J Mater Sci (2018) 53:185–201
REVIEW
Review
Zinc oxide nanoparticles: a review of their biological
synthesis, antimicrobial activity, uptake, translocation
and biotransformation in plants
Ajey Singh1
1
2
, N. B. Singh1,*
, Shadma Afzal2
, Tanu Singh2
, and Imtiyaz Hussain1
Plant Physiology Laboratory, Department of Botany, University of Allahabad, Allahabad, India
Department of Botany, University of Allahabad, Allahabad, U.P. 211002, India
Received: 20 May 2017
ABSTRACT
Accepted: 31 August 2017
Over the past decade, incorporation of nanomaterials into agricultural practices
like nanofertilizers and nanopesticides has gained a lot of attention. Progress
and application of fertilizers in nanoforms are one of the effective options for
considerable improvement of the agricultural yield worldwide. Zinc oxide
nanoparticles (ZnO NPs) are considered as a biosafe material for biological
species. Earlier studies have shown the potential of ZnO NPs in stimulation of
seed germination and plant growth as well as disease suppression and plant
protection by its antimicrobial activity. However, both positive and negative
effects of ZnO NPs on plant growth and metabolism at various developmental
periods have been documented. Uptake, translocation and accumulation of ZnO
NPs by plants depend upon the features of NPs as well as the anatomy of the
host plant. This review summarizes the applications of ZnO NPs as nanofertilizer in crop production and also attempts to examine and record the possible
mechanism of antimicrobial activity of ZnO NPs. Biological synthesis of ZnO
NPs and their uptake, translocation and biotransformation in plants via various
routes have also been examined.
Published online:
7 September 2017
Ó Springer Science+Business
Media, LLC 2017
Introduction
Nanotechnology provides a great possibility of novel
application in the fields of biotechnology and agricultural industries. It is the branch of technology that
deals with materials having dimensions of less than
100 nanometers (nm), especially the manipulation of
discrete atoms and molecules [1]. Nanotechnology is
considered as the application of nanoparticles (NPs)
Address correspondence to E-mail: singhnb166@gmail.com
DOI 10.1007/s10853-017-1544-1
which can be defined as a small object that behaves as
a whole unit in terms of its transport and properties.
Nanotechnology has a great potential to provide an
opportunity for the researchers to develop new tools
for incorporation of NPs into plants that could supplement existing functions and add new ones.
Interaction of NPs with plants causes several
morphological and physiological changes, depending
on the properties of NPs. The efficiency of NPs is
186
determined by different factors like their chemical
composition, size, surface covering, reactivity and
most importantly the extent to which they are effective [2]. Conventional fertilizers are being used
worldwide at high rates for augmentation in grain
production to fulfil the demand of the rapidly
growing population. Even though fertilizers are crucial for plant growth and development, the majority
of the applied fertilizers stay unavailable to plants
due to numerous aspects and few of them are
leaching, degradation by photolysis, hydrolysis and
decomposition. Therefore, it is required to decrease
the nutrient losses in fertilization and to improve the
crop yield with the help of use of new techniques and
their applications through nanotechnology and NPs.
Zinc (Zn) is the only metal found in all six enzyme
classes, viz. oxidoreductases, lyases, isomerases,
transferases, hydrolases and ligases [3]. Zinc being
essential micronutrient plays an important role in
many integral metabolic processes [4]. Zn can also help
increase the biosynthesis of chlorophylls and carotenoids and enhance the photosynthetic apparatus of
the plant [5]. Significant optoelectrical, physical and
antimicrobial properties of zinc oxide (ZnO) NPs offers
great potential to boost agriculture productivity [6].
There are some studies which report strong absorption
abilities for a series of organic compounds, heavy
metals, ZnO and its NPs [7]. ZnO NPs have a large
surface area-to-volume ratio that results in a significant increase in the effectiveness in blocking UV radiation as compared to the bulk material [8].
The impact of ZnO NPs has been evaluated in various studies on crop plants. Nanodimensional ZnO
particle enhanced germination, pigments, sugar and
protein contents with increased activities of antioxidant enzymes in various vegetable crops [9]. ZnO NPs
have significant effect on the root epidermis and cortex
of Lolium perenne with internalization of NPs in the
endodermal and vascular tissues [10]. ZnO NPs possess antimicrobial activity against many pathogenic
organisms like Escherichia coli, Pseudomonas aeruginosa,
Campylobacter jejuni. [11]. Increased yield is directly
linked to the decrease in number of pathogenic
microorganisms and also to the potential nutritional
value of the NPs themselves, mainly for the essential
micronutrients necessary for host defence [12].
ZnO NPs can be synthesized by several chemical
methods such as precipitation, vapour transport and
hydrothermal process. The biogenic synthesis of ZnO
NPs by using different plant extracts or
J Mater Sci (2018) 53:185–201
microorganisms is emerging as a new area of interest
nowadays. The biological approach to the synthesis
of NPs has an advantage over traditional chemical
and physical methods [13]. Applications of biosynthesized metallic NPs range from various biomedical
functions, viz. antimicrobial coatings, medical imaging and drug delivery to catalytic water treatment
and environmental sensors [6]. Green chemistry
reduces pollution risk at source level where the
principle focus is on the choice of reagents which are
eco-friendly. In addition, Bioresource-based green
synthesis of metal as well as metal oxide NPs has
been reported [14]. Despite several advantageous
aspects of ZnO NPs in agriculture sector, there are
some reports discussing the toxicity of ZnO NPs on
plants. The annotation of mechanisms of cytotoxicity
and genotoxicity of ZnO NPs remains an unexplored
field of study. The increasing commercial use and
extensive fabrication of engineered NPs may result in
unintended exposure to flora and fauna of the environment. Key aspects that influenced toxicity in
plants are the concentration of NPs, particle size,
surface area, stability, physicochemical properties,
plant species, plant age/phenological stage, the
medium of exposure and dilution agent [15]. It is
demonstrated that exposure of Allium cepa roots to
ZnO NPs causes cytotoxicity and genotoxicity [16]. In
another report, there was concentration-dependent
inhibition of mitotic index, which indicated the
cytotoxic potential of ZnO NPs in Allium cepa [17].
The major objective of this review is to collect,
evaluate and create the most up to date knowledge
regarding the biological synthesis of ZnO NPs and
their role in improvement of plant growth and yield.
This review also attempts to examine and record the
possible mechanism of uptake, translocation and
accumulation of ZnO NPs in plants via different
routes. Moreover, this review is proposed to provide
a critical assessment of the antimicrobial activity and
phytotoxicity of the application of ZnO NPs in plants.
Biological synthesis of zinc oxide
nanoparticles
Biological synthesis of NPs has an advantage over
conventional chemical and physical methods. In the
recent times, ‘‘green’’ method for the synthesis of NPs
has become an area of utmost interest. The focus is
applied in this direction because the use of
J Mater Sci (2018) 53:185–201
187
Figure 1 Possible mechanism
involved in biological
synthesis of zinc oxide
nanoparticles.
conventional chemical methods is expensive and
requires the use of chemical compounds or organic
solvents as reducing agents [6]. Conventional chemical reduction method involves various toxic chemicals for the synthesis of NPs which can later be a
reason for various health issues due to their toxicity,
while green synthesis method is an eco-friendly
approach to produce NPs. Green synthesis method is
free of contaminants thus favorable for biological
applications where purity is a matter of concern [18].
The use of toxic chemicals on the surface of NPs and
non-polar diluents in the chemical synthesis method
restricts their applications in clinical and biological
fields [19]. NPs synthesized by plants are more
stable and biocompatible due to the process of coating with biogenic surfactants or capping agents and
they also have reduced environmental impacts,
exhibit variations in shape and size and have a faster
rate of synthesis in comparison with the NPs produced by other organisms [19]. The faster rate of
synthesis is owed to the biological capacity to act as a
catalyst for reactions in aqueous media at standard
temperature and pressure conditions [6].
A diagrammatic representation summarizing the
possible mechanism of biological synthesis of ZnO
NPs is given in Fig. 1. In biological synthesis of NPs,
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J Mater Sci (2018) 53:185–201
Table 1 Biological synthesis of zinc oxide nanoparticles using different biological extracts
Biological entities
Precursor conditions
Shape
Size (nm)
References
Aeromonas Hydrophila
Aloe barbadensis (source gel)
Cassia auriculata (flower extract)
Hibiscus subdariffa (leaf extract)
Coriandrum sativum (leaf extract)
ZnO, 24 h at 30 °C
Zn(NO3)2, 5–6 h at 150 °C
ZnNO3, 60–80 °C
Zn(CH3COO)2H2O
Zn(O2CCH3)2(H2O)2,
overnight at 60 °C
ZnNO3, 60–400 °C
Spherical and oval
Spherical
Spherical
57.72
40
[20]
[25]
[26]
[27]
[22]
Spherical-shaped
forming
agglomerates
Spherical and granular
nature
30–35
[22]
5–40
[28]
Calotropis gigantea (leaf extract)
Rhizoctonia bataticola
Aspergillus fumigatus, Aspergillus
flavus (extracellular secretions)
Camellia sinensis (aqueous extract of
green tea leaves)
Hibiscus rosa sinensis (leaf extract)
Zn(CH3COO)2H2O,
NaOH, 60 °C
Zn(O2CCH3)2(H2O)2,
overnight at 60 °C
Zn(CH3COO)2H2O,
NaOH
Zn(CH3COO)2H2O,
NaOH
ZnO salt solution
ZnSO4, ZnO, ZnCl2 and
ZnNO3
Zn(CH3COO)2H2O,
overnight dried at 60 °C
ZnNO3
Citrus aurantifolia (fruit extract)
Lobelia leschenaultiana (leaf extract)
Zn(CH3COO)2H2O
Zn(O2CCH3)2
Calotropis procera (latex)
Acalypha indica (leaf extract)
Catharanthus roseus (leaf extract)
Elaeagnus angustifolia (flower extract)
Azadirachta indica (leaf extract)
Ixora coccinea (leaf extract)
Poncirus trifoliata (leaf extract)
Lantana aculeata (leaf extract)
Sargassum myriocystum (sea weed
extract)
Parthenium hysterophorus (leaf
extract)
Sedum alfrediihance
Spherical
23–57
[21]
Spherical
20–40
[7]
Spherical
Oval to spherical
15–25
30–70
[29]
[30]
16
[31]
Spherical and
crystalline
Spherical
Spherical and
hexagonal
Spherical
30–35
[32]
50–200
20–65
[33]
[34]
90–500
[35]
Spherical, triangular
and hexagonal
Rod shaped
45–150 nm with average
size of 75 ± 5 nm
50–180
[36]
9.6–25.5
145.1
8.48–32.5
12 ± 3
36
[38]
[39]
[40]
[41]
[42]
ZnNO3
Spherical
Spherical
Nearly spherical
Spherical
Hexagonal, triangular,
rod and radial
Spherical, hexagonal
27 ± 5, 84 ± 2
[43]
ZnNO3
Pseudo spherical
53.7
[44]
Abrus precatorius (aqueous solution of Zn(CH3COO)2H2O
seed extract)
Alternaria alternata
ZnSO4
Plectranthus amboinicus (leaf extract)
[23]
ZnO salt solution, 80 °C
for 5 h
Zn(CH3COO)22H2O
Zn(CH3COO)2H2O
ZnNO3
ZnNO3
ZnNO3
the plant/microorganism extract is simply mixed
with a metal salt solution at room temperature. The
synthesis process completes within hours. There are
plenty of reports on the green synthesis of ZnO NPs.
This report embodies some studies dealing with the
biosynthesis of ZnO NPs using different plant
[37]
extracts and few reproducible microorganisms as
eco-friendly reducing and capping agents.
Synthesis of ZnO NPs (57–72 nm, spherical), via
reproducible bacteria Aeromonas hydrophila was carried out at room temperature from ZnO solution in a
duration of 24 h. The synthesized NPs exhibited
antimicrobial activity against both Pseudomonas
J Mater Sci (2018) 53:185–201
aeruginosa and Aspergillus flavus [20]. Extracellular
synthesis of ZnO NPs (23–57 nm, spherical) was
carried out by reduction of 0.025 M aqueous zinc
acetate with an aqueous leaf extract of Catharanthus
roseus. These ZnO NPs were evaluated for antibacterial activity, and the maximum antimicrobial
activity was recorded against Pseudomonas aeruginosa
followed by Staphylococcus aureus [21]. ZnO NPs
(20–40 nm) were rapidly synthesized at room temperature by treating zinc acetate dehydrate with the
flower extract of Elaeagnus angustifolia [7], and these
synthesized particles reflected the positive effect on
growth and metabolism of tomato plant at low concentration. The synthesis of ZnO NPs by reduction of
aqueous zinc acetate dehydrate using leaf extract of
Coriandrum sativum, Calotropis gigantea and Acalypha
indica was also reported [22, 23]. The synthesis
mechanism of ZnO NPs is a complicated process and
not explored in detail. In the biological synthesis
process, ZnO produced due to reaction between
Zn?? ions coming from zinc salt and reducing agent
which can be a biological extract. Various phytochemicals viz., polyphenols, carboxylic acid, amino
acids and proteins, might act as stabilizing or growth
terminator of ZnO NPs as well as a linker molecule
between two or more ZnO NPs in making selfassembly [7, 24].
Table 1 summarizes some of the reports pertaining
to the synthesis of NPs mediated by the different
biological extracts.
Uptake, translocation and accumulation
of zinc oxide nanoparticles
Transport of NPs through environment into the
plants is the most critical factor to estimate NPs
impact on plant metabolism. Plants are an essential
component of the environment and act as a probable
pathway for the uptake, transport and accumulation
of NPs into the food chain [45]. Uptake, translocation
and accumulation of NPs depend on the plant species
and the size, chemical configuration, stability and
concentration of the NPs. The high mobility of NPs is
determined by van der Waal forces, Brownian motion
(diffusion), gravity and double-layer forces which are
responsible for their adhering property [46, 47]. The
processes of translocation and accumulation of ZnO
NPs in crops are not studied adequately. This area of
research is recent and the studies have commonly
189
been performed up to germination stage, providing
only limited information and the results obtained are
sometimes contradictory. One of the most important
factors for uptake is the size of NPs, and it is problematic for NPs of large size to enter through the
plant cell walls and transport across the plasma
membranes. Ions and water can move easily through
ion channels and aquaporins, respectively, because
the size of ions and water molecules are around
0.28 nm, whereas the cell wall pore size fluctuates in
between 2 and 20 nm [48]. The surface characteristics
of NPs are also important for their aggregation pattern, movement in aquatic and terrestrial ecosystems
and interactions with algae, plants and fungi [49].
Uptake and accumulation of ZnO NPs (8 nm) by
Glycine max seedlings were examined by LopezMoreno [50]. The Zn uptake by soybean seedlings
was higher at 500 mg L-1 due to lesser aggregation,
whereas, at high concentrations (1000–4000 mg L-1),
an increased chance for aggregate formation was
proposed, making passage difficult through the cell
wall pores consequently, reducing Zn uptake and
accumulation. Although it is expected that ZnO NP is
a source for Zn2? found within tissues but the results
in X-ray absorption spectroscopy (XAS) study fail to
figure out the source of Zn2? whether it is produced
by the biotransformation of the ZnO NP or not.
Therefore, it can be concluded that ZnO NPs ionized
by the root exudates on the root surface, as no trace of
ZnO NPs was found in XAS spectra. Similarly, in
ryegrass (Lolium perenne), SEM and TEM analyses
reveal the presence of ZnO NPs scattered in the
apoplast, cytoplasm, nuclei of the endodermal cells
and the vascular cylinder of the plant [10]. However,
results of the study were contradicted by the findings
of Wang P et al. [45] which shows that there was no
translocation detected from root to shoot in the Vigna
unguiculata plant, in spite of extensive quantity of
NPs around the root surface. Hence the Zn transfer
coefficient which is the fraction of Zn in the leaf
comparative to the root was quite low. Therefore,
restricted transport of ZnO NPs to the shoot or its
increased adhesion might be the reason of increased
accumulation of Zn in roots. On exposure to the
environment, ZnO NPs rapidly undergo dissolution
or biotransformation and the attachment of NPs to
the soil particles also explains the absence of ZnO
NPs in shoots [51, 52]. Carboxyl groups play a significant role as ligands involved in the transport and
storage of Zn in shoots [53]. In the seeds of Vigna
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J Mater Sci (2018) 53:185–201
(a)
Foliar
exposure
Entry through wound Aggregaon on leaf epidermis
Entry through cucle penetraon
(b) Root
Entry through
hydathodes
Entry through stomata
Symplasc pathway
exposure
Through injury
Soil parcles
Entry through lencel
Apoplasc pathway
Biotransformaon
ZnO NPs
Zn2+
ZnPO4
Figure 2 An overview and general principle of uptake, translocation and biotransformation pathway of zinc oxide nanoparticles
in a plant system. a Transverse cross section of the leaf showing
entry of nanoparticles through stomata, cuticle penetration,
hydathodes and wounds. b Transverse cross section of the root
showing entry of nanoparticles through lenticels, injury or
biotransformation into zinc ions and they follow apoplastic and
symplastic pathways.
unguiculata, high concentration of Zn was reported in
the outer layer of cotyledon and hypocotyl, while low
Zn concentration in the testa and inner cotyledon.
LCF examination of seeds indicated that Zn was
predominantly associated with citrate, histidine,
malate, phytate and polygalacturonic acid and precipitated in the form of zinc phosphate [45].
In recent study, Jitao et al. [54] investigated that a
large amount of Zn was taken up resulting from Zn2?
released from ZnO NPs and Zn accumulated in the
form of ZnPO4ZnO NPs adsorbed on root surfaces
move into the root cortex as a result of quick cell
division and elongation of the root tips, and hence the
ZnO NPs were detected mainly in the epidermis,
cortex, vascular system and root tip cells. ZnO NPs
enter the vascular system through the gaps of the
casparian strips at the location of the primary and
lateral root junction but no ZnO NPs were observed
to be translocated into shoots, possibly due to the
dissolution and biotransformation of ZnO NPs inside
the plants from ZnO NPs to ZnPO4 which further
limit their long-distance transport. The use of confocal microscopy technique suggested the uptake of
ZnO NPs in corn plants growing in soil [55]. It was
J Mater Sci (2018) 53:185–201
observed that aggregates of ZnO NPs entered the
root epidermis and cortex via the apoplastic pathway. However, the occurrence of ZnO NPs aggregates in xylem vessels in corn proposed the
movement through the symplastic pathway via the
endodermis. A schematic representation is given to
demonstrate the pathway for uptake, translocation
and accumulation of zinc in the form of ZnO NPs and
zinc ions in plant; for detailed understanding, the
transverse cross section of leaf and root is shown to
display possible pathways and mechanisms of
absorption, translocation and biotransformation of
ZnO NPs (Fig. 2).
Zinc oxide nanoparticles as biofertilizer
Zn deficiency is the most common micronutrient
deficiency confining crop production in the world
[56]. Studies have successfully demonstrated that the
nanopowders can be effectively used as fertilizers
[57]. ZnO NPs have potential to increase the yield
and growth of food crops. The use of ZnO NPs as a
Zn fertilizer in soil and also as a foliar fertilizer has
been proposed [58].
Apart from the property of rapid absorption, the
nanofertilizers also exhibit slow release and they are
required in scarce amount and thus can reduce fertilizer consumption and environmental pollution
[57]. ZnO NP apart from being an essential
micronutrient is also a co-factor for nutrient mobilizing and activating enzymes [59]. It is essential to
mention that selection of the suitable concentration of
NPs is vital for obtaining higher profits for an aimed
agro-economic attribute [59]. The equation given
below refers basically to the dissolution of ZnO NPs
into soluble ions in solution (water or soil solutions)
causing discharge of the micronutrient (Zn). The
amount and speed of dissolution are considerably
higher than bulk fertilizers due to the reduced particle size and greater specific surface area of ZnO
NPs.
ZnO(NPs) þ H2 O , Zn2þ þ 2OH
Triticum aestivum grown in acidic and alkaline soils
amended with ZnO NPs exhibited 200 times higher
soluble Zn content in the acidic soil and ten times
higher concentration of Zn in wheat shoots, compared to the alkaline soil [60]. On the other hand,
plants grown in the alkaline soil amended with a
191
concentration of 500 mg kg-1 of ZnO NPs resulted in
an increase in lateral root production while those in
the acidic soil decreased root growth.
Exogenously synthesized ZnO NPs using extracellular secretions of Aspergillus fumigatus affected
Cyamopsis tetragonoloba when applied by foliar treatment [61]. Shoot length (22.7%), root length (43.4%),
total protein content (17.2%), chlorophyll content
(54.5%) and rhizosphere microbial population
(13.6%) increased significantly. A similar observation
has been recorded on the growth of Pennisetum
americanum using Zn NP (10 mg L-1) biosynthesized
by Rhizoctonia bataticola [29].
Raliya et al. [59] studied the influence of ZnO NPs
(25 ± 3.5 nm) on the tomato plant. The authors considered parameters such as plant life cycle, fruit
yield, total biomass, nutritive value and chlorophyll
contents. The results from the study specified an
optimum concentration of ZnO NPs which promoted
the plant development while no stimulation was
reported beyond the optimum concentration. The
foliar application was more effective than soil treatments. The authors reported that the highest stimulation in plant height, root length and biomass was
observed at a concentration of 250 mg kg-1, whereas
maximum lycopene content and fruit yield at
100 mg kg-1 and improved chlorophyll content at
750 mg kg-1 concentration.
The seeds of Arachis hypogea treated with different
concentrations of ZnO NPs (25 nm) affected the plant
growth factors such as seed germination, seedling
vigour index, root growth, flowering, chlorophyll
content and pod yield [62]. It has been reported that
ZnO NPs at a concentration of 1000 ppm promoted
seed germination as well as seedling vigour and
increased stem and root growth. The early germination and establishment of seeds in soil resulted in
early flowering and increased chlorophyll content in
leaf.
ZnO NPs (15–40 nm) were synthesized using the
flower extract of Elaeagnus angustifolia [7]. The effect
of different concentrations of ZnO NPs and zinc
sulphate (ZnSO4) on Solanum lycopersicum was
reported. The authors observed an increase in germination rate, seedling vigour, pigment, protein and
sugar content at a concentration of 1.2 mM with
respect to control and ZnSO4ZnO NPs in 3.0 mM
concentration successfully decreased the MDA and
SOD contents. Leaves of plants exposed to 6.1 mM
concentration of ZnO NPs recorded utmost
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J Mater Sci (2018) 53:185–201
Table 2 Positive impact of zinc oxide nanoparticles in different plant species
NPs
Size
(nm)
ZnO
NPs
ZnO 25
NPs
ZnO
NPs
ZnO
NPs
ZnO
NPs
ZnO
NPs
ZnO
NPs
ZnO
NPs
ZnO
NPs
Concentrations
Test plants
Effects
References
800 mg kg-1
Cucumis sativus
(fruit)
Arachis hypogaea
Enhanced growth and increase in dry weight
[66]
Increased germination, chlorophyll, stem and root growth
and pod yield (29.5%)
Increase in dry weight
[62]
Increase in shoot height (6%), shoot biomass (27%), root
length (53%) and root biomass (37%)
Root elongation and increased seed germination
[68]
[69]
Increase in shoot dry weight
[70]
1000 ppm (foliar
spray)
500, 1000, 2000 and Vigna radiata
4000 ppm
Cicer arietinum
1 mg L-1
(chickpea seedlings)
Brassica napus (rape
2 mg L-1
seed)
1.5 ppm (foliar
Cicer arietinum L var.
spray)
HC-1
20 mg L-1
Vigna radiata (mung
bean)
Lolium perenne
2 mg L-1
(ryegrass seed)
20 ppm
Vigna radiata
(suspension, foliar
spray)
ZnO
2 ppm
Zea mays corn (SC
NPs
704)
ZnO 1.2–6.8 10 ppm
Cyamopsis
NPs
tetragonoloba
Lupinus termis
ZnO
60 mg L-1
NPs
Triticum aestivum
ZnO 20–50 1000 mg L-1
(wheat)
NPs
ZnO
2 mg L-1
Raphanus sativus
NPs
(radish)
Glycine max
ZnO
500 mg L-1
(soybean)
NPs
Allium cepa (onion)
ZnO 20
20 lg mL-1
NPs
Pennisetum glaucum
Zn
15–25 10 mg L-1
(pearl millet)
NPs
ZnO [100
10 mg L-1
Brassica nigra (black
NPs
mustard)
ZnO
9 lM
Cabbage, cauliflower
NPs
and tomato
[67]
Increase in shoot height (98%) shoot biomass (76%), root [68]
length (42%) and root biomass (41%)
Enhanced growth of seedlings and root elongation
[69]
Increase in biomass
[71]
Increase in shoot dry matter and leaf area index by 63.8
and 69.7%
Increased biomass, root and shoot length, chlorophyll
content and protein synthesis
Decreased MDA and Na content, improved salt tolerance
in plant
Increased pigment and protein content
[72]
[61]
[73]
[26]
Improved root elongation in germinated seeds
[69]
Increased root growth
[50]
Increased seed germination
[74]
Enhanced shoot (10.8%), chlorophyll content (18.4%) and [29]
grain yield (29.5%)
Shoot emergence, root hair formation and enhanced radical [75]
scavenging activity
Increased pigment and protein content
[9]
reflectance. In the study of Ates et al. [63], it has been
reported that the suspensions of Zn NPs induced
more toxicity than ZnO NPs to Artemia salina larvae.
Authors of this study concluded that this effect was
associated with prominent release of free Zn2? from
Zn NPs into exposure medium. Moreover, both Zn
and ZnO NPs exhibited differences in toxic impacts
depending on the size of their nanopowders, viz. the
smaller size NPs were found to be more toxic.
Some of the applications reported in this review are
summarized in Table 2 which shows examples taking
into account of the ZnO NPs, their size and concentration, the plant species and the observed positive
effects. Peng et al. [64] reported that aggregation and
dissolution of NPs and ROS generation by NPs can be
influenced by many factors, including the size,
shapes and surface charge of NPs. The shape of NPs
can affect both the equilibrium concentrations and
J Mater Sci (2018) 53:185–201
193
Figure 3 Possible affirmative
and negative impacts of zinc
oxide nanoparticles on plant
growth and metabolism.
rates of their dissolution. In the study of Misra et al.
[65], it was reported that the dissolved rate of
spherical NPs was faster than that of rod and spindleshaped NPs.
Figure 3 shows some of the positive and negative
effects of ZnO NPs as fertilizer in agricultural crops
as reported by various researchers. ZnO NPs have
both positive and negative impacts on germination,
growth, biomass, leaf area, radical scavenging activity, shoot and root length, protein content, photosynthetic pigments and yield.
Antimicrobial activity of zinc oxide
nanoparticles
Vigneshwaran et al. [76] were the first to publish
reports on antimicrobial effects of biosynthesized NPs.
These NPs exhibit antifungal, anticorrosive, antibacterial properties due to increased specific surface area,
reduced particle size, enhanced particle surface reactivity and abrasive surface texture or surface defects
[77]. ZnO NPs have recently shown to provide effective pathogen growth control as they have lower toxicity as well as positive impact on soil fertility [78]. The
chemically synthesized ZnO NPs have been found to
be convincing antibacterial agents because they have
the ability to absorb UV radiation [79]. There are
numerous reports stating that Gram-positive bacteria
are probably extra sensitive to ZnO NPs than Gramnegative bacteria [38]. In this report, we have conferred
various studies that described the antimicrobial effect
of ZnO NPs on various microbes (Table 3).
ZnO NPs (9.6–25.5 nm, spherical) synthesized via
Azadirachta indica (neem) leaf extract have been used
for their high antibacterial impact. The study reported the antibacterial activity of ZnO NPs against
Staphylococcus aureus, Streptococcus pyogenes and
Escherichia coli at wide range of concentration. The
percentage of bacterial growth reduction was found
to be 69.2, 57 and 52% for E. coli, S. aureus and S.
pyogenes, respectively [38].
ZnO NPs can inhibit and destroy food-borne
pathogens [80, 81]. In the report of Kaur et al. [80], the
bactericidal activity of ZnO NPs (8–10 nm) against
E. coli DH5a and S. Aureus was effective at 80 and
100 gm L-1. ZnO NPs disordered and degenerated
the cell membrane of bacteria causing cytoplasmic
leakage. The NPs which act as bactericidal agents on
the food surface where bacteria reside, hinder the
growth of bacteria thus preventing food spoilage [82].
This type of packaging is called antimicrobial packaging, where direct interaction occurs between the
product and the NPs leading to the killing or
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J Mater Sci (2018) 53:185–201
Table 3 Antimicrobial activity of zinc oxide nanoparticles
NPs and
concentrations
Growth media
Pathogens
Effects
References
ZnO NPs
Culture
Inhibition in growth of bacterial cell
[90]
ZnO NPs
100 mg L-1
ZnO NP
Culture
Escherichia coli and
Staphylococcus aureus
Mucor plumbeus
Inhibition of spore germination
[91]
Fusarium graminearum
Reduced growth 26%
[92]
Pseudomonas aeruginosa
High suppression in growth
[20]
Culture media
and milk
Listeria monocytogenes
and Bacillus cereus
Inhibited growth (63–80%) and (61–91%), respectively,
hyphal malformation and fungal death
Beneficial effect
Inhibitory effect
20% decrease in fungal germination and 15% reduction in
hyphal growth
Growth inhibition
[93]
Soil
Culture
Plating assay
Botrytis cinerea and
Penicillium expansum
Pseudomonas putida
Klebsiella pneumoniae
Fusarium oxysporum
ZnO NPs
25 lg mL-1
ZnO NPs
3–12 mM
ZnO NPs
ZnO NPs
ZnO NPs
ZnO NPs
10 mM
Mung bean
broth agar
Culture
Plating assay
inhibition of bacterial growth on food surface [83].
ZnO NPs (36 nm) have been synthesized using Sargassum myriocystum (brown seaweed) [42]. The
authors reported that ZnO NPs exhibited moderate
activity against Gram-positive bacteria like Streptococcus mutants, Vibrio cholerae and Neisseria gonorrhoea
and low activity against Gram-negative bacteria such
as Micrococcus luteus and Klebsiella pneumoniae. The
reason might be related to the structural difference of
bacterial cell as Gram-positive bacteria posses single
cytoplasmic membrane with multilayer of peptidoglycan polymer and a thicker cell wall, whereas
Gram-negative bacteria wall possess two cell membranes, an outer membrane and a plasma membrane
with a thin layer of peptidoglycan. Therefore, NPs
size can readily pass through the peptidoglycan and
hence are highly susceptible to damage.
The antimicrobial effect of ZnO NPs (50 nm,
spherical) on Campylobacter jejuni, E. coli O15:H7 and
Salmonella enteritidis was studied [11]. Bacteria cultured on agar plates and in broth recorded that the
growth of C. Jejuni was completely inhibited at
C0.03 mg mL-1 of ZnO NPs, whereas the concentration for growth inhibition in E. coli O157:H7 and S.
enteritidis was 0.4 mg mL-1. In this study, it was
observed ZnO NP behaved as a bactericidal but not
bacteriostatic agent for C. jejuni.
ZnO NPs (60–70 nm) synthesized using Trifolium
pratens flower extract and their antibacterial activity
[90]
[31]
[94]
[95]
was tested against P. aeruginosa ATCC 6749, S. aureus
ATCC 4163, E. coli ATCC 25922, S. Aureus and P.
aeruginosa. The synthesized ZnO NPs exhibited high
activity against S. Aureus ATCC 4163, E. coli ATCC
25922, S. aureus at 1028 lg mL-1 and maximum zone
of their growth inhibition was 31 mm, while in P.
aeruginosa and P. aeruginosa ATCC 6749 high activity
was observed at 516 lg mL-1, whereas maximum
zone of growth inhibition was 24–26 mm [84].
Other proposed antibacterial mechanisms of ZnO
NPs include direct interaction between ZnO NPs and
bacterial cells that affect cell membrane permeability
following disorganization of the membrane and
changing the protein structure [85, 86]. The entry of
ZnO NPs as a result of proton motive force and
uptake of toxic dissolved zinc ions causes oxidative
stress inside bacterial cell and generation of reactive
oxygen species (ROS). The toxicity of ROS to bacteria
is accredited to their high reactivity and oxidizing
property, the reactive species including hydrogen
peroxide (H2O2), OH- (hydroxyl radicals) and O2
2
(peroxide) [49, 87]. The toxicity of these species
includes damage of cellular components such as
lipids, DNA and proteins, as a result of their incorporation into the bacterial cell membrane. ZnO NPs
activate the respiratory enzymes as well, causing
inadequate mitochondrial functioning and inhibition
of cellular metabolism as well as in outflow of cytoplasmic contents ultimately causing cell growth
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J Mater Sci (2018) 53:185–201
inhibition and or bacterial cell death [88, 89]. A
schematic representation of interaction between ZnO
NPs and bacterial cell has been demonstrated in
Fig. 4. Uptake of ZnO NPs causes disruption of the
cell wall and depletion in intracellular content as well
as the disturbance in DNA replication, releasing
metallic ions and ROS generation in the bacterial cell.
Cellular and genotoxicity of zinc oxide
nanoparticles in plants
The increase in the production of ZnO NPs and their
use in diverse areas undoubtedly lead to destructive
impact on the environment and exhibit toxicity in
biological species. Studies at proteomic, genomic and
Figure 4 Schematic
presentation of possible
antimicrobial mechanisms of
zinc oxide nanoparticles. a
Attachment of NPs to the cell
surface of bacteria directly. b
Disruption of membrane and
leakage of cytoplasmic
content, inhibition of
respiratory dehydrogenases
and electron transport system,
ATPase complex and
generation of ROS and
reactive species including
hydrogen peroxide (H2O2),
OH- (hydroxyl radicals) and
O2
2 (superoxide), dysfunction
of mitochondria, inhibition of
DNA replication in plasmid,
DNA denaturation.
c Oxidative damage, DNA
damage and other organelle
damage due to excess
production of ROS leading to
cell death.
(a)
(b)
(c)
metabolic stages are still needed because physiological and visual toxicological impacts in higher plants
might not be a sensitive indicator of toxicity. Zn is an
essential element used in a majority of biochemical
and physiological processes within plants [96]. Most
plants require only minute quantity of Zn
(0.05 mg L-1) in soil solution for normal growth;
therefore, higher levels of Zn may lead to phytotoxicity [57] (Table 4).
The cellular and genotoxicity of ZnO NPs in plants
are related with stimulation of lipid peroxidation and
oxidative stress [97]. Toxicity may also arise due to
particle dissolution in the nutrient solution and particle adhesion onto the root surface, rather than the
uptake of NPs. Zn2? release by ZnO NPs as a result of
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J Mater Sci (2018) 53:185–201
Table 4 Negative effects of zinc oxide nanoparticles on plant growth and metabolism
NPs and size Exposure
(nm)
concentrations
ZnO NPs
ZnO NPs
10–25 nm
ZnO NPs
ZnO NPs
ZnO NPs
ZnO NPs
Zn NPs
ZnO NPs
9–37 nm
ZnO NPs
ZnO NPs
ZnO NPs
ZnO NPs
10–15 nm
ZnO NPs
ZnO NPs
50–100 nm
Test plants
Effects
References
500–4000 mg L-1 Prosopisjulifra velutina Increase in CAT activity in roots, stems and leaves; POX
increased only in stems and leaves
500 and
Brassica oleracea
Inhibition of germination and root growth (40.6%)
1000 lg mL-1
Allium cepa
Inhibition of root growth
20 lg mL-1
2000 lg mL-1
Arachis hypogaea
Reduced crop growth and pod yield
100 lg mL-1
Allium cepa
Mitotic index decreased with increase in pycnotic cells,
cellular dysfunctions
Cicer arietinum
Decreased root biomass
10 lg mL-1
2000 mg L-1
Radish, rape, ryegrass, Highly reduced root growth
lettuce, corn,
cucumber
(Lollium perenne)
Reduced biomass, shrank root tips, epidermis and root caps
1000 mg L-1
ryegrass
were broken, highly vacuolated and collapsed cortical cells
Cucurbita pepo
Reduced biomass (78–90%)
1000 mg L-1
(zucchini)
Glycine max (soybean) Decreased root growth
4000 mg L-1
2000 mg L-1
Corn, radish, rape,
Reduced germination and highly reduced root growth
ryegrass, lettuce,
cucumber
Sesamum indicum
Decreased photosynthetic pigment, biomass and protein
1 and 2 g L-1
content
Fagopyrum esculentum Marked decrease in initial growth
1 and 2 g L-1
500 mg L-1
Oryza sativa (rice)
Stunted root length and reduction in number of roots
dissolution or transformation of NPs is possibly
another reason for toxicity, and it was also hypothesized that ZnO NPs became transformed into Zn2? on
the root surface or inside it [45]. These outcomes are
in accordance with previous reports which concluded
that the toxicity of ZnO NPs was solely due to solubilized Zn2? [98–100]. An experiment was conducted
by Wang X. et al. [101] to study the toxic effects of
ZnO NPs at a concentration of 300 mg mL-1 on
Arabidopsis. The authors reported the inhibition of
plant growth resulting in reduced rosette size, generation of oxidative stress in plant, [50% decrease in
chlorophyll a and b which directly led to 50% drop in
net rate of photosynthesis, transpiration, stomatal
conductance in leaf and intercellular CO2 concentration. Authors of this study also observed up to five
times down-regulation in levels of genes expression
of CHLOROPHYLLAOXYGENASE (CAO), CHLOROPHYLLSYNTHASE (CHLG) etc. The exact toxicity
mechanism needs elaboration. It is possible that the
[105]
[106]
[107]
[62]
[17]
[67]
[69]
[10]
[108]
[50]
[69]
[109]
[110]
[111]
Zn2? release by ZnO NPs into the soil may be partially accountable for the lethal effects of ZnO NPs
[102].
Cytotoxicity of ZnO NPs at a concentration of
4000 mg L-1 was studied by Lopez-Moreno et al. [50]
in soybean seedlings. They used random amplified
polymorphic DNA (RAPD) technique to inspect
genotoxicity by detecting new DNA bands in the
RAPD profile. The toxicity may arise due to the
interaction of the plant genome with the Zn ions
released by the ZnO NPs or with the direct interaction of DNA with the ZnO NPs, but the results from
the XANES study (absence of ZnO NPs in plant tissues) failed to determine the precise reason for
genotoxic response of ZnO NPs in soybean. In
another study, ZnO NPs at 4000 mg L-1 exhibited
toxic effects and decreased seed germination in
tomato, alfalfa, cucumber and soybean. Although
reduce seed germination was reported in corn at a
concentration of 500 mg L-1 [103]. It is important to
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J Mater Sci (2018) 53:185–201
note that the majority of plants displayed
detectable signs of reciprocity of NP toxicity specifying that toxicity was temporary [104].
Conclusion and future aspects
This review highlights the possible role of ZnO NPs
applications in area of agricultural development. In
the present review, we have discussed the various
aspects like eco-friendly biogenic synthesis of ZnO
NPs, mechanism of their uptake, translocation and
accumulation in plants and possible impact of ZnO
NPs in the agricultural field as nanofertilizer
enhancing the crop productivity. Moreover, protection of plants to microbes by the antimicrobial
activity of ZnO NPs has also been discussed. Various
physiological and biochemical toxicity caused by
varied concentration of ZnO NPs have also been
summarized.
NPs synthesized by biological entities are more
stable and biocompatible due to the process of coating with biogenic surfactants or capping agents, and
they also show reduced hazardous impacts on the
environment as no toxic chemicals involve in this
process. The process of uptake, translocation and
accumulation of ZnO NPs in crops is not studied
adequately as many of the studies have commonly
been performed until germination stage only. In this
review, we tried to draw an outline for the probable
pathways of uptake, translocation and accumulation
of zinc in the form of ZnO NPs and zinc ions in
plants. Despite several beneficial roles of ZnO NPs in
agriculture sector, the heavy use of ZnO NPs in
various industries certainly leads to negative impact
on the environment and exhibits toxicity on flora and
fauna.
Although plenty of studies dealing with phytotoxicity, uptake and accumulation of ZnO NPs have
been conducted in the last few years, we are still in
the early stage of this area and various questions
need to be answered. The probable connection
between the different characteristics of NPs like their
surface area, size and shape with their performance
in biological applications has to be investigated.
There is need to understand the relationship between
plant species and environmental factors with the
uptake and accumulation of NPs. Plenty of studies
stated the different resistivity of NPs by different
plant species, yet the reason of how and why
different plant species exhibit dissimilar behaviour to
ZnO NPs is to be explored. There are limited reports
to describe the biotransformation of NPs in food
crops and their transmission to the subsequent generation. The potential biomagnification of NPs in the
food chain is also unidentified. Although this review
summarizes the potential application of ZnO NPs in
various agricultural sectors, additional examination
and research are needed to understand the possibilities of ZnO NPs application in agriculture.
Acknowledgement
The authors are thankful to the University Grant
Commission (UGC), New Delhi, India, and University of Allahabad, India, for providing financial
assistance to Ajey Singh.
Compliance with ethical standards
Conflict of interest There is no conflict of interest
for this manuscript.
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