hund-Rinke K, Kuhlbusch T et al (2014a) Fate and Bio-
for environmental remediation: applications and implications. availability of Engineered Nanoparticles in Soils: A Review,
Springer, Cham, pp 255–267. https:​ //doi.org/10.1007/978-3-319- Interactions within natural soils have often been neglected-
53162​-5_9 when assessing fate and bioavailability of engineered nanoma-
Brunetti G, Donner E, Laera G et al (2015) Fate of zinc and silver engi- terials (ENM) in soils. This review combines patchwise ENM
neered nanoparticles in sewerage networks. Water Res 77:72–84. resea. Crit Rev Environ Sci Technol 44:2720–2764. https​://doi.
https​://doi.org/10.1016/j.watre​s.2015.03.003 org/10.1080/10643​389.2013.82976​7
Burklew CE, Ashlock J, Winfrey WB, Zhang B (2012) Effects of alu- Cornelis G, Hund-Rinke K, Kuhlbusch T et al (2014b) Fate and
minum oxide nanoparticles on the growth, development, and bioavailability of engineered nanoparticles in soils: a review.
microrna expression of tobacco (Nicotiana tabacum). PLoS ONE Crit Rev Environ Sci Technol 44:2720–2764. https ​ : //doi.
7(5):e34783. https​://doi.org/10.1371/journ​al.pone.00347​83 org/10.1080/10643​389.2013.82976​7
Burman U, Kumar P (2018) Plant Response to Engineered Nanopar- Cornelis G, Ryan B, McLaughlin MJ et al (2011) Solubility and batch
ticles Nanomaterials in Plants, Algae, and Microorganisms. retention of CeO2 nanoparticles in soils. Environ Sci Technol
Elseiver, Amsterdam, pp 103–118. https:​ //doi.org/10.1016/B978- 45:2777–2782. https​://doi.org/10.1021/es103​769k
0-12-81148​7-2.00005​-0 Corredor E, Testillano PS, Coronado MJ et al (2009) Nanoparticle
Cao XF, Liu LP (2016) Ecological toxicity of engineered nano materi- penetration and transport in living pumpkin plants: In situ sub-
als to the organisms in the environment. In: Material science and cellular identification. BMC Plant Biol 9(1):45. https​://doi.
environmental engineering - proceedings of the 3rd annual 2015 org/10.1186/1471-2229-9-45
international conference on material science and environmental Da Costa MVJ, Sharma PK (2016) Effect of copper oxide nanopar-
engineering, ICMSEE 2015, pp 335–338 ticles on growth, morphology, photosynthesis, and antioxidant
Capaldi Arruda SC, Diniz Silva AL, Moretto Galazzi R et al (2015) response in Oryza sativa. Photosynthetica 54:110–119. https​://
Nanoparticles applied to plant science: a review. Talanta doi.org/10.1007/s1109​9-015-0167-5
131:693–705. https​://doi.org/10.1016/j.talan​ta.2014.08.050 Cox A, Venkatachalam P, Sahi S, Sharma N (2017) Reprint of: Silver
Castiglione MR, Giorgetti L, Geri C, Cremonini R (2011) The effects and titanium dioxide nanoparticle toxicity in plants: a review of
of nano-TiO2 on seed germination, development and mito- current research. Plant Physiol Biochem 110:33–49. https​://doi.
sis of root tip cells of Vicia narbonensis L. and Zea mays L. J org/10.1016/j.plaph​y.2016.05.022
Nanoparticle Res 13:2443–2449. https​://doi.org/10.1007/s1105​ Cross RK, Tyler C, Galloway TS (2015) Transformations that affect
1-010-0135-8 fate, form and bioavailability of inorganic nanoparticles in
Cendrowski K, Sikora P, Zielinska B et al (2017) Chemical and ther- aquatic sediments. Environ Chem 12:627–642. https​: //doi.
mal stability of core-shelled magnetite nanoparticles and solid org/10.1071/EN142​73
silica. Appl Surf Sci 407:391–397. https​://doi.org/10.1016/j. Cui D, Zhang P, Ma Y et al (2014) Effect of cerium oxide nanoparticles
apsus​c.2017.02.118 on asparagus lettuce cultured in an agar medium. Environ Sci
Chakraborty S, Nair A, Paliwal M et al (2018) Exposure media a criti- Nano 1:459–465. https​://doi.org/10.1039/c4en0​0025k​
cal factor for controlling dissolution of CuO nanoparticles. J Cvjetko P, Milošić A, Domijan AM et al (2017) Toxicity of silver ions
Nanoparticle Res 20(12):331. https​://doi.org/10.1007/s1105​ and differently coated silver nanoparticles in Allium cepa roots.
1-018-4428-7 Ecotoxicol Environ Saf 137:18–28. https​://doi.org/10.1016/j.
Chen M, Xu N, Christodoulatos C, Wang D (2018) Synergistic effects ecoen​v.2016.11.009
of phosphorus and humic acid on the transport of anatase tita- Das P, Barua S, Sarkar S et al (2018) Mechanism of toxicity and trans-
nium dioxide nanoparticles in water-saturated porous media. formation of silver nanoparticles: Inclusive assessment in earth-
Environ Pollut 243:1368–1375. https​://doi.org/10.1016/j.envpo​ worm-microbe-soil-plant system. Geoderma 314:73–84. https​://
l.2018.09.106 doi.org/10.1016/j.geode​rma.2017.11.008
Chhipa H (2017) Nanofertilizers and nanopesticides for agriculture. Das K, Roychoudhury A (2014) Reactive oxygen species (ROS)
Environ Chem Lett 15(1):15–22. https​://doi.org/10.1007/s1031​ and response of antioxidants as ROS-scavengers during envi-
1-016-0600-4 ronmental stress in plants. Front Environ Sci 2:53. https​://doi.
Chichiriccò G, Poma A (2015) Penetration and toxicity of nanoma- org/10.3389/fenvs​.2014.00053​
terials in higher plants. Nanomaterials 5:851–873. https​://doi. Dasgupta N, Ranjan S, Ramalingam C (2017) Applications of nano-
org/10.3390/nano5​02085​1 technology in agriculture and water quality management. Envi-
Chung IM, Rekha K, Venkidasamy B, Thiruvengadam M (2019a) ron Chem Lett 15(4):591–605. https​://doi.org/10.1007/s1031​
Effect of copper oxide nanoparticles on the physiology, bioac- 1-017-0648-9
tive molecules, and transcriptional changes in Brassica rapa ssp. De A, Chakrabarti M, Ghosh I, Mukherjee A (2016) Evaluation of
rapa Seedlings. Water Air Soil Pollut. https​://doi.org/10.1007/ genotoxicity and oxidative stress of aluminium oxide nanoparti-
s1127​0-019-4084-2 cles and its bulk form in Allium cepa. Nucl 59:219–225. https​://
Chung IM, Rekha K, Venkidasamy B, Thiruvengadam M (2019b) doi.org/10.1007/s1323​7-016-0179-y
Effect of copper oxide nanoparticles on the physiology, bioactive De La Torre RR, Pagano L, Majumdar S et al (2018) Co-exposure
molecules, and transcriptional changes in Brassica rapa ssp. rapa of imidacloprid and nanoparticle Ag or CeO2 to Cucurbita
Seedlings. Water Air Soil Pollut 230:48. https:​ //doi.org/10.1007/ pepo (zucchini): Contaminant bioaccumulation and transloca-
s1127​0-019-4084-2 tion. NanoImpact 11:136–145. https​://doi.org/10.1016/j.impac​
t.2018.07.001

13
1600 Environmental Chemistry Letters (2021) 19:1545–1609

Dev A, Srivastava AK, Karmakar S (2018) Nanomaterial toxicity for Faisal M, Saquib Q, Alatar AA et al (2013) Phytotoxic hazards of NiO-
plants. Environ Chem Lett 16:85–100. https​://doi.org/10.1007/ nanoparticles in tomato: a study on mechanism of cell death. J
s1031​1-017-0667-6 Hazard Mater 250–251:318–332. https:​ //doi.org/10.1016/j.jhazm​
Dhoke SK, Mahajan P, Kamble R, Khanna A (2013) Effect of nanopar- at.2013.01.063
ticles suspension on the growth of mung (Vigna radiata) seed- Faisal M, Saquib Q, Alatar AA et al (2016) Cobalt oxide nanoparticles
lings by foliar spray method. Nanotechnol Dev 3(1):e1. https​:// aggravate DNA damage and cell death in eggplant via mitochon-
doi.org/10.4081/nd.2013.e1 drial swelling and NO signaling pathway. Biol Res 49(1):20.
Dimkpa CO, Latta DE, McLean JE et al (2013) Fate of CuO and ZnO https​://doi.org/10.1186/s4065​9-016-0080-9
nano- and microparticles in the plant environment. Environ Sci Faisal M, Saquib Q, Alatar AA, Al-Khedhairy AA (2018). Phytotox
Technol 47:4734–4742. https​://doi.org/10.1021/es304​736y Nnanopart. https​://doi.org/10.1007/978-3-319-76708​-6
Dimkpa CO, McLean JE, Britt DW, Anderson AJ (2015) Nano-CuO Falco WF, Scherer MD, Oliveira SL et al (2020) Phytotoxicity of silver
and interaction with nano-ZnO or soil bacterium provide evi- nanoparticles on Vicia faba: evaluation of particle size effects
dence for the interference of nanoparticles in metal nutrition of on photosynthetic performance and leaf gas exchange. Sci Total
plants. Ecotoxicology 24:119–129. https:​ //doi.org/10.1007/s1064​ Environ. https​://doi.org/10.1016/j.scito​tenv.2019.13481​6
6-014-1364-x Fayiga A (2017) Nanoparticles in biosolids: effect on soil health and
Dimkpa CO, McLean JE, Latta DE et al (2012) CuO and ZnO nanopar- crop growth. Peertechz J Environ Sci Toxicol 2:059–067. https​
ticles: phytotoxicity, metal speciation, and induction of oxidative ://doi.org/10.17352​/pjest​.00001​3
stress in sand-grown wheat. J Nanoparticle Res 14(9):1125. https​ Feizi H, Rezvani Moghaddam P, Shahtahmassebi N, Fotovat A (2012)
://doi.org/10.1007/s1105​1-012-1125-9 Impact of bulk and nanosized titanium dioxide (TiO2) on wheat
Dimkpa CO, Singh U, Bindraban PS et al (2018) Exposure to weath- seed germination and seedling growth. Biol Trace Elem Res
ered and fresh nanoparticle and ionic Zn in soil promotes grain 146:101–106. https​://doi.org/10.1007/s1201​1-011-9222-7
yield and modulates nutrient acquisition in wheat (Triticum Fellmann S, Eichert T (2017) Acute effects of engineered nanoparticles
aestivum L.). J Agric Food Chem 66:9645–9656. https​://doi. on the growth and gas exchange of Zea mays L.—What are the
org/10.1021/acs.jafc.8b038​40 underlying causes? Water Air Soil Pollut 228(5):1–3. https​://doi.
Dimkpa CO, White JC, Elmer WH, Gardea-Torresdey J (2017) Nano- org/10.1007/s1127​0-017-3364-y
particle and ionic Zn promote nutrient loading of sorghum grain Frazier TP, Burklew CE, Zhang B (2014) Titanium dioxide nanopar-
under low NPK fertilization. J Agric Food Chem 65:8552–8559. ticles affect the growth and microRNA expression of tobacco
https​://doi.org/10.1021/acs.jafc.7b029​61 (Nicotiana tabacum). Funct Integr Genomics 14:75–83. https​://
Driouich A, Follet-Gueye ML, Vicré-Gibouin M, Hawes M (2013) doi.org/10.1007/s1014​2-013-0341-4
Root border cells and secretions as critical elements in plant Fry SC (2011) Plant cell walls From chemistry to biology. Ann Bot
host defense. Curr Opin Plant Biol 16:489–495. https​://doi. 108:8–9. https​://doi.org/10.1093/aob/mcr12​8
org/10.1016/j.pbi.2013.06.010 Galway ME (2006) Root hair cell walls: Filling in the framework. Can
Du W, Gardea-Torresdey JL, Xie Y et al (2017) Elevated CO2 lev- J Bot 84:613–621. https​://doi.org/10.1139/B06-006
els modify TiO2 nanoparticle effects on rice and soil micro- Gankanda A, Cwiertny DM, Grassian VH (2016) Role of atmospheric
bial communities. Sci Total Environ 578:408–416. https​://doi. CO2 and H2O adsorption on ZnO and CuO nanoparticle aging:
org/10.1016/j.scito​tenv.2016.10.197 formation of new surface phases and the impact on nanoparticle
Du W, Sun Y, Ji R et al (2011) TiO2 and ZnO nanoparticles negatively dissolution. J Phys Chem C 120(34):19195–19203. https​://doi.
affect wheat growth and soil enzyme activities in agricultural org/10.1021/acs.jpcc.6b059​31
soil. J Environ Monit 13:822–828. https:​ //doi.org/10.1039/c0em0​ Gao X, Avellan A, Laughton S et al (2018) CuO nanoparticle dissolu-
0611d​ tion and toxicity to wheat (Triticum aestivum) in rhizosphere soil.
Du W, Tan W, Peralta-Videa JR et al (2017) Interaction of metal oxide Environ Sci Technol 52:2888–2897. https​://doi.org/10.1021/acs.
nanoparticles with higher terrestrial plants: physiological and est.7b058​16
biochemical aspects. Plant Physiol Biochem 110:210–225. https​ Gao X, Spielman-Sun E, Rodrigues SM et al (2017) Time and nano-
://doi.org/10.1016/j.plaph​y.2016.04.024 particle concentration affect the extractability of Cu from CuO
Duran NM, Medina-Llamas M, Cassanji JGB et al (2018) Bean seed- NP-amended soil. Environ Sci Technol 51:2226–2234. https​://
ling growth enhancement using magnetite nanoparticles. J doi.org/10.1021/acs.est.6b047​05
Agric Food Chem 66:5746–5755. https​://doi.org/10.1021/acs. García A, Espinosa R, Delgado L et al (2011) Acute toxicity of
jafc.8b005​57 cerium oxide, titanium oxide and iron oxide nanoparticles
Dwivedi AD, Dubey SP, Sillanpää M et al (2015) Fate of engineered using standardized tests. Desalination 269:136–141. https​://doi.
nanoparticles: implications in the environment. Coord Chem Rev org/10.1016/j.desal​.2010.10.052
287:64–78. https​://doi.org/10.1016/j.ccr.2014.12.014 García-Gómez C, García S, Obrador AF et al (2018) Effects of aged
Ebbs SD, Bradfield SJ, Kumar P et al (2016) Accumulation of zinc, ZnO NPs and soil type on Zn availability, accumulation and
copper, or cerium in carrot (Daucus carota) exposed to metal toxicity to pea and beet in a greenhouse experiment. Ecotoxi-
oxide nanoparticles and metal ions. Environ Sci Nano 3:114– col Environ Saf 160:222–230. https​://doi.org/10.1016/j.ecoen​
126. https​://doi.org/10.1039/c5en0​0161g​ v.2018.05.019
Eduok S, Coulon F (2017) Engineered nanoparticles in the environ- García-Gómez C, Obrador A, González D et al (2017) Comparative
ments: Interactions with microbial systems and microbial activ- effect of ZnO NPs, ZnO bulk and ZnSO4 in the antioxidant
ity. Microb Ecotoxicol. https:​ //doi.org/10.1007/978-3-319-61795​ defences of two plant species growing in two agricultural soils
-4_5 under greenhouse conditions. Sci Total Environ 589:11–24. https​
Eduok S, Hendry C, Ferguson R et al (2015) Insights into the effect of ://doi.org/10.1016/j.scito​tenv.2017.02.153
mixed engineered nanoparticles on activated sludge performance. García-Gómez C, Obrador A, González D et al (2018) Comparative
FEMS Microbiol Ecol. https​://doi.org/10.1093/femse​c/fiv08​2 study of the phytotoxicity of ZnO nanoparticles and Zn accu-
Eichert T, Goldbach HE (2008) Equivalent pore radii of hydrophilic mulation in nine crops grown in a calcareous soil and an acidic
foliar uptake routes in stomatous and astomatous leaf surfaces soil. Sci Total Environ 644:770–780. https​://doi.org/10.1016/j.
- further evidence for a stomatal pathway. Physiol Plant 132:491– scito​tenv.2018.06.356
502. https​://doi.org/10.1111/j.1399-3054.2007.01023​.x

13
Environmental Chemistry Letters (2021) 19:1545–1609 1601

García-Sánchez S, Bernales I, Cristobal S (2015) Early response to PLoS ONE 10(8):e0134261. https ​ : //doi.org/10.1371/journ​
nanoparticles in the Arabidopsis transcriptome compromises al.pone.01342​61
plant defence and root-hair development through salicylic acid Gunsolus IL, Mousavi MPS, Hussein K et al (2015) Effects of humic
signalling. BMC Genomics 16(1):1–7. https​://doi.org/10.1186/ and fulvic acids on silver nanoparticle stability, dissolution, and
s1286​4-015-1530-4 toxicity. Environ Sci Technol 49(13):8078–8086. https​://doi.
Geisler-Lee J, Wang Q, Yao Y et al (2013) Phytotoxicity, accumula- org/10.1021/acs.est.5b014​96
tion and transport of silver nanoparticles by Arabidopsis thali- Gómez-Sagasti MT, Epelde L, Anza M et al (2019) The impact of
ana. Nanotoxicology 7:323–337. https​://doi.org/10.3109/17435​ nanoscale zero-valent iron particles on soil microbial communi-
390.2012.65809​4 ties is soil dependent. J Hazard Mater 364:591–599. https​://doi.
Gelabert A, Sivry Y, Ferrari R et al (2014) Uncoated and coated ZnO org/10.1016/j.jhazm​at.2018.10.034
nanoparticle life cycle in synthetic seawater. Environ Toxicol Han L, Cheng S, Zhuang G et al (2015) The changes and long-range
Chem 33(2):341–349. https​://doi.org/10.1002/etc.2447 transport of PM2.5 in Beijing in the past decade. Atmos Environ
Gentile A, Ruffino F, Grimaldi MG (2016) Complex-morphology 110:186–195. https​://doi.org/10.1016/j.atmos​env.2015.03.013
metal-based nanostructures: Fabrication, characterization, and Hawthorne J, De La Torre RR, Xing B et al (2014) Particle-size
applications. Nanomaterials 6(6):110. https​://doi.org/10.3390/ dependent accumulation and trophic transfer of cerium oxide
nano6​06011​0 through a terrestrial food chain. Environ Sci Technol 48:13102–
Getnet Z, Husen A, Fetene M, Yemata G (2015) Growth, water status, 13109. https​://doi.org/10.1021/es503​792f
physiological, biochemical and yield response of stay green sor- Hayyan M, Hashim MA, Alnashef IM (2016) Superoxide ion: genera-
ghum (Sorghum bicolor (L.) moench) varieties-a field trial under tion and chemical implications. Chem Rev 116:3029–3085. https​
drought-prone area in Amhara Regional State. Ethiopia J Agron ://doi.org/10.1021/acs.chemr​ev.5b004​07
14:188–202. https​://doi.org/10.3923/ja.2015.188.202 Hernandez-Viezcas JA, Castillo-Michel H, Andrews JC et al (2013)
Ghosh M, Bhadra S, Adegoke A et al (2015) MWCNT uptake in In situ synchrotron X-ray fluorescence mapping and speciation of
Allium cepa root cells induces cytotoxic and genotoxic responses CeO 2 and ZnO nanoparticles in soil cultivated soybean (Glycine
and results in DNA hyper-methylation. Mutat Res - Fundam Mol max). ACS Nano 7:1415–1423. https​://doi.org/10.1021/nn305​
Mech Mutagen 774:49–58. https​://doi.org/10.1016/j.mrfmm​ 196q
m.2015.03.004 Hernandez-Viezcas JA, Castillo-Michel H, Servin AD et al (2011)
Ghosh M, Ghosh I, Godderis L et al (2019) Genotoxicity of engi- Spectroscopic verification of zinc absorption and distribution
neered nanoparticles in higher plants. Mutat Res - Genet Toxicol in the desert plant Prosopis juliflora-velutina (velvet mesquite)
Environ Mutagen 842:132–145. https​://doi.org/10.1016/j.mrgen​ treated with ZnO nanoparticles. Chem Eng J 170:346–352. https​
tox.2019.01.002 ://doi.org/10.1016/j.cej.2010.12.021
Ghosh M, Jana A, Sinha S et al (2016) Effects of ZnO nanoparticles Hillaireau H (2016) Investigating interactions between nanoparticles
in plants: cytotoxicity, genotoxicity, deregulation of antioxi- and cells: internalization and intracellular trafficking. In: Vauth-
dant defenses, and cell-cycle arrest. Mutat Res - Genet Toxicol ier C, Ponchel G (eds) Polymer nanoparticles for nanomedicines.
Environ Mutagen 807:25–32. https​://doi.org/10.1016/j.mrgen​ Springer, Cham. https​://doi.org/10.1007/978-3-319-41421​-8_10
tox.2016.07.006 Hirano T, Kiyota M, Kitaya Y, Aiga I (1990) The physical effects of
Ghosh I, Mukherjee A, Mukherjee A (2017) In planta genotoxicity of dust on photosynthetic rate of plant leaves. J Agric Meteorol
nZVI: influence of colloidal stability on uptake, DNA damage, 46:1–7. https​://doi.org/10.2480/agrme​t.46.1
oxidative stress and cell death. Mutagenesis 32:371–387. https​ Holz M, Leue M, Ahmed MA et al (2018) Spatial distribution of
://doi.org/10.1093/mutag​e/gex00​6 mucilage in the rhizosphere measured with infrared spectros-
Giese B, Klaessig F, Park B et al (2018) Risks, release and concentra- copy. Front Environ Sci 6:87. https​: //doi.org/10.3389/fenvs​
tions of engineered nanomaterial in the environment. Sci Rep .2018.00087​
8(1):1–8. https​://doi.org/10.1038/s4159​8-018-19275​-4 Hong J, Peralta-Videa JR, Rico C et al (2014) Evidence of translocation
Glenn JB, White SA, Klaine SJ (2012) Interactions of gold nanopar- and physiological impacts of foliar applied CeO2 nanoparticles
ticles with freshwater aquatic macrophytes are size and species on cucumber (Cucumis sativus) plants. Environ Sci Technol
dependent. Environ Toxicol Chem 31:194–201. https​://doi. 48:4376–4385. https​://doi.org/10.1021/es404​931g
org/10.1002/etc.728 Hong J, Rico CM, Zhao L et al (2015) Toxic effects of copper-based
Global Nanotechnology Market Outlook 2024. (2020). Retrieved on nanoparticles or compounds to lettuce (Lactuca sativa) and
May 12, 2020 from https:​ //www.prnews​ wire.​ com/news-releas​ es/ alfalfa (Medicago sativa). Environ Sci Process Impacts 17:177–
globa​l-nanot​echno​logy-marke​t-outlo​ok-2024-30092​4265.html 185. https​://doi.org/10.1039/c4em0​0551a​
Gong N, Shao K, Feng W et al (2011) Biotoxicity of nickel oxide nano- Hong J, Wang L, Sun Y et al (2016) Foliar applied nanoscale and
particles and bio-remediation by microalgae Chlorella vulgaris. microscale CeO2 and CuO alter cucumber (Cucumis sativus)
Chemosphere 83(4):510–516. https​://doi.org/10.1016/j.chemo​ fruit quality. Sci Total Environ 563–564:904–911. https​://doi.
spher​e.2010.12.059 org/10.1016/j.scito​tenv.2015.08.029
Gopalakrishnan Nair PM, Kim SH, Chung IM (2014) Copper oxide Hong F, Zhou J, Liu C et al (2005) Effect of Nano-TiO2 on photo-
nanoparticle toxicity in mung bean (Vigna radiata L.) seed- chemical reaction of chloroplasts of spinach. Biol Trace Elem
lings: physiological and molecular level responses of in vitro Res 105:269–279. https​://doi.org/10.1385/BTER:105:1-3:269
grown plants. Acta Physiol Plant 36:2947–2958. https​://doi. Horst WJ, Wang Y, Eticha D (2010) The role of the root apoplast in
org/10.1007/s1173​8-014-1667-9 aluminium-induced inhibition of root elongation and in alumin-
Gottschalk F, Nowack B (2011) The release of engineered nanomateri- ium resistance of plants: a review. Ann Bot 106:185–197. https​
als to the environment. J Environ Monit 13(5):1145–1155 ://doi.org/10.1093/aob/mcq05​3
Gottschalk F, Sonderer T, Scholz RW, Nowack B (2009) Modeled envi- Hossain Z, Mustafa G, Sakata K, Komatsu S (2016) Insights into the
ronmental concentrations of engineered nanomaterials (TiO2, proteomic response of soybean towards Al2O3, ZnO, and Ag
ZnO, Ag, CNT, fullerenes) for different regions. Environ Sci nanoparticles stress. J Hazard Mater 304:291–305. https​://doi.
Technol 43:9216–9222. https​://doi.org/10.1021/es901​5553 org/10.1016/j.jhazm​at.2015.10.071
Gui X, Zhang Z, Liu S et al (2015) Fate and phytotoxicity of CeO2
nanoparticles on lettuce cultured in the potting soil environment.

13
1602 Environmental Chemistry Letters (2021) 19:1545–1609

Huang J (1986) Ultrastructure of bacterial penetration in plants. Annu Kasana RC, Panwar NR, Kaul RK, Kumar P (2017) Biosynthesis and
Rev Phytopathol 24:141–157. https​://doi.org/10.1146/annur​ effects of copper nanoparticles on plants. Environ Chem Lett
ev.py.24.09018​6.00104​1 15(2):233–240. https​://doi.org/10.1007/s1031​1-017-0615-5
Huangfu X, Wang Y, Liu Y et al (2014) Effects of humic acid and Keller AA, Huang Y, Nelson J (2018) Detection of nanoparticles in
surfactants on the aggregation kinetics of manganese dioxide col- edible plant tissues exposed to nano-copper using single-particle
loids. Front Environ Sci Eng 9:105–111. https:​ //doi.org/10.1007/ ICP-MS. J Nanoparticle Res 20(4):101. https​://doi.org/10.1007/
s1178​3-014-0726-1 s1105​1-018-4192-8
Hussain HI, Yi Z, Rookes JE et al (2013) Mesoporous silica nanopar- Keller AA, Lazareva A (2013) Predicted releases of engineered nano-
ticles as a biomolecule delivery vehicle in plants. J Nanoparticle materials: from global to regional to local. Environ Sci Technol
Res 15(6):1676. https​://doi.org/10.1007/s1105​1-013-1676-4 Lett 1:65–70. https​://doi.org/10.1021/ez400​106t
Iswarya V, Bhuvaneshwari M, Alex SA et al (2015) Combined toxicity Keller AA, McFerran S, Lazareva A, Suh S (2013) Global life cycle
of two crystalline phases (anatase and rutile) of Titania nanopar- releases of engineered nanomaterials. J Nanoparticle Res
ticles towards freshwater microalgae: Chlorella sp. Aquat Toxicol 15(6):1692. https​://doi.org/10.1007/s1105​1-013-1692-4
161:154–169. https​://doi.org/10.1016/j.aquat​ox.2015.02.006 Kent RD, Vikesland PJ (2016) Dissolution and persistence of copper-
Jahan S, Alias YB, Bakar AFBA, Bin YI (2018) Toxicity evaluation based nanomaterials in undersaturated solutions with respect to
of ZnO and TiO2 nanomaterials in hydroponic red bean (Vigna cupric solid phases. Environ Sci Technol 50(13):6772–6781.
angularis) plant: Physiology, biochemistry and kinetic transport. https​://doi.org/10.1021/acs.est.5b047​19
J Environ Sci (China) 72:140–152. https​://doi.org/10.1016/j. Khan US, Amanullah MA et al (2015) Transformation mechanism of
jes.2017.12.022 magnetite nanoparticles. Mater Sci Pol 33:278–285. https​://doi.
Jampílek J, Kráľová K (2019) Impact of nanoparticles on photosyn- org/10.1515/msp-2015-0037
thesizing organisms and their use in hybrid structures with some Khodakovskaya MV, Kim BS, Kim JN et al (2013) Carbon nanotubes
components of photosynthetic apparatus. In: Prasad R (eds) Plant as plant growth regulators: effects on tomato growth, reproduc-
Nanobionics. Nanotechnology in the Life Sciences. Springer, tive system, and soil microbial community. Small 9:115–123.
Cham, pp 255–332. https​://doi.org/10.1007/978-3-030-12496​ https​://doi.org/10.1002/smll.20120​1225
-0_11 Khodakovskaya MV, De Silva K, Biris AS et al (2012) Carbon nano-
Jha S, Pudake RN (2016) Molecular mechanism of plant-nanoparticle tubes induce growth enhancement of tobacco cells. ACS Nano
interactions. In: Chittaranjan Kole D, Sakthi K, Mariya VK (eds) 6:2128–2135. https​://doi.org/10.1021/nn204​643g
Plant Nanotechnology: Principles and Practices. Springer, Cham. Kim S, Kim J, Lee I (2011) Effects of Zn and ZnO nanoparticles
https​://doi.org/10.1007/978-3-319-42154​-4_7 and zn2+ on soil enzyme activity and bioaccumulation of
Jhanzab HM, Razzaq A, Bibi Y et al (2019) Proteomic analysis of the Zn in Cucumis sativus. Chem Ecol 27:49–55. https​: //doi.
effect of inorganic and organic chemicals on silver nanoparticles org/10.1080/02757​540.2010.52907​4
in wheat. Int J Mol Sci 20(4):825. https​://doi.org/10.3390/ijms2​ Kim JH, Lee Y, Kim EJ et al (2014) Exposure of iron nanoparticles to
00408​25 Arabidopsis thaliana enhances root elongation by triggering cell
Ji Y, Zhou Y, Ma C et al (2017) Jointed toxicity of TiO2 NPs and wall loosening. Environ Sci Technol 48:3477–3485. https​://doi.
Cd to rice seedlings: NPs alleviated Cd toxicity and Cd pro- org/10.1021/es404​3462
moted NPs uptake. Plant Physiol Biochem 110:82–93. https​:// Kittler S, Greulich C, Diendorf J et al (2010) Toxicity of silver nano-
doi.org/10.1016/j.plaph​y.2016.05.010 particles increases during storage because of slow dissolution
Jian LY, Ya YL, Yue JZ et al (2008) Cell wall polysaccharides are under release of silver ions. Chem Mater 22(16):4548–4554.
specifically involved in the exclusion of aluminum from the rice https​://doi.org/10.1021/cm100​023p
root apex. Plant Physiol 146:602–611. https​://doi.org/10.1104/ Kole C, Kole P, Randunu KM et al (2013) Nanobiotechnology can
pp.107.11198​9 boost crop production and quality: First evidence from increased
Jiang C, Aiken GR, Hsu-Kim H (2015) Effects of natural organic plant biomass, fruit yield and phytomedicine content in bitter
matter properties on the dissolution kinetics of zinc oxide nano- melon (Momordica charantia). BMC Biotechnol 13(1):37. https​
particles. Environ Sci Technol 49:11476–11484. https​://doi. ://doi.org/10.1186/1472-6750-13-37
org/10.1021/acs.est.5b024​06 Kopittke PM, Blamey FPC, Menzies NW (2008) Toxicities of soluble
Jiang HS, Yin LY, Ren NN et al (2017) Silver nanoparticles induced Al, Cu, and la include ruptures to rhizodermal and root cortical
reactive oxygen species via photosynthetic energy transport cells of cowpea. Plant Soil 303:217–227. https:​ //doi.org/10.1007/
imbalance in an aquatic plant. Nanotoxicology 11:157–167. https​ s1110​4-007-9500-5
://doi.org/10.1080/17435​390.2017.12788​02 Korotkova AM, Lebedev SV, Kayumov FG, Sizova EA (2017) The
John AC, Küpper M, Manders-Groot AMM et al (2017) Emissions and influence metal nanoparticles (Fe, Cu, Ni) and their oxides
possible environmental Implication of engineered nanomaterials (Fe3O4, CuO, NiO). Sel’skokhozyaistvennaya Biol 52:172–182.
(ENMs) in the atmosphere. Atmosphere (Basel) 8(5):84. https​:// https​://doi.org/10.15389​/agrob​iolog​y.2017.1.172en​g
doi.org/10.3390/atmos​80500​84 Kulizhskiy SP, Loiko SV, Morgalev YN et al (2017) Investigation of
Jorge de Souza TA, Rosa Souza LR, Franchi LP (2019) Silver nano- Platinum and Nickel Nanoparticles Migration and Accumula-
particles: an integrated view of green synthesis methods, trans- tion in Soils within the Southeastern Part of West Siberia. Nano
formation in the environment, and toxicity. Ecotoxicol Environ Hybrids Compos 13:115–122. https​://doi.org/10.4028/www.
Saf 171:691–700. https​://doi.org/10.1016/j.ecoen​v.2018.12.095 scien​tific​.net/nhc.13.115
Ju-Nam Y, Lead J (2016) Properties, sources, pathways, and fate of Kumar P, Al-Dabbous AN (2016) Emission, transformation, and
nanoparticles in the Environment. In: Engineered nanoparticles fate of nanoparticles in the atmosphere. Eng Nanopart Environ
and the environment: biophysicochemical processes and toxicity. Biophysicochem Processes Toxicity 29:205–223. https​://doi.
pp 95–117. https​://doi.org/10.1002/97811​19275​855.ch6 org/10.1002/97811​19275​855.ch11
Karami Mehrian S, De Lima R (2016) Nanoparticles cyto and geno- Kumar N, Tripathi P, Nara S (2018) Gold nanomaterials to plants:
toxicity in plants: Mechanisms and abnormalities. Environ impact of bioavailability, particle size, and surface coating. In:
Nanotechnol Monit Manag 6:184–193. https:​ //doi.org/10.1016/j. Nanomaterials in plants, algae, and microorganisms. Academic
enmm.2016.08.003 Press, pp 195–220. https​://doi.org/10.1016/B978-0-12-81148​
7-2.00009​-8

13
Environmental Chemistry Letters (2021) 19:1545–1609 1603

Kumari M, Khan SS, Pakrashi S et al (2011) Cytogenetic and genotoxic Liu J, Pennell KG, Hurt RH (2011) Kinetics and mechanisms of
effects of zinc oxide nanoparticles on root cells of Allium cepa. nanosilver oxysulfidation. Environ Sci Technol 45(17):7345–
J Hazard Mater 190:613–621. https​://doi.org/10.1016/j.jhazm​ 7353. https​://doi.org/10.1021/es201​539s
at.2011.03.095 Liu Z, Wang C, Hou J et al (2018) Aggregation, sedimentation, and
Landa P, Cyrusova T, Jerabkova J et al (2016) Effect of metal oxides on dissolution of CuO and ZnO nanoparticles in five waters. Environ
plant germination: phytotoxicity of nanoparticles, bulk materials, Sci Pollut Res 25:31240–31249. https​://doi.org/10.1007/s1135​
and metal ions. Water Air Soil Pollut 227(12):448. https​://doi. 6-018-3123-7
org/10.1007/s1127​0-016-3156-9 Lv J, Christie P, Zhang S (2019) Uptake, translocation, and transforma-
Landa P, Prerostova S, Petrova S et al (2015) The Transcriptomic tion of metal-based nanoparticles in plants: recent advances and
response of arabidopsis thaliana to zinc oxide: a comparison of methodological challenges. Environ Sci Nano 6:41–59. https​://
the impact of nanoparticle, bulk, and ionic zinc. Environ Sci doi.org/10.1039/C8EN0​0645H​
Technol 49:14537–14545. https​://doi.org/10.1021/acs.est.5b033​ Lv J, Zhang S, Luo L et al (2015) Accumulation, speciation and uptake
30 pathway of ZnO nanoparticles in maize. Environ Sci Nano 2:68–
Landa P, Vankova R, Andrlova J et al (2012) Nanoparticle-specific 77. https​://doi.org/10.1039/c4en0​0064a​
changes in Arabidopsis thaliana gene expression after exposure Lyu S, Wei X, Chen J et al (2017) Titanium as a beneficial element for
to ZnO, TiO2, and fullerene soot. J Hazard Mater 241–242:55– crop production. Front Plant Sci 8:1–19. https:​ //doi.org/10.3389/
62. https​://doi.org/10.1016/j.jhazm​at.2012.08.059 fpls.2017.00597​
Lanzl CA, Baltrusaitis J, Cwiertny DM (2012) Dissolution of hematite López-Moreno ML, De La Rosa G, Hernández-Viezcas JA et al
nanoparticle aggregates: influence of primary particle size, dis- (2010) X-ray absorption spectroscopy (XAS) corroboration of
solution mechanism, and solution pH. Langmuir 28(45):15797– the uptake and storage of CeO2 nanoparticles and assessment
15808. https​://doi.org/10.1021/la302​2497 of their differential toxicity in four edible plant species. J Agric
Larue C, Castillo-Michel H, Sobanska S et al (2014) Fate of pristine Food Chem 58:3689–3693. https​://doi.org/10.1021/jf904​472e
TiO2 nanoparticles and aged paint-containing TiO2 nanoparti- López-Vargas ER, Ortega-Ortíz H, Cadenas-Pliego G et al (2018)
cles in lettuce crop after foliar exposure. J Hazard Mater 273:17– Foliar application of copper nanoparticles increases the fruit
26. https​://doi.org/10.1016/j.jhazm​at.2014.03.014 quality and the content of bioactive compounds in tomatoes.
Lee KH, Koh RH, Song HG (2008) Enhancement of growth and yield Appl Sci 8:1020. https​://doi.org/10.3390/app80​71020​
of tomato by Rhodopseudomonas sp. under greenhouse condi- Lü P, Cao J, He S et al (2010) Nano-silver pulse treatments improve
tions. J Microbiol 46:641–646. https​://doi.org/10.1007/s1227​ water relations of cut rose cv. Movie Star flowers Postharvest
5-008-0159-2 Biol Technol 57:196–202. https​://doi.org/10.1016/j.posth​arvbi​
Lesniak A, Salvati A, Santos-Martinez MJ et al (2013) Nanoparticle o.2010.04.003
adhesion to the cell membrane and its effect on nanoparticle Ma C, Chhikara S, Xing B et al (2013) Physiological and molecular
uptake efficiency. J Am Chem Soc 135:1438–1444. https​://doi. response of Arabidopsis thaliana (L.) to nanoparticle cerium and
org/10.1021/ja309​812z indium oxide exposure. ACS Sustain Chem Eng 1:768–778. https​
Li J, Hu J, Xiao L et al (2018) Interaction mechanisms between ://doi.org/10.1021/sc400​098h
α-Fe2O3, γ-Fe2O3 and Fe3O4 nanoparticles and Citrus max- Ma X, Geiser-Lee J, Deng Y, Kolmakov A (2010) Interactions between
ima seedlings. Sci Total Environ 625:677–685. https​://doi. engineered nanoparticles (ENPs) and plants: Phytotoxicity,
org/10.1016/j.scito​tenv.2017.12.276 uptake and accumulation. Sci Total Environ 408:3053–3061.
Li J, Song Y, Wu K et al (2018) Effects of Cr2O3 nanoparticles on the https​://doi.org/10.1016/j.scito​tenv.2010.03.031
chlorophyll fluorescence and chloroplast ultrastructure of soy- Ma X, Gurung A, Deng Y (2013) Phytotoxicity and uptake of nanoscale
bean (Glycine max). Environ Sci Pollut Res 25:19446–19457. zero-valent iron (nZVI) by two plant species. Sci Total Environ
https​://doi.org/10.1007/s1135​6-018-2132-x 443:844–849. https​://doi.org/10.1016/j.scito​tenv.2012.11.073
Li W, Zheng Y, Zhang H et al (2016) Phytotoxicity, uptake, and trans- Ma Y, He X, Zhang P et al (2011) Phytotoxicity and biotransforma-
location of fluorescent carbon dots in mung bean plants. ACS tion of La 2O 3 nanoparticles in a terrestrial plant cucumber
Appl Mater Interfaces 8:19939–19945. https​://doi.org/10.1021/ (Cucumis sativus). Nanotoxicology 5:743–753. https​://doi.
acsam​i.6b072​68 org/10.3109/17435​390.2010.54548​7
Li Y, Zhu N, Liang X et al (2020) A comparative study on the accu- Ma Y, He X, Zhang P et al (2017) Xylem and phloem based trans-
mulation, translocation and transformation of selenite, selenate, port of CeO2 nanoparticles in hydroponic cucumber plants.
and SeNPs in a hydroponic-plant system. Ecotoxicol Environ Environ Sci Technol 51:5215–5221. https​://doi.org/10.1021/
Saf 189:109955. https​://doi.org/10.1016/j.ecoen​v.2019.10995​5 acs.est.6b059​98
Liman R (2013) Genotoxic effects of bismuth (III) oxide nanoparticles Ma R, Levard C, Judy JD et al (2014) Fate of zinc oxide and silver
by allium and comet assay. Chemosphere 93:269–273. https​:// nanoparticles in a pilot wastewater treatment plant and in pro-
doi.org/10.1016/j.chemo​spher​e.2013.04.076 cessed biosolids. Environ Sci Technol 48:104–112. https​://doi.
Lin S, Reppert J, Hu Q et al (2009) Uptake, translocation, and transmis- org/10.1021/es403​646x
sion of carbon nanomaterials in rice plants. Small 5:1128–1132. Ma R, Levard C, Michel FM et al (2013) Sulfidation mechanism for
https​://doi.org/10.1002/smll.20080​1556 zinc oxide nanoparticles and the effect of sulfidation on their
Lin D, Xing B (2008) Root uptake and phytotoxicity of ZnO nano- solubility. Environ Sci Technol 47(6):2527–2534. https​://doi.
particles. Environ Sci Technol 42:5580–5585. https​: //doi. org/10.1021/es303​5347
org/10.1021/es800​422x Mahdi KNM, Peters R, van der Ploeg M et al (2018) Tracking the
Liu Q, Chen B, Wang Q et al (2009) Carbon nanotubes as molecular Transport of Silver Nanoparticles in Soil: a Saturated Column
transporters for walled plant cells. Nano Lett 9:1007–1010. https​ Experiment. Water Air Soil Pollut 229(10):334. https​://doi.
://doi.org/10.1021/nl803​083u org/10.1007/s1127​0-018-3985-9
Liu C, Li F, Luo C et al (2009) Foliar application of two silica sols Majedi SM, Lee HK, Kelly BC (2013) Role of water temperature in the
reduced cadmium accumulation in rice grains. J Hazard Mater fate and transport of zinc oxide nanoparticles in aquatic environ-
161:1466–1472. https​://doi.org/10.1016/j.jhazm​at.2008.04.116 ment. In: Journal of physics: conference series
Majumdar S, Almeida IC, Arigi EA et al (2015) Environmental effects
of nanoceria on seed production of common bean (Phaseolus

13
1604 Environmental Chemistry Letters (2021) 19:1545–1609

vulgaris): a proteomic analysis. Environ Sci Technol 49:13283– Mudunkotuwa IA, Rupasinghe T, Wu CM, Grassian VH (2012) Dis-
13293. https​://doi.org/10.1021/acs.est.5b034​52 solution of ZnO nanoparticles at circumneutral pH: a study of
Majumdar S, Trujillo-Reyes J, Hernandez-Viezcas JA et al (2016) size effects in the presence and absence of citric acid. Langmuir
Cerium biomagnification in a terrestrial food chain: influence 28:396–403. https​://doi.org/10.1021/la203​542x
of particle size and growth stage. Environ Sci Technol 50:6782– Mukherjee A, Majumdar S, Servin AD et al (2016) Carbon nanomateri-
6792. https​://doi.org/10.1021/acs.est.5b047​84 als in agriculture: a critical review. Front Plant Sci 7:172. https​
Manna I, Bandyopadhyay M (2017) Engineered nickel oxide nanopar- ://doi.org/10.3389/fpls.2016.00172​
ticle causes substantial physicochemical perturbation in plants. Mukherjee A, Peralta-Videa JR, Bandyopadhyay S et al (2014) Physi-
Front Chem 5:92. https​://doi.org/10.3389/fchem​.2017.00092​ ological effects of nanoparticulate ZnO in green peas (Pisum
Margenot AJ, Rippner DA, Dumlao MR et al (2018) Copper oxide sativum L.) cultivated in soil. Metallomics 6:132–138. https​://
nanoparticle effects on root growth and hydraulic conductiv- doi.org/10.1039/c3mt0​0064h​
ity of two vegetable crops. Plant Soil 431:333–345. https​://doi. Mushtaq YK (2011) Effect of nanoscale Fe3O4, TiO2 and carbon par-
org/10.1007/s1110​4-018-3741-3 ticles on cucumber seed germination. J Environ Sci Heal Part A
Marie T, Mélanie A, Lenka B et al (2014) Transfer, transformation, and Toxic/Hazardous Subst Environ Eng 46:1732–1735. https​://doi.
impacts of ceria nanomaterials in aquatic mesocosms simulating org/10.1080/10934​529.2011.63340​3
a pond ecosystem. Environ Sci Technol 48:9004–9013. https​:// Máté Z, Horváth E, Kozma G et al (2016) Size-dependent toxicity
doi.org/10.1021/es501​641b differences of intratracheally instilled manganese oxide nano-
Martínez-Fernández D, Vítková M, Bernal MP, Komárek M (2015) particles: conclusions of a subacute animal experiment. Biol
Effects of nano-maghemite on trace element accumulation Trace Elem Res 171:156–166. https​://doi.org/10.1007/s1201​
and drought response of Helianthus annuus L. in a contami- 1-015-0508-z
nated mine soil. Water Air Soil Pollut 226(4):101. https​://doi. Nagaonkar D, Shende S, Rai M (2015) Biosynthesis of copper nanopar-
org/10.1007/s1127​0-015-2365-y ticles and its effect on actively dividing cells of mitosis in Allium
Matlochová A, Plachá D, Rapantová N (2013) The application of cepa. Biotechnol Prog 31:557–565. https​://doi.org/10.1002/
nanoscale materials in groundwater remediation. Polish J Envi- btpr.2040
ron Stud 22(5):1401 Nair PMG, Chung IM (2014) A mechanistic study on the toxic effect
Mauter MS, Zucker I, Perreault F et al (2018) The role of nanotechnol- of copper oxide nanoparticles in soybean (Glycine max L.) root
ogy in tackling global water challenges. Nat Sustain 1:166–175. development and lignification of root cells. Biol Trace Elem Res
https​://doi.org/10.1038/s4189​3-018-0046-8 162:342–352. https​://doi.org/10.1007/s1201​1-014-0106-5
McCann MC, Wells B, Roberts K (1990) Direct visualization of cross- Nair PMG, Chung IM (2015) Physiological and molecular level studies
links in the primary plant cell wall. J Cell Sci 96:323–334 on the toxicity of silver nanoparticles in germinating seedlings of
Medina-Velo IA, Zuverza-Mena N, Tamez C et al (2018) Minimal mung bean (Vigna radiata L.). Acta Physiol Plant 37:1–11. https​
transgenerational effect of ZnO nanomaterials on the physiology ://doi.org/10.1007/s1173​8-014-1719-1
and nutrient profile of phaseolus vulgaris. ACS Sustain Chem Nasim SA, Dhir B (2010) Heavy metals alter the potency of medicinal
Eng 6:7924–7930. https:​ //doi.org/10.1021/acssus​ cheme​ ng.8b011​ plants. Rev Environ Contam Toxicol 203:139–149. https​://doi.
88 org/10.1007/978-1-4419-1352-4_5
Meisrimler CN, Planchon S, Renaut J et al (2011) Alteration of plasma Nasser F, Constantinou J, Lynch I (2020) Nanomaterials in the environ-
membrane-bound redox systems of iron deficient pea roots by ment acquire an “eco-corona” impacting their toxicity to daphnia
chitosan. J Proteomics 74:1437–1449. https​://doi.org/10.1016/j. magna—a call for updating toxicity testing policies. Proteomics
jprot​.2011.01.012 20(9):1800412. https​://doi.org/10.1002/pmic.20180​0412
Miao AJ, Zhang XY, Luo Z et al (2010) Zinc oxide-engineered nano- Navarro E, Baun A, Behra R et al (2008) Environmental behavior and
particles: dissolution and toxicity to marine phytoplankton. Envi- ecotoxicity of engineered nanoparticles to algae, plants, and
ron Toxicol Chem 29:2814–2822. https:​ //doi.org/10.1002/etc.340 fungi. Ecotoxicology 17:372–386. https:​ //doi.org/10.1007/s1064​
Mikkelsen R (2018) Nanofertilizer and Nanotechnology: a quick look. 6-008-0214-0
Better Crop with Plant Food 102:18–19. https:​ //doi.org/10.24047​ Nechitailo GS, Bogoslovskaya OA, Ol’khovskaya IP, Glushchenko
/bc102​318 NN, (2018) Influence of iron, zinc, and copper nanoparticles on
Milani N, Hettiarachchi GM, Kirby JK et al (2015) Fate of zinc oxide some growth indices of pepper plants. Nanotechnologies Russ
nanoparticles coated onto macronutrient fertilizers in an alka- 13:161–167. https​://doi.org/10.1134/S1995​07801​80200​52
line calcareous soil. PLoS ONE 10(5):e0126275. https​://doi. Odzak N, Kistler D, Sigg L (2017) Influence of daylight on the fate of
org/10.1371/journ​al.pone.01262​75 silver and zinc oxide nanoparticles in natural aquatic environ-
Mirzajani F, Askari H, Hamzelou S et al (2014) Proteomics study of sil- ments. Environ Pollut 226:1–11. https​://doi.org/10.1016/j.envpo​
ver nanoparticles toxicity on Oryza sativa L. Ecotoxicol Environ l.2017.04.006
Saf 108:335–339. https​://doi.org/10.1016/j.ecoen​v.2014.07.013 Onelli E, Prescianotto-Baschong C, Caccianiga M, Moscatelli A (2008)
Mohd Omar F, Abdul Aziz H, Stoll S (2014) Aggregation and disag- Clathrin-dependent and independent endocytic pathways in
gregation of ZnO nanoparticles: influence of pH and adsorption tobacco protoplasts revealed by labelling with charged nanogold.
of Suwannee River humic acid. Sci Total Environ 468–469:195– J Exp Bot 59:3051–3068. https​://doi.org/10.1093/jxb/ern15​4
201. https​://doi.org/10.1016/j.scito​tenv.2013.08.044 Ozyigit II, Filiz E, Vatansever R et al (2016) Identification and com-
Mondal A, Basu R, Das S, Nandy P (2011) Beneficial role of carbon parative analysis of H2O2-scavenging enzymes (ascorbate per-
nanotubes on mustard plant growth: an agricultural prospect. J oxidase and glutathione peroxidase) in selected plants employ-
Nanoparticle Res 13:4519–4528. https​://doi.org/10.1007/s1105​ ing bioinformatics approaches. Front Plant Sci 7:301. https:​ //doi.
1-011-0406-z org/10.3389/fpls.2016.00301​
Movafeghi A, Khataee A, Abedi M et al (2018) Effects of TiO2 Pagano L, Servin AD, De La Torre-Roche R et al (2016) Molecular
nanoparticles on the aquatic plant Spirodela polyrrhiza: evalu- response of crop plants to engineered nanomaterials. Environ Sci
ation of growth parameters, pigment contents and antioxidant Technol 50:7198–7207. https​://doi.org/10.1021/acs.est.6b018​16
enzyme activities. J Environ Sci (China) 64:130–138. https​:// Pakrashi S, Jain N, Dalai S et al (2014) In vivo genotoxicity assessment
doi.org/10.1016/j.jes.2016.12.020 of titanium dioxide nanoparticles by Allium cepa root tip assay

13
Environmental Chemistry Letters (2021) 19:1545–1609 1605

at high exposure concentrations. PLoS ONE 9(2):e87789. https​ Qiu H, Smolders E (2017) Nanospecific phytotoxicity of CuO nano-
://doi.org/10.1371/journ​al.pone.00877​89 particles in soils disappeared when bioavailability factors were
Pallavi MCM, Srivastava R et al (2016) Impact assessment of silver considered. Environ Sci Technol 51:11976–11985. https​://doi.
nanoparticles on plant growth and soil bacterial diversity. 3 Bio- org/10.1021/acs.est.7b018​92
tech 6(2):254. https​://doi.org/10.1007/s1320​5-016-0567-7 Quik JTK, Velzeboer I, Wouterse M et al (2014) Heteroaggregation and
Palocci C, Valletta A, Chronopoulou L et al (2017) Endocytic path- sedimentation rates for nanomaterials in natural waters. Water
ways involved in PLGA nanoparticle uptake by grapevine cells Res 48:269–279. https​://doi.org/10.1016/j.watre​s.2013.09.036
and role of cell wall and membrane in size selection. Plant Cell Rafique R, Zahra Z, Virk N et al (2018) Dose-dependent physiological
Rep 36:1917–1928. https​://doi.org/10.1007/s0029​9-017-2206-0 responses of Triticum aestivum L. to soil applied TiO2 nano-
Peijnenburg W, Praetorius A, Scott-Fordsmand J, Cornelis G (2016) particles: alterations in chlorophyll content, H2O2 production,
Fate assessment of engineered nanoparticles in solids dominated and genotoxicity. Agric Ecosyst Environ 255:95–101. https:​ //doi.
media—Current insights and the way forward. Environ Pollut org/10.1016/j.agee.2017.12.010
218:1365–1369. https​://doi.org/10.1016/j.envpo​l.2015.11.043 Rai PK, Kumar V, Lee SS et al (2018) Nanoparticle-plant interaction:
Peng C, Xu C, Liu Q et al (2017) Fate and Transformation of CuO implications in energy, environment, and agriculture. Environ Int
nanoparticles in the soil-rice system during the life cycle of 119:1–19. https​://doi.org/10.1016/j.envin​t.2018.06.012
rice plants. Environ Sci Technol 51:4907–4917. https​://doi. Rajeshwari A, Kavitha S, Alex SA et al (2015) Cytotoxicity of alu-
org/10.1021/acs.est.6b058​82 minum oxide nanoparticles on Allium cepa root tip—effects of
Peng C, Zhang W, Gao H et al (2017) Behavior and potential impacts oxidative stress generation and biouptake. Environ Sci Pollut Res
of metal-based engineered nanoparticles in aquatic environments. 22:11057–11066. https​://doi.org/10.1007/s1135​6-015-4355-4
Nanomaterials 7(1):21. https​://doi.org/10.3390/nano7​01002​1 Rajput V, Minkina T, Fedorenko A et al (2018) Toxicity of copper oxide
Perreault F, Samadani M, Dewez D (2014) Effect of soluble cop- nanoparticles on spring barley (Hordeum sativum distichum).
per released from copper oxide nanoparticles solubilisation Sci Total Environ 645:1103–1113. https:​ //doi.org/10.1016/j.scito​
on growth and photosynthetic processes of Lemna gibba L. tenv.2018.07.211
Nanotoxicology 8:374–382. https ​ : //doi.org/10.3109/17435​ Rajput VD, Minkina T, Fedorenko A et al (2019) Destructive effect
390.2013.78993​6 of copper oxide nanoparticles on ultrastructure of chloroplast,
Philippe A, Schaumann GE (2014) Interactions of dissolved organic plastoglobules and starch grains in spring barley (Hordeum sati-
matter with natural and engineered inorganic colloids: a review. vum). Int J Agric Biol 21:171–174. https​://doi.org/10.17957​/
Environ Sci Technol 48:8946–8962. https​://doi.org/10.1021/ IJAB/15.0877
es502​342r Rajput VD, Minkina T, Sushkova S et al (2018) Effect of nanoparti-
Pinďáková L, Kašpárková V, Kejlová K et al (2017) Behaviour of sil- cles on crops and soil microbial communities. J Soils Sediments
ver nanoparticles in simulated saliva and gastrointestinal fluids. 18:2179–2187. https​://doi.org/10.1007/s1136​8-017-1793-2
Int J Pharm 527(1–2):12–20. https​://doi.org/10.1016/j.ijpha​ Rajput VD, Minkina T, Suskova S et al (2018) Effects of copper nano-
rm.2017.05.026 particles (CuO NPs) on crop plants: a mini review. Bionanosci-
Pittol M, Tomacheski D, Simões DN et al (2017) Macroscopic effects ence 8:36–42. https​://doi.org/10.1007/s1266​8-017-0466-3
of silver nanoparticles and titanium dioxide on edible plant Raliya R, Franke C, Chavalmane S et al (2016) Quantitative under-
growth. Environ Nanotechnol Monit Manag 8:127–133. https​:// standing of nanoparticle uptake in watermelon plants. Front Plant
doi.org/10.1016/j.enmm.2017.07.003 Sci 7:1288. https​://doi.org/10.3389/fpls.2016.01288​
Plaksenkova I, Jermaļonoka M, Bankovska L et al (2019) Effects of Raliya R, Nair R, Chavalmane S et al (2015) Mechanistic evaluation of
Fe3O4 Nanoparticle Stress on the Growth and Development of translocation and physiological impact of titanium dioxide and
Rocket Eruca sativa. J Nanomater 2019:2678247. https​://doi. zinc oxide nanoparticles on the tomato (Solanum lycopersicum
org/10.1155/2019/26782​47 L.) plant. Metallomics 7:1584–1594. https​://doi.org/10.1039/
Pokhrel LR, Dubey B (2013) Evaluation of developmental responses c5mt0​0168d​
of two crop plants exposed to silver and zinc oxide nanoparticles. Raliya R, Tarafdar JC (2013) ZnO Nanoparticle Biosynthesis and its
Sci Total Environ 452–453:321–332. https​://doi.org/10.1016/j. effect on phosphorous-mobilizing enzyme secretion and gum
scito​tenv.2013.02.059 contents in clusterbean (Cyamopsis tetragonoloba L.). Agric
Pradas Del Real AE, Vidal V, Carrière M et al (2017) Silver nanopar- Res 2:48–57. https​://doi.org/10.1007/s4000​3-012-0049-z
ticles and wheat roots: a complex interplay. Environ Sci Technol Raliya R, Tarafdar JC, Biswas P (2016) Enhancing the Mobilization
51:5774–5782. https​://doi.org/10.1021/acs.est.7b004​22 of native phosphorus in the mung bean rhizosphere using ZnO
Priester JH, Ge Y, Mielke RE et al (2012) Soybean susceptibility to nanoparticles synthesized by soil fungi. J Agric Food Chem
manufactured nanomaterials with evidence for food quality and 64:3111–3118. https​://doi.org/10.1021/acs.jafc.5b052​24
soil fertility interruption. Proc Natl Acad Sci U S A 109:E2451– Rastogi A, Zivcak M, Sytar O et al (2017) Impact of metal and metal
E2456. https​://doi.org/10.1073/pnas.12054​31109​ oxide nanoparticles on plant: a critical review. Front Chem
Priester JH, Moritz SC, Espinosa K et al (2017) Damage assessment 5:78. https​://doi.org/10.3389/fchem​.2017.00078​
for soybean cultivated in soil with either CeO2 or ZnO manufac- Rastogi A, Zivcak M, Sytar O, Kalaji HM, He X, Mbarki S, Bres-
tured nanomaterials. Sci Total Environ 579:1756–1768. https​:// tic M (2017) Impact of metal and metal oxide nanoparticles
doi.org/10.1016/j.scito​tenv.2016.11.149 on plant: a critical review. Frontiers Chem 5:78. https​://doi.
Pryor WA (1991) The antioxidant nutrients and disease prevention— org/10.3389/fchem​.2017.00078​
What do we know and what do we need to find out? Am J Clin Rawat S, Pullagurala VLR, Adisa IO et al (2018) Factors affecting
Nut 53(1):391S-S393. https​://doi.org/10.1093/ajcn/53.1.391S fate and transport of engineered nanomaterials in terrestrial
Pérez-de-Luque A (2017) Interaction of nanomaterials with plants: environments. Curr Opin Environ Sci Heal 6:47–53. https​://
What do we need for real applications in agriculture? Front Envi- doi.org/10.1016/j.coesh​.2018.07.014
ron Sci 5:12. https​://doi.org/10.3389/fenvs​.2017.00012​ Reddy AM, Kumar SG, Jyothsnakumari G et al (2005) Lead induced
Qi M, Liu Y, Li T (2013) Nano-TiO2 improve the photosynthesis changes in antioxidant metabolism of horsegram (Macrotyloma
of tomato leaves under mild heat stress. Biol Trace Elem Res uniflorum (Lam.) Verdc.) and bengalgram (Cicer arietinum
156:323–328. https​://doi.org/10.1007/s1201​1-013-9833-2 L.). Chemosphere 60:97–104. https​://doi.org/10.1016/j.chemo​
spher​e.2004.11.092

13
1606 Environmental Chemistry Letters (2021) 19:1545–1609

Rees F, Sterckeman T, Morel JL (2016) Root development of non- the apoplast for the mineral nutrition of higher plants. https:​ //doi.
accumulating and hyperaccumulating plants in metal-contam- org/10.1007/978-1-4020-5843-1
inated soils amended with biochar. Chemosphere 142:48–55. Schreiber L (2005) Polar paths of diffusion across plant cuticles: New
https​://doi.org/10.1016/j.chemo​spher​e.2015.03.068 evidence for an old hypothesis. Ann Bot 95:1069–1073. https​://
Rezaei F, Moaveni P, Mozafari H (2015) Effect of Different concen- doi.org/10.1093/aob/mci12​2
trations and time of nano TiO2 spraying on quantitative and Schultz C, Powell K, Crossley A et al (2015) Analytical approaches
qualitative yield of soybean (Glycine max L) at Shahr-e-Qods. to support current understanding of exposure, uptake and dis-
Iran. Biol Forum Int J 7:957–964 tributions of engineered nanoparticles by aquatic and terrestrial
Richardson AE (2001) Prospects for using soil microorganisms to organisms. Ecotoxicology 24:239–261. https​://doi.org/10.1007/
improve the acquisition of phosphorus by plants. Aust J Plant s1064​6-014-1387-3
Physiol 28(9):897–906. https​://doi.org/10.1071/PP010​93 Schwabe F, Tanner S, Schulin R et al (2015) Dissolved cerium contrib-
Rico CM, Barrios AC, Tan W et al (2015) Physiological and bio- utes to uptake of Ce in the presence of differently sized CeO2-
chemical response of soil-grown barley (Hordeum vulgare nanoparticles by three crop plants. Metallomics 7:466–477. https​
L.) to cerium oxide nanoparticles. Environ Sci Pollut Res ://doi.org/10.1039/c4mt0​0343h​
22:10551–10558. https​://doi.org/10.1007/s1135​6-015-4243-y Schwaminger SP, Fraga-García P, Selbach F et al (2017) Bio-nano
Rico CM, Hong J, Morales MI et al (2013) Effect of cerium oxide interactions: cellulase on iron oxide nanoparticle surfaces.
nanoparticles on rice: a study involving the antioxidant defense Adsorption 23:281–292. https ​ : //doi.org/10.1007/s1045​
system and in vivo fluorescence imaging. Environ Sci Technol 0-016-9849-y
47:5635–5642. https​://doi.org/10.1021/es401​032m Sendra M, Yeste MP, Gatica JM et al (2017) Homoagglomeration and
Rico CM, Majumdar S, Duarte-Gardea M et al (2011) Interaction of heteroagglomeration of TiO2, in nanoparticle and bulk form,
nanoparticles with edible plants and their possible implications onto freshwater and marine microalgae. Sci Total Environ
in the food chain. J Agric Food Chem 59:3485–3498. https​:// 592:403–411. https​://doi.org/10.1016/j.scito​tenv.2017.03.127
doi.org/10.1021/jf104​517j Servin AD, Castillo-Michel H, Hernandez-Viezcas JA et al (2012)
Rico CM, Morales MI, McCreary R et al (2013) Cerium oxide nan- Synchrotron micro-XRF and micro-XANES confirmation of
oparticles modify the antioxidative stress enzyme activities the uptake and translocation of TiO2 nanoparticles in cucumber
and macromolecule composition in rice seedlings. Environ Sci (Cucumis sativus) plants. Environ Sci Technol 46:7637–7643.
Technol 47:14110–14118. https​://doi.org/10.1021/es403​3887 https​://doi.org/10.1021/es300​955b
Rico CM, Peralta-Videa JR, Gardea-Torresdeya JL (2015) Differ- Servin AD, Morales MI, Castillo-Michel H et al (2013) Synchrotron
ential effects of cerium oxide nanoparticles on rice, wheat, verification of TiO2 accumulation in cucumber fruit: a pos-
and barley roots: a Fourier Transform Infrared (FT-IR) micro- sible pathway of TiO2 nanoparticle transfer from soil into the
spectroscopy study. Appl Spectrosc 69:287–295. https​://doi. food chain. Environ Sci Technol 47:11592–11598. https​://doi.
org/10.1366/14-07495​ org/10.1021/es403​368j
Robinson MS (2015) Forty years of clathrin-coated vesicles. Traffic Servin AD, Pagano L, Castillo-Michel H et al (2017) Weathering in
16:1210–1238. https​://doi.org/10.1111/tra.12335​ soil increases nanoparticle CuO bioaccumulation within a ter-
Romero-Freire A, Lofts S, Martín Peinado FJ, van Gestel CAM restrial food chain. Nanotoxicology 11:98–111. https​://doi.
(2017) Effects of aging and soil properties on zinc oxide org/10.1080/17435​390.2016.12772​74
nanoparticle availability and its ecotoxicological effects to the Shankramma K, Yallappa S, Shivanna MB, Manjanna J (2016) Fe2O3
earthworm Eisenia andrei. Environ Toxicol Chem 36:137–146. magnetic nanoparticles to enhance S. lycopersicum (tomato)
https​://doi.org/10.1002/etc.3512 plant growth and their biomineralization. Appl Nanosci 6:983–
Saharan V, Sharma G, Yadav M et al (2015) Synthesis and in vitro 990. https​://doi.org/10.1007/s1320​4-015-0510-y
antifungal efficacy of Cu-chitosan nanoparticles against patho- Sharma SS, Dietz KJ (2009) The relationship between metal toxicity
genic fungi of tomato. Int J Biol Macromol 75:346–353. https​ and cellular redox imbalance. Trends Plant Sci 14:43–50. https​
://doi.org/10.1016/j.ijbio​mac.2015.01.027 ://doi.org/10.1016/j.tplan​ts.2008.10.007
Salehi H, Chehregani A, Lucini L et al (2018) Morphological, prot- Sharma PK, Raghubanshi AS, Shah K (2020) Examining dye degrada-
eomic and metabolomic insight into the effect of cerium diox- tion and antibacterial properties of organically induced α-MoO3
ide nanoparticles to Phaseolus vulgaris L. under soil or foliar nanoparticles, their uptake and phytotoxicity in rice seedlings.
application. Sci Total Environ 616–617:1540–1551. https​://doi. Environ Nanotechnol Monit Manag 14:100315. https​://doi.
org/10.1016/j.scito​tenv.2017.10.159 org/10.1016/j.enmm.2020.10031​5
Salvati A, Åberg C, dos Santos T et al (2011) Experimental and Sharma S, Uttam KN (2017) Rapid analyses of stress of copper oxide
theoretical comparison of intracellular import of polymeric nanoparticles on wheat plants at an early stage by laser induced
nanoparticles and small molecules: toward models of uptake fluorescence and attenuated total reflectance Fourier transform
kinetics. Nanomed Nanotech Biol Med 7:818–826. https​://doi. infrared spectroscopy. Vib Spectrosc 92:135–150. https​://doi.
org/10.1016/j.nano.2011.03.005 org/10.1016/j.vibsp​ec.2017.06.004
Saquib Q, Faisal M, Alatar AA et al (2016) Genotoxicity of ferric Shen CX, Zhang QF, Li J et al (2010) Induction of programmed cell
oxide nanoparticles in Raphanus sativus: deciphering the role death in Arabidopsis and rice by single-wall carbon nanotubes.
of signaling factors, oxidative stress and cell death. J Environ Am J Bot 97:1602–1609. https​://doi.org/10.3732/ajb.10000​73
Sci (China) 47:49–62. https​://doi.org/10.1016/j.jes.2015.12.037 Sheng A, Liu F, Shi L, Liu J (2016) Aggregation kinetics of hema-
Sardoiwala MN, Kaundal B, Choudhury SR (2018) Toxic impact of tite particles in the presence of outer membrane cytochrome
nanomaterials on microbes, plants and animals. Environ Chem OmcA of Shewanella oneidenesis MR-1. Environ Sci Technol
Lett 16(1):147–160. https​://doi.org/10.1007/s1031​1-017-0672-9 50:11016–11024. https​://doi.org/10.1021/acs.est.6b029​63
Sattelmacher B, Mühling K-H, Pennewiß K (1998) The apoplast Shewfelt RL, Erickson MC (1991) Role of lipid peroxidation in
- its significance for the nutrition of higher plants. Zeitschrift the mechanism of membrane-associated disorders in edible
für Pflanzenernährung und Bodenkd 161:485–498. https​://doi. plant tissue. Trends Food Sci Technol 2:152–154. https​://doi.
org/10.1002/jpln.1998.35816​10502​ org/10.1016/0924-2244(91)90661​-2
Sattelmacher B, Horst WJ (2007) The apoplast of higher plants: Com-
partment of storage, transport and reactions: the significance of

13
Environmental Chemistry Letters (2021) 19:1545–1609 1607

Sheykhbaglou R, Sedghi M, Shishevan MT, Sharifi RS (2010) Effects Arabidopsis thaliana. Environ Pollut 212:605–614. https​://doi.
of nano-iron oxide particles on agronomic traits of soybean. Not org/10.1016/j.envpo​l.2016.03.019
Sci Biol 2:112–113. https​://doi.org/10.15835​/nsb22​4667 Taranath TC, Patil BN, Santosh TU, Sharath BS (2015) Cytotoxicity
Shi J, Abid AD, Kennedy IM et al (2011) To duckweeds (Landoltia of zinc nanoparticles fabricated by Justicia adhatoda L. on root
punctata), nanoparticulate copper oxide is more inhibitory than tips of Allium cepa L.—a model approach. Environ Sci Pollut
the soluble copper in the bulk solution. Environ Pollut 159:1277– Res 22:8611–8617. https​://doi.org/10.1007/s1135​6-014-4043-9
1282. https​://doi.org/10.1016/j.envpo​l.2011.01.028 Taylor AF, Rylott EL, Anderson CWN, Bruce NC (2014) Investigat-
Siddiqi KS, Husen A (2017a) Plant response to engineered metal oxide ing the toxicity, uptake, nanoparticle formation and genetic
nanoparticles. Nanoscale Res Lett 12:92. https:​ //doi.org/10.1186/ response of plants to gold. PLoS ONE 9(4):e93793. https​://doi.
s1167​1-017-1861-y org/10.1371/journ​al.pone.00937​93
Siddiqi KS, Husen A (2017b) Plant response to engineered metal Tighe-Neira R, Carmora E, Recio G et al (2018) Metallic nanoparticles
oxide nanoparticles. Nanoscale Res Lett 12(1):92. https​://doi. influence the structure and function of the photosynthetic appa-
org/10.1186/s1167​1-017-1861-y ratus in plants. Plant Physiol Biochem 130:408–417. https​://doi.
Singh B, Satyanarayana T (2011) Microbial phytases in phosphorus org/10.1016/j.plaph​y.2018.07.024
acquisition and plant growth promotion. Physiol Mol Biol Plants Tiwari AJ, Fields CG, Marr LC (2013) Aerosol science and technol-
17:93–103. https​://doi.org/10.1007/s1229​8-011-0062-x ogy a cost-effective method of aerosolizing dry powdered nano-
Singh P, Singh R, Borthakur A et al (2016) Effect of nanoscale TiO particles. Aerosol Sci Technol 47(11):1267–1275. https​://doi.
2 -activated carbon composite on Solanum lycopersicum (L.) org/10.1080/02786​826.2013.83429​2
and Vigna radiata (L.) seeds germination. Energy Ecol Environ Tiwari AJ, Marr LC (2010) The role of atmospheric transformations in
1:131–140. https​://doi.org/10.1007/s4097​4-016-0009-8 determining environmental impacts of carbonaceous nanoparti-
Singh AK (2016) Mechanisms of Nanoparticle Toxicity. In: Singh AK cles. J Environ Qual 39(6):1883–1895. https​://doi.org/10.2134/
(eds) Engineered Nanoparticles. Elsevier, pp 295–341. https​:// jeq20​10.0050
doi.org/10.1016/B978-0-12-80140​6-6.00007​-8 Tripathi DK, Mishra RK, Singh S et al (2017) Nitric oxide ameliorates
Soenen SJ, Parak WJ, Rejman J, Manshian B (2015) (Intra)cellular zinc oxide nanoparticles phytotoxicity in wheat seedlings: Impli-
stability of inorganic nanoparticles: effects on cytotoxicity, cation of the ascorbate–glutathione cycle. Front Plant Sci 8:1–10.
particle functionality, and biomedical applications. Chem Rev https​://doi.org/10.3389/fpls.2017.00001​
115:2109–2135. https​://doi.org/10.1021/cr400​714j Tumburu L, Andersen CP, Rygiewicz PT, Reichman JR (2015) Phe-
Son J, Vavra J, Forbes VE (2015) Effects of water quality parameters notypic and genomic responses to titanium dioxide and cerium
on agglomeration and dissolution of copper oxide nanoparticles oxide nanoparticles in Arabidopsis germinants. Environ Toxicol
(CuO-NPs) using a central composite circumscribed design. Sci Chem 34:70–83. https​://doi.org/10.1002/etc.2756
Total Environ 521–522:183–190. https​://doi.org/10.1016/j.scito​ Tumburu L, Andersen CP, Rygiewicz PT, Reichman JR (2017) Molec-
tenv.2015.03.093 ular and physiological responses to titanium dioxide and cerium
Song G, Hou W, Gao Y et al (2016) Effects of CuO nanoparticles on oxide nanoparticles in Arabidopsis. Environ Toxicol Chem
Lemna minor. Bot Stud 57(1):1–8. https:​ //doi.org/10.1186/s4052​ 36:71–82. https​://doi.org/10.1002/etc.3500
9-016-0118-x Uddin MN, Desai F, Asmatulu E (2020) Engineered nanomateri-
Srivastava AK, Dev A, Karmakar S (2018) Nanosensors and nanobio- als in the environment: bioaccumulation, biomagnification
sensors in food and agriculture. Environ Chem Lett 16(1):161– and biotransformation. Environ Chem Lett 4:1–1. https​://doi.
182. https​://doi.org/10.1007/s1031​1-017-0674-7 org/10.1007/s1031​1-019-00947​-0
Srivastava LM (2002) Seed germination, mobilization of food reserves, Ullah H, Li X, Peng L et al (2020) In vivo phytotoxicity, uptake, and
and seed dormancy. In: Srivastava LM (eds) Plant growth and translocation of PbS nanoparticles in maize (Zea mays L) plants.
development. Academic Press, Elsevier, pp 447–471. https:​ //doi. Sci Total Environ 737:139558. https​://doi.org/10.1016/j.scito​
org/10.1016/B978-01266​0570-9/50161​-1 tenv.2020.13955​8
Sudha PN, Sangeetha K, Vijayalakshmi K, Barhoum A (2018) Nano- Umeyama T, Matano D, Baek J et al (2015) Boosting of the perfor-
materials history, classification, unique properties, production mance of perovskite solar cells through systematic introduction
and market. In: Emerging applications of nanoparticles and of reduced graphene oxide in TiO2 Layers. Chem Lett 44:1410–
architectural nanostructures: current prospects and future trends. 1412. https​://doi.org/10.1246/cl.15065​1
pp 341–384. Doi: https​://doi.org/10.1016/B978-0-323-51254​ Van NL, Ma C, Rui Y et al (2015) Phytotoxic mechanism of nano-
-1.00012​-9 particles: Destruction of chloroplasts and vascular bundles and
Sun TY, Bornhöft NA, Hungerbühler K, Nowack B (2016) Dynamic alteration of nutrient absorption. Sci Rep 5(1):1–3. https​://doi.
probabilistic modeling of environmental emissions of engineered org/10.1038/srep1​1618
nanomaterials. Environ Sci Technol 50:4701–4711. https​://doi. Vannini C, Domingo G, Onelli E et al (2013) Morphological and pro-
org/10.1021/acs.est.5b058​28 teomic responses of eruca sativa exposed to silver nanoparticles
Sun Y, Jing R, Zheng F et al (2019) Evaluating phytotoxicity of bare or silver nitrate. PLoS ONE 8(7):e68752. https:​ //doi.org/10.1371/
and starch-stabilized zero-valent iron nanoparticles in mung journ​al.pone.00687​52
bean. Chemosphere 236:124336. https:​ //doi.org/10.1016/j.chemo​ Villaseñor MJ, Ríos Á (2018) Nanomaterials for water cleaning and
spher​e.2019.07.067 desalination, energy production, disinfection, agriculture and
Sun Z, Xiong T, Zhang T et al (2019) Influences of zinc oxide nano- green chemistry. Environ Chem Lett 16(1):11–34. https​://doi.
particles on Allium cepa root cells and the primary cause of phy- org/10.1007/s1031​1-017-0656-9
totoxicity. Ecotoxicology 28:175–188. https​://doi.org/10.1007/ Vithanage M, Seneviratne M, Ahmad M et al (2017) Contrasting effects
s1064​6-018-2010-9 of engineered carbon nanotubes on plants: a review. Environ
Tan XM, Lin C, Fugetsu B (2009) Studies on toxicity of multi-walled Geochem Health 39:1421–1439. https​://doi.org/10.1007/s1065​
carbon nanotubes on suspension rice cells. Carbon N Y 47:3479– 3-017-9957-y
3487. https​://doi.org/10.1016/j.carbo​n.2009.08.018 Vittori Antisari L, Carbone S, Gatti A et al (2015) Uptake and trans-
Tang Y, He R, Zhao J et al (2016) Oxidative stress-induced toxicity location of metals and nutrients in tomato grown in soil pol-
of CuO nanoparticles and related toxicogenomic responses in luted with metal oxide (CeO2, Fe3O4, SnO2, TiO2) or metallic

13
1608 Environmental Chemistry Letters (2021) 19:1545–1609

(Ag Co, Ni) engineered nanoparticles. Environ Sci Pollut Res Xu L, Liang HW, Yang Y, Yu SH (2018) Stability and reactivity:
22:1841–1853. https​://doi.org/10.1007/s1135​6-014-3509-0 positive and negative aspects for nanoparticle processing.
Von Moos N, Bowen P, Slaveykova VI (2014) Bioavailability of inor- Chem Rev 118:3209–3250. https​://doi.org/10.1021/acs.chemr​
ganic nanoparticles to planktonic bacteria and aquatic micro- ev.7b002​08
algae in freshwater. Environ Sci Nano 1:214–232. https​://doi. Xuming W, Fengqing G, Linglan M et al (2008) Effects of nano-
org/10.1039/C3EN0​0054K​ anatase on ribulose-1, 5-bisphosphate carboxylase/oxygenase
Wan J, Wang R, Wang R et al (2019) Comparative physiological and mrna expression in spinach. Biol Trace Elem Res 126:280–
transcriptomic analyses reveal the toxic effects of ZnO nanopar- 289. https​://doi.org/10.1007/s1201​1-008-8203-y
ticles on plant growth. Environ Sci Technol 53:4235–4244. https​ Yan A, Chen Z (2019) Impacts of silver nanoparticles on plants: a
://doi.org/10.1021/acs.est.8b066​41 focus on the phytotoxicity and underlying mechanism. Int J
Wang H, Kou X, Pei Z et al (2011) Physiological effects of magnetite Mol Sci 20:1003. https​://doi.org/10.3390/ijms2​00510​03
(Fe3O4) nanoparticles on perennial ryegrass (Lolium perenne L.) Yan X, Chen X (2012) Titanium dioxide nanomaterials. In: Materials
and pumpkin (Cucurbita mixta) plants. Nanotoxicology 5:30–42. research society symposium proceedings, pp 1–38.
https​://doi.org/10.3109/17435​390.2010.48920​6 Yang Z, Chen J, Dou R et al (2015) Assessment of the phytotoxic-
Wang F, Liu X, Shi Z et al (2016) Arbuscular mycorrhizae alleviate ity of metal oxide nanoparticles on two crop plants, maize
negative effects of zinc oxide nanoparticle and zinc accumula- (Zea mays L.) and rice (Oryza sativa L.). Int J Environ Res
tion in maize plants: a soil microcosm experiment. Chemosphere Public Health 12:15100–15109. https​://doi.org/10.3390/ijerp​
147:88–97. https​://doi.org/10.1016/j.chemo​spher​e.2015.12.076 h1212​14963​
Wang Q, Ma X, Zhang W et al (2012) The impact of cerium oxide Yang F, Liu C, Gao F et al (2007) The improvement of spinach
nanoparticles on tomato (Solanum lycopersicum L.) and its growth by nano-anatase TiO2 treatment is related to nitrogen
implications for food safety. Metallomics 4:1105–1112. https​:// photoreduction. Biol Trace Elem Res 119:77–88. https​://doi.
doi.org/10.1039/c2mt2​0149f​ org/10.1007/s1201​1-007-0046-4
Wang P, Menzies NW, Lombi E et al (2013) Fate of ZnO nanoparticles Yanga J, Cao W, Rui Y (2017) Interactions between nanoparticles and
in soils and cowpea (Vigna unguiculata). Environ Sci Technol plants: phytotoxicity and defense mechanisms. J Plant Interact
47:13822–13830. https​://doi.org/10.1021/es403​466p 12:158–169. https​://doi.org/10.1080/17429​145.2017.13109​44
Wang X, Qi Z, Wang S et al (2011) The study of a single BGC823 cell Yanlk F, Vardar F (2015) Toxic effects of aluminum oxide (Al2O3)
using Fourier transform infrared microspectroscopic imaging. Nanoparticles on root growth and development in Triticum aes-
Spectrochim Acta Part A Mol Biomol Spectrosc 79:1660–1662. tivum. Water Air Soil Pollut 226:296. https​://doi.org/10.1007/
https​://doi.org/10.1016/j.saa.2011.05.031 s1127​0-015-2566-4
Wang WN, Tarafdar JC, Biswas P (2013) Nanoparticle synthesis and Yanık F, Vardar F (2018) Oxidative stress response to aluminum oxide
delivery by an aerosol route for watermelon plant foliar uptake. (Al2O3) nanoparticles in Triticum aestivum. Biology 73:129–
J Nanoparticle Res 15(1):1417. https​://doi.org/10.1007/s1105​ 135. https​://doi.org/10.2478/s1175​6-018-0016-7
1-013-1417-8 Yasmeen F, Raja NI, Mustafa G et al (2016) Quantitative proteomic
Wang Y, Westerhoff P, Hristovski KD (2012) Fate and biological analysis of post-flooding recovery in soybean root exposed to
effects of silver, titanium dioxide, and C 60 (fullerene) nano- aluminum oxide nanoparticles. J Proteomics 143:136–150. https​
materials during simulated wastewater treatment processes. J ://doi.org/10.1016/j.jprot​.2016.03.014
Hazard Mater 201–202:16–22. https​://doi.org/10.1016/j.jhazm​ Yata VK, Tiwari BC, Ahmad I (2018) Nanoscience in food and agri-
at.2011.10.086 culture: research, industries and patents. Environ Chem Lett
Wang Z, Xie X, Zhao J et al (2012) Xylem- and phloem-based transport 16(1):79–84. https​://doi.org/10.1007/s1031​1-017-0666-7
of CuO nanoparticles in maize (Zea mays L.). Environ Sci Tech- Yu S, Liu J, Yin Y, Shen M (2018) Interactions between engineered
nol 46:4434–4441. https​://doi.org/10.1021/es204​212z nanoparticles and dissolved organic matter: a review on mecha-
Wang Z, Zhang L, Zhao J, Xing B (2016) Environmental processes nisms and environmental effects. J Environ Sci (China) 63:198–
and toxicity of metallic nanoparticles in aquatic systems as 217. https​://doi.org/10.1016/j.jes.2017.06.021
affected by natural organic matter. Environ Sci Nano 3:240– Yuan J, Chen Y, Li H et al (2018) New insights into the cellular
255. https​://doi.org/10.1039/C5EN0​0230C​ responses to iron nanoparticles in Capsicum annuum. Sci Rep
Wibowo D, Zhao CX, Peters BC, Middelberg APJ (2014) Sustained 8(1):1–9. https​://doi.org/10.1038/s4159​8-017-18055​-w
release of fipronil insecticide in Vitro and in Vivo from bio- Yuan J, He A, Huang S et al (2016) Internalization and phytotoxic
compatible silica nanocapsules. J Agric Food Chem 62:12504– effects of CuO nanoparticles in arabidopsis thaliana as revealed
12511. https​://doi.org/10.1021/jf504​455x by fatty acid profiles. Environ Sci Technol 50:10437–10447.
Willats WGT, Mccartney L, Mackie W, Knox JP (2001) Pectin: Cell https​://doi.org/10.1021/acs.est.6b026​13
biology and prospects for functional analysis. Plant Mol Biol Yuan H, Lu T, Wang Y et al (2016) Sewage sludge biochar: nutri-
47:9–27. https​://doi.org/10.1023/A:10106​62911​148 ent composition and its effect on the leaching of soil nutri-
Wu H, Tito N, Giraldo JP (2017) Anionic cerium oxide nanoparticles ents. Geoderma 267:17–23. https​: //doi.org/10.1016/j.geode​
protect plant photosynthesis from abiotic stress by scavenging rma.2015.12.020
reactive oxygen species. ACS Nano 11:11283–11297. https​:// Yung MMN, Wong SWY, Kwok KWH et al (2015) Salinity-depend-
doi.org/10.1021/acsna​no.7b057​23 ent toxicities of zinc oxide nanoparticles to the marine diatom
Wu B, Zhu L, Le XC (2017) Metabolomics analysis of TiO2 nano- Thalassiosira pseudonana. Aquat Toxicol 165:31–40. https​://
particles induced toxicological effects on rice (Oryza sativa doi.org/10.1016/j.aquat​ox.2015.05.015
L.). Environ Pollut 230:302–310. https​: //doi.org/10.1016/j. Zafar H, Ali A, Ali JS et al (2016) Effect of ZnO nanoparticles on
envpo​l.2017.06.062 Brassica nigra seedlings and stem explants: growth dynamics
Xi ZG, Chao FH, Yang DF et al (2004) The effects of DNA damage and antioxidative response. Front Plant Sci 7:535. https​://doi.
induced by acetaldehyde. Huan Jing Ke Xue 25:102–105 org/10.3389/fpls.2016.00535​
Xiong T, Dumat C, Dappe V et al (2017) Copper oxide nanoparticle Zahra Z, Waseem N, Zahra R et al (2017) Growth and metabolic
foliar uptake, phytotoxicity, and consequences for sustainable responses of rice (Oryza sativa L.) cultivated in phosphorus-
urban agriculture. Environ Sci Technol 51:5242–5251. https​:// deficient soil amended with TiO2 nanoparticles. J Agric Food
doi.org/10.1021/acs.est.6b055​46 Chem 65:5598–5606. https​://doi.org/10.1021/acs.jafc.7b018​43

13
Environmental Chemistry Letters (2021) 19:1545–1609 1609

Zangi R, Filella M (2012) Transport routes of metalloids into and morphology and toxicity. Chemosphere 191:324–334. https​://
out of the cell: a review of the current knowledge. Chem Biol doi.org/10.1016/j.chemo​spher​e.2017.10.016
Interact 197:47–57. https​://doi.org/10.1016/j.cbi.2012.02.001 Zhang X, Xu Z, Wu M et al (2019) Potential environmental risks of
Zhai G, Walters KS, Peate DW et al (2014) Transport of gold nano- nanopesticides: application of Cu(OH)2 nanopesticides to soil
particles through plasmodesmata and precipitation of gold ions mitigates the degradation of neonicotinoid thiacloprid. Environ
in woody poplar. Environ Sci Technol Lett 1:146–151. https​:// Int 129:42–50. https​://doi.org/10.1016/j.envin​t.2019.05.022
doi.org/10.1021/ez400​202b Zhang H, Zhang Y (2020) Effects of iron oxide nanoparticles on Fe and
Zhang W, Dan Y, Shi H, Ma X (2017) Elucidating the mechanisms heavy metal accumulation in castor (Ricinus communis L.) plants
for plant uptake and in-planta speciation of cerium in radish and the soil aggregate. Ecotoxicol Environ Saf 200:110728. https​
(Raphanus sativus L.) treated with cerium oxide nanoparti- ://doi.org/10.1016/j.ecoen​v.2020.11072​8
cles. J Environ Chem Eng 5:572–577. https​://doi.org/10.1016/j. Zhang T, Zhu Z, Gong W et al (2016) Characteristics of fine parti-
jece.2016.12.036 cles in an urban atmosphere—relationships with meteorologi-
Zhang Z, He X, Zhang H et al (2011) Uptake and distribution of ceria cal parameters and trace gases. Int J Environ Res Public Health
nanoparticles in cucumber plants. Metallomics 3:816–822. 13(8):807. https​://doi.org/10.3390/ijerp​h1308​0807
https​://doi.org/10.1039/c1mt0​0049g​ Zhao L, Huang Y, Hu J et al (2016) 1H NMR and GC-MS based
Zhang K, Liu H, Song J et al (2016) Physiological and compara- metabolomics reveal defense and detoxification mechanism of
tive proteome analyses reveal low-phosphate tolerance and cucumber plant under Nano-Cu stress. Environ Sci Technol
enhanced photosynthesis in a maize mutant owing to reinforced 50:2000–2010. https​://doi.org/10.1021/acs.est.5b050​11
inorganic phosphate recycling. BMC Plant Biol 16(1):129. Zhao L, Ortiz C, Adeleye AS et al (2016) Metabolomics to detect
https​://doi.org/10.1186/s1287​0-016-0825-1 response of lettuce (Lactuca sativa) to Cu(OH)2 nanopesticides:
Zhang P, Ma Y, Xie C et al (2019) Plant species-dependent transfor- oxidative stress response and detoxification mechanisms. Environ
mation and translocation of ceria nanoparticles. Environ Sci Sci Technol 50:9697–9707. https:​ //doi.org/10.1021/acs.est.6b027​
Nano 6:60–67. https​://doi.org/10.1039/C8EN0​1089G​ 63
Zhang P, Ma Y, Zhang Z et al (2012a) Biotransformation of ceria Zhao L, Peng B, Hernandez-Viezcas JA et al (2012) Stress response and
nanoparticles in cucumber plants. ACS Nano 6:9943–9950. tolerance of Zea mays to CeO2 nanoparticles: Cross talk among
https​://doi.org/10.1021/nn303​543n H2O2, heat shock protein, and lipid peroxidation. ACS Nano
Zhang P, Ma Y, Zhang Z et al (2012b) Comparative toxicity of nano- 6:9615–9622. https​://doi.org/10.1021/nn302​975u
particulate/bulk Yb 2O 3 and YbCl 3 to cucumber (Cucumis Zhao L, Peralta-Videa JR, Ren M et al (2012) Transport of Zn in a
sativus). Environ Sci Technol 46:1834–1841. https​: //doi. sandy loam soil treated with ZnO NPs and uptake by corn plants:
org/10.1021/es202​7295 electron microprobe and confocal microscopy studies. Chem Eng
Zhang Y, Newton B, Lewis E et al (2015) Cytotoxicity of organic J 184:1–8. https​://doi.org/10.1016/j.cej.2012.01.041
surface coating agents used for nanoparticles synthesis and Zhu H, Han J, Xiao JQ, Jin Y (2008) Uptake, translocation, and accu-
stability. Toxicol Vitr 29:762–768. https​://doi.org/10.1016/j. mulation of manufactured iron oxide nanoparticles by pumpkin
tiv.2015.01.017 plants. J Environ Monit 10:713–717. https​://doi.org/10.1039/
Zhang T, Sun H, Lv Z et al (2018) Using synchrotron-based b8059​98e
approaches to examine the foliar application of ZnSO4 and Zuverza-Mena N, Medina-Velo IA, Barrios AC et al (2015) Copper
ZnO nanoparticles for field-grown winter wheat. J Agric Food nanoparticles/compounds impact agronomic and physiological
Chem 66:2572–2579. https​://doi.org/10.1021/acs.jafc.7b041​53 parameters in cilantro (Coriandrum sativum). Environ Sci Pro-
Zhang W, Xiao B, Fang T (2018) Chemical transformation of cess Impacts 17:1783–1793. https:​ //doi.org/10.1039/c5em00​ 329f​
silver nanoparticles in aquatic environments: mechanism,
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