Review

pubs.acs.org/JAFC

Nanofertilizer for Precision and Sustainable Agriculture: Current

State and Future Perspectives
Ramesh Raliya,*,† Vinod Saharan,‡ Christian Dimkpa,§ and Pratim Biswas*,†
†
Washington University in St. Louis, St. Louis, Missouri 63130, United States
‡
Maharana Pratap University of Agriculture and Technology, Udaipur, Rajasthan 313001, India
§
International Fertilizer Development Center, Muscle Shoals, Alabama 35662, United States

ABSTRACT: The increasing food demand as a result of the rising global population has prompted the large-scale use of
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fertilizers. As a result of resource constraints and low use efficiency of fertilizers, the cost to the farmer is increasing dramatically.
Nanotechnology offers great potential to tailor fertilizer production with the desired chemical composition, improve the nutrient
use efficiency that may reduce environmental impact, and boost the plant productivity. Furthermore, controlled release and
targeted delivery of nanoscale active ingredients can realize the potential of sustainable and precision agriculture. A review of
nanotechnology-based smart and precision agriculture is discussed in this paper. Scientific gaps to be overcome and fundamental
questions to be answered for safe and effective development and deployment of nanotechnology are addressed.
KEYWORDS: nanofertilizer, nanotechnology, smart and precision agriculture, nanoparticle aerosol technology, plant nutrition,
agrochemicals

1. INTRODUCTION applied using these methods is lost to the atmosphere or

The world’s agricultural zones are facing a wide spectrum of surface water bodies, thereby polluting ecosystems.15,16 For
challenges, such as stagnation in crop yields, low nutrient use example, excess nitrogen is lost through volatilization as NH3 or
efficiency, declining soil organic matter, multi-nutrient emission as N2O or NO or through NO3 leaching or runoff to
deficiencies, shrinking arable land, water availability, and water bodies. In contrast, excess phosphorus becomes “fixed” in
shortage of labor as a result of an exodus of people from soil, where it forms chemical bonds with other elements, such
farming.1,2 Data compiled by the Food and Agriculture as Ca−P, Mg−P, Al−P, Fe−P, and Zn−P, and becomes
Organization of the United Nations (FAO) indicate that unavailable for uptake by the plants. Eventually, rain washes the
depletion and degradation of land and water pose serious nitrogen and phosphorus compounds into waterways such as
challenges to producing enough food and other agricultural rivers, lakes, and the sea, where they can cause serious pollution
products to sustain livelihoods and meet the needs of the problems.16 Fertilizer use worldwide is increasing, along with
world’s ever increasing population.3 Nanotechnology, designing global population growth. Currently, farmers are using nearly
ultrasmall particles having exceptional properties, such as 85% of the world’s total mined phosphorus as fertilizer,
surface area/volume size ratio and enhanced optoelectronic although the plants can uptake only about 42% of the applied
and physicochemical properties, compared to their bulk phosphorus.17 If this scenario persists, the world’s supply of
counterparts,4 is now emerging as a promising strategy to phosphorus could run out within the next 80 years, affecting
promote plant growth and productivity.5−8 This idea is part of agricultural productivity.17,18 In the United States, trends from
the evolving science of precision agriculture, in which farmers 1978 to 1987 suggest that metropolitan-influenced counties
make use of technology to efficiently use water, fertilizer, and experienced a decline in cropland of 77%.19,20 To meet the
other inputs. Precision farming makes agriculture more food demand, farmers apply more chemical fertilizers, which
sustainable by reducing the waste and energy demand.9 In eventually affect soil and environmental health and reduce
agriculture, nanotechnology and its derivative outcomes are natural resources. Some crops can be grown under artificial
being evaluated for various applications, such as nanoscale conditions using hydroponic techniques, but the cost (in
sensors for sensing nutrients, pesticides, and contamination, energy and dollars) is approximately 10 times that of
postharvest processing of agriculture products for improved conventional agriculture. Such systems are neither affordable
shelf life, nanoscale pesticides for effective control of plant nor sustainable for the future.21 Therefore, it is necessary to
diseases, smart and target delivery of biomolecules and develop sustainable strategies that result in more nutritious and
nutrients, agronomic fortifications, water purification, nutrient
recovery, and smart fertilizers and their delivery.4,5,8,10−14 In
Special Issue: Nanotechnology Applications and Implications of
this review, we focused on nanotechnology for smart fertilizers,
Agrochemicals toward Sustainable Agriculture and Food Systems
herein termed “nanofertilizers”.
Fertilizers provide nutrients needed by the plants for optimal Received: May 9, 2017
productivity. Farmers typically apply fertilizers through the soil Revised: August 18, 2017
by either surface broadcasting, subsurface placement, or mixing Accepted: August 23, 2017
with irrigation water. However, a large portion of fertilizers Published: August 23, 2017

© 2017 American Chemical Society 6487 DOI: 10.1021/acs.jafc.7b02178

J. Agric. Food Chem. 2018, 66, 6487−6503
Journal of Agricultural and Food Chemistry Review

Figure 1. Comparative analysis of possible pros and cons of the conventional approach with respect to nanotechnology-mediated agriculture
production. The impact on the rhizosphere as well as the environment is elucidated. Red color text represents potential negative impacts of a
technology. (∗) Note that the influence of the nanofertilizer further depends upon the plant growth and the soil rhizosphere depends upon the
nanoparticle type, composition, and exposure concentration.

enhanced crop production by minimizing the use of resources the plants, allowing for efficient uptake or slow release of active
and fertilizers. In contrast to conventional fertilizer use, which ingredients. Conventional bulk fertilizers have low plant uptake
involves 80−140 or more kg of inputs per hectare under efficiencies, and thus, larger amounts have to be applied. Two
intensive production systems, nanotechnology focuses on the main challenges of the low nutrient uptake efficiency for
use of smaller quantities. Moreover, nanoscale fertilizer may nitrogen- and phosphorus-based fertilizers are the rapid
have potential to minimize nutrient losses through leaching and changes into chemical forms that the plants do not take up
avoid rapid changes in their chemical nature, thus enhancing and runoff, leaching, or atmospheric losses. The resultant
nutrient use efficiency and addressing fertilizer environmental effects are emission of harmful greenhouse gases (such as
concerns. certain oxides of nitrogen) and eutrophication, with negative
It is worth noting that the definition of “nanofertilizer” is consequences for soil and environmental health. Therefore, it is
debatable. In the literature related to nanotechnology critical to develop smart fertilizers that are more readily taken
application in agriculture, nanofertilizer is used for both up by the plants. Nanotechnology is one possible route for
materials of a physical diameter between 1 and 100 nm in at sustainably and precisely attaining this objective, for which
least one dimension (e.g., ZnO nanoparticles) and those reason scientists are actively researching a range of metal and
existing at the bulk scale with more than 100 nm in size but that metal oxide nanoparticles for use in plant science and
have been modified with nanoscale materials (e.g., bulk agriculture.5 However, environmental health and safety aspects
fertilizer coated with nanoparticles). Therefore, in this review, of nanotechnology should also be considered, and it is crucial
the term “nanofertilizer” refers to true nanomaterials and nano- to determine the toxicity/biocompatibility of nanofertil-
enabled bulk materials used as fertilizers. As a result of their izers.24−27 Because nanoscale particles are smaller in dimension
unique properties, nanoparticles may influence metabolic compared to bulk particles, the plants can absorb them with
activities of the plant to different degrees compared to different dynamics than bulk particles or ionic salts, which
conventional materials and have the potential to mobilize presents an added advantage.26,28−30
native nutrients, such as phosphorus, in the rhizosphere.22,23 A A number of inorganic, organic, and composite nanomateri-
comparative schematic of fertilization strategies attempted in als have been tested on various the plants to assess their
the past and a hypothesized nanotechnology-based agri-input is potential impact on plant growth, development, and
illustrated in Figure 1. productivity. A brief summary of the nanoparticles used as
In the following sections, recent literature relevant to nutrients/fertilizers and validated on agriculturally important
nanoscale material/nanoparticles/nanocomposites used for crops is presented in Table 1. To be on focus, we have limited
plant nutrition as nanofertilizers is reviewed. The discussion this review to the technical aspects of nanofertilizers and their
is presented systematically to allow for a better understanding application. For information regarding aspects of the
of both fundamental and applied aspects of nanofertilizers for commercial and socioeconomic impacts of nanofertilizers,
sustainable and precision agriculture. readers are directed to a perspective recently published in
this journal.12 Because the effects of nanoscale materials and
2. NANOFERTILIZERS corresponding plant responses depend upon various factors
Nanofertilizers are nutrient fertilizers composed, in whole or related to nanoscale properties, soil, and environment, the table
part, of nanostructured formulation(s) that can be delivered to included the information on the type of nanoparticles,
6488 DOI: 10.1021/acs.jafc.7b02178
J. Agric. Food Chem. 2018, 66, 6487−6503
 Table 1. Nanomaterials That Influence Plant Growth and Development
nanoparticle property
concentration
type of nanoparticle size (nm) (ppm) mode of treatment plant plant observation
Essential Plant Nutrient
carbon 1.5−5 5−500 nutrient media and foliar tomato;102,161,162 tobacco99,101,162 promote upregulation of stress-related genes; promote in vitro growth and
uptake; seed treatment biomass
carbon-based nanoparticles (CNT, wheat;163 gram103,164 enhanced root elongation
graphene); MWCNT; SWCNT; bitter melon165 improving crop yield and seed quality
fullerol
saltmarsh cordgrass166 reduce heavy metal toxicity and stress
soybean102,167,168
corn, barley, rice,
switchgrass102,168
nitrogen <200 50 kg/ha soil exposure rice11,33 slow release of nitrogen
urea HA improved rice yield
phosphorus <50 10−100 soil and foliar applications cotton;43 pearl millets42 protect against oxidative stress
Journal of Agricultural and Food Chemistry

CaPO4, CMC−HA, phosphorite mobilize native P and enhance uptake

Zn-induced P beans38,40,41 enhances plant growth and yield
wheat, rye, pea, barley, corn,
buckwheat, radish, cucumber39
magnesium <10 15 foliar clusterbean169 improving biomass, chlorophyll content, and phenological growth
MgO
manganese 20 0.1−1 seed mung bean170 improve nitrogen uptake and metabolism

6489
copper >10 100−1200 foliar and seed treatment corn,22 tomato171 enhanced seedling growth, plant biomass, and biochemical activities
Cu−chitosan
zinc 20−30 10−2000 foliar application; seed peanut172 increase yield potential and plant growth
ZnO application beans29,40,41,47 enhance phytohormone level and plant growth
tomato48 help reduce drought stress and improve agronomic fortification
cotton43
maize30
iron 10−100 1.5−4000 foliar spray wheat;65 watermelon49,64 enhance photosynthesis rate, chlorophyll content, biomass, grain yield, and
nutritional quality
iron oxide clover;66 soybean67,68,173 improving plant growth
rice;69 tomato174 enhance nutrient absorption by enhancing microbial enzyme activity in
peanut;70 corn62 rhizosphere
pumpkin63
Non-essential Plant Nutrient
titanium 5−100 200−600 seed, soil, and foliar spinach80−82,88−92,175 increased plant biomass and photosynthetic activity
TiO2 exposure Lemna minor83 enhanced biochemical enzyme activity and light absorption by chloroplast;
increase photosynthesis, RuBISCO activity and carbon fixation
tomato;48,174 wheat84 increased germination rate
watermelon;49 mung bean;85 moth enhanced nitrogen metabolism
bean87
pearl millet87
clusterbean86,87
cerium 8−30 0.1−250 irrigation; seed/root tomato176,177 improved plant growth and yield
Review

DOI: 10.1021/acs.jafc.7b02178
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Journal of Agricultural and Food Chemistry Review

nanoscale property, mode of nanoparticle delivery, tested

increase nutrient absorption by enhancing microbial activity in rhizosphere

plants, and studied responses. In the following subsections, we
discuss specific examples of nanoparticles used as nanofertilizers

enhance germination and growth; enhancement in total protein and

or nanonutrients.
2.1. Nitrogen (N). N is one of the key nutrients, categorized
as a primary macronutrient; it is, however, deficient in most
agriculture soils. Although the atmosphere consists of more

help overcome salinity stress and enhance plant growth

than 78% N, plants cannot use N in its atmospheric form. The
plant needs specific chemical forms of N, namely, nitrate and
improved physiological and molecular response

improved physiological and molecular response

ammonium. All commercial N fertilizer manufacturing begins

observation

with a source of hydrogen gas and atmospheric N that are

increase stress tolerance enzyme activity

promoted seedling growth and quality

reacted to form ammonia, in a reaction known as the Haber−
Bosch process.31 Nitrogen fertilizers clearly make a very
influence phytostimulatory effect

essential contribution to maintaining an adequate supply of

nutritious food by influencing plant growth and development.31
N in urea, a commercial N fertilizer, vanishes approximately
promote plant growth

chlorophyll content

promote root growth

75% soon after application as a result of rapid volatilization and
leaching. The current N fertilizers, therefore, face the problem
of low utilization efficiency (<20%), whereby loss of N in the
environment causes eutrophication and greenhouse gas
increase.32 Recently, a group from the Sri Lankan Institute of
Nanotechnology developed an advanced N nanofertilizer using
urea-coated hydroxyapatite nanoparticles (rod-shaped struc-
tures, with an average aspect ratio of 10) for targeted delivery
Arabidopsis thaliana;182 clover66

and slow release of N.33 Urea−hydroxyapatite nanoparticles

Arabidopsis thaliana178,179

were selected as a result of their chemical compatibility and rich

Arabidopsis thaliana179

N and phosphorus sources, respectively. The nanohybrid of

cilantro;180 wheat181
plant

urea-modified hydroxyapatite, synthesized with N weight of

Non-essential Plant Nutrient

wheat, lupin185

Larix olgensis71
mung bean183

40%, releases N 12 times slower than conventional urea.

tomato72,184

Moreover, field trials with rice showed that slow release

poplars182

tomato186

properties of the nanohybrid resulted in better yield at a 50%

lower concentration of urea (Figure 2). A subsequent goal
would, therefore, be to optimize the nanoscale N fertilizer to
soil irrigation; seed and root

maximize its potential in a range of arable soil types by

mode of treatment plant

following quantitative−structural area relationship models.11

2.2. Phosphorus (P). Along with N, P is essential to all
hydroponics; soil

sprouts exposure

living organisms. More than 90% of globally mined P is used for

root exposure

food production. Rock phosphate (RP) is the starting raw

exposure
seed/root

material used to manufacture most commercial phosphate

fertilizers available in the market. Global RP reserves are very
limited and, according to the geological estimates, will last only
the next 100 years. However, the consumption rate of P
concentration

fertilizer will not remain at the current level as a result of

nanoparticle property

(ppm)

1−1000
5−800
1−10

increased global population. Therefore, the price of P fertilizer

250

10

is consistently going up, and market availability and accessibility

for P fertilizer are stepping down. According to a global P
research initiative, RP prices spiked 800% compared to the
size (nm)

20−70

5−25

8−15

previous decade (http://phosphorusfutures.net/). The major

n/aa

n/a

concerns for P fertilizers are low use or uptake efficiency and

rapid conversion of the plant-usable P into less available forms.
Additionally, there are environmental concerns of eutrophica-
tion (increased N and P levels in water).34,35 In the past,
different approaches, such as phosphorus-solubilizing bacteria,
phosphatase- and phytase-producing fungi, organic-acid-pro-
type of nanoparticle

n/a = values not reported.

ducing microorganisms, and vesicular−arbuscular mycorrhiza,

upconverson nanophosphore

have been investigated for enhancing P uptake. However, the

Table 1. continued

success of phosphorus-mobilizing microorganisms has been

limited as a result of low soil organic carbon, which limits the
supply of energy to P-mobilizing microorganisms and high
In2O3

cobalt ferrite

evaporation of water from surface soils. This adversely affects

CeO

SiO2
SiO
Ag

the survivability of nutrient mobilizing microorganisms.36

Si
indium

Nanotechnology and nanoscience researchers are looking for

silver

silica

opportunities that enhance P uptake efficiency, slow release of

a

6490 DOI: 10.1021/acs.jafc.7b02178

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Journal of Agricultural and Food Chemistry Review

Figure 2. Nanotechnology-based slow releasing nitrogen fertilizer. Nanohybrids of urea−hydroxyapatite rod-shaped nanostructure and molecular
level structural depiction and pot and field experiments with the synthesized nanohybrids. The figure is adapted with permission from ref 11.
Copyright 2017 American Chemical Society.

Figure 3. Phosphorus fertilization using nanoscale technology. (A) Growth of 6-week-old soybean plants treated with nanoscale hydroxyapatite and
compared to other P sources and control.38 (B) Phenotypic growth of cluster bean after 4 weeks of germination, treated with ZnO nanoparticles and
compared to its bulk counterpart and control.40 Here, ZnO nanoparticles increase P-mobilizing enzyme activities and enhance native P mobilization
in rhizosphere and P uptake by the plant without any additional P fertilization.41 Panel A is adapted with permission from ref 29. Copyright 2017
Springer. Panel B is adapted with permission from ref 31. Copyright 2008 Springer Nature.

the fertilizer, long-term stability in plant-usable P forms, and with soil components than charged ions of conventional P
mobilization of native P to plants. Tarafdar et al.,37 synthesized fertilizer, thus facilitating P uptake by the plant, relative to
fungal-mediated P nanoparticles using tricalcium phosphate as a conventional P.38 However, further studies will be required to
precursor salt. They confirmed using electron dispersive understand the uptake efficiency with time under various
spectroscopy that 62% (by atom) was P, in 28 nm size. agricultural soil types having variations in pH, ionic state,
Subsequently, Liu and Lal38 synthesized carboxymethyl
organic carbon, and water content. A recent report on P
cellulose (CMC)-stabilized hydroxyapatite nanoparticles of 16
nanofertilizer, a water−phosphorite suspension of 60−120 nm
nm and investigated their effect on soybean. In a greenhouse
experiment, the authors applied these nanoparticles in soil and obtained from natural raw phosphorite by ultrasonic dispersion,
found that treated soybean increased the phenological growth gave promising results upon seed treatment. Nano P enhanced
rate by 33% (Figure 3A) and yield by 18%, relative to plants morphometric indices of corn plants in greenhouse and field
treated with a conventional P fertilizer. Mechanistically, the tests; the fresh yield increases from 2.4% to 2.2-fold, and the
hydroxyapatite nanoparticles have relatively weaker interactions corn yield increases from 14.5 to 24.1%. The improvement in
6491 DOI: 10.1021/acs.jafc.7b02178
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Journal of Agricultural and Food Chemistry Review

crop production quality by a set of indices from 0.3% to 2.6- sprayed with 100 ppm of ZnO nanoparticles.30 The increased
fold was noted.39 Zn content may, thus, help to address Zn deficiency in human/
It is often reported that total soil P is adequate but not in the animal nutrition. The authors concluded that the accumulation
plant-usable form, so that farmers always need more P of Zn in various plant parts depends upon nanoparticle
fertilization. To address the issue, zinc nanoparticles were concentration, particle solubility, ability of the plant to uptake
used to mobilize native P (a plant-unavailable P form) into the nutrient, and size and delivery of the nanoparticles.
plant-available P to enhance its use efficiency. Enzymes, such as Previously, our group reported that nanoparticles exposed to
phosphatase and phytase, require Zn as a cofactor. It was found plants through foliar application (aerosol spray) can be taken
that foliar application of ZnO nanoparticles increased the up efficiently and translocated to the different plant parts.49,50
activities of these enzymes, resulting in about 11% increase in P Moreover, uptake of nutrients (either nano or bulk) by the
uptake by the legumes and cereals, without the addition of any plant largely depends upon the surface biophysical state and its
external P fertilizer (Figure 4).40−42 Increased native P interaction with plant type.29 Furthermore, the elemental
distribution studies by inductively coupled plasma mass
spectrometry (ICP−MS) showed that Zn was distributed in
all plant parts, including seeds. It is unclear what the nature of
this Zn was, although it has been observed previously that ZnO
nanoparticle-exposed plants contain more ions than particles,
suggesting transformation of the ZnO nanoparticles, either
before or after entry into the plant.46,51−53 The distribution of
ions depends upon nanoparticle properties, such as solubility,
stability, and dissolution kinetics, plant age, plant species, and
exposure concentration versus uptake of nanoparticles.
However, the concentration of Zn in the seeds/edible plant
Figure 4. Mechanism of the influence of ZnO nanoparticles on native parts has been found to be within the limit of the dietary
P mobilization in the rhizosphere and uptake by plants. Zinc ion act as recommendation for humans.54
a cofactor for P-mobilizing enzymes, and their activity was found to be ZnO nanoparticles not only increase Zn biofortification but
increased as a result of ZnO nanoparticle treatment. Furthermore, also improve nutritional quality. In tomato, ZnO nanoparticles
enhanced P uptake by mung bean plants evidenced the influence of (100 ppm exposure concentration and 25 nm particle size)
the ZnO nanoparticles on native nutrient mobilization. The figure is increased lycopene content by 113% over the control.48
adapted with permission from ref 41. Copyright 2016 American Lycopene is an antioxidant, an important nutritional parameter
Chemical Society.
in tomato fruits. However, the mechanism behind nanoparticle-
induced lycopene biosynthesis is still unknown. In addition, Zn
mobilization and uptake by plants also improved plant growth, nanoparticles were also used, in a composite with CaO and
biomass, yield, and nutritional quality of cereals and legumes chelators, for the nutritional enrichment of food. For example,
(Figure 3B). Similar results of plant growth and development in Zn−Fe2O4 nanostructured powder, produced by flame spray
response to ZnO nanoparticle exposure along with P pyrolysis that can control chemical composition and surface
supplements were observed on cotton plants by Venkatachalam area, was demonstrated to possess superior sensory qualities in
et al.43 ZnO nanoparticles with P supplementation increased reactive food matrices at equivalent solubility to the commercial
biomass, photosynthetic pigments, and proteins in cotton, counterpart and does not affect the color/texture of the
exhibiting a protective role against oxidative damage by product.55 Thus, nanostructured powders may be used for the
increasing the activities of antioxidant enzymes.43 Magnetite fortification of color-sensitive foods, such as extruded artificial
(Fe3O4) nanoparticles were also found to be capable of cereal grains, chocolate drinks, and fruit yogurts.56
mobilizing native P in soil.23 In summary, attempts to improve Furthermore, ZnO nanoparticles have also been used to
P uptake by generating P-based nanoparticles or to stimulate improve the uptake of native nutrients from the soil. Recently,
native P mobilization by nanoparticle micronutrients (such as Raliya et al.41 used biosynthesized ZnO nanoparticles to
Zn and Fe) not only improve plant growth and development enhance native phosphorus uptake in mung bean. The level of
but also address environmental consequences of P-induced resultant P uptake in mung bean was 10.8% more than control
eutrophication and limited P availability. plants. Mechanistically, it was found that ZnO nanoparticles
2.3. Zinc (Zn). Zn is a micronutrient required for the growth (mean diameter of 25 nm and concentration of 10 ppm)
and development of the plant.44 Zinc deficiency is ubiquitous in enhanced the activities of phosphorus-mobilizing enzymes,
arable soils because availability of Zn for plant uptake is such as acid and alkaline phosphatases, enzymes involved in
restricted in the root zone.45 This causes Zn deficiency in transforming complex forms of phosphorus (i.e., Ca−P, Fe−P,
cereals and legumes growing on potentially Zn-deficient soils. Al−P, and Zn−P) into the plant-available form (Figure 4).40,41
The low human dietary bioavailability of Zn from plant-based Tarafdar et al.42 tested Zn nanofertilizer (average Zn particle
diets causes its deficiency worldwide and may impair growth size between 15 and 25 nm) on a cereal crop, pearl millet
and immune functions. As a result of the ultrasmall size and (Pennisetum americanum L.). In comparison to the control
high surface area/volume size ratio, Zn nanoparticles, applied as plants, they observed significant improvements in the
either foliar spray or root placement, can be transported phenological growth of the plant, chlorophyll content, total
efficiently in the plant system.45−48 Recently, Subbaiah et al.30 soluble leaf protein (38.7%), and plant dry biomass (12.5%) in
sprayed 25 nm ZnO nanoparticles on maize foliage and 6-week-old plants under natural field conditions. Moreover,
observed that the nanoparticles positively influenced plant grain yield at crop maturity was improved by 37.7% as a result
growth, yield, and Zn content in the maize grains. Notably, of foliar application of Zn nanofertilizer.42 The various studies
about 36 ppm of Zn was recorded in the grains of plants using Zn/ZnO or Zn−composite nanomaterials are of
6492 DOI: 10.1021/acs.jafc.7b02178
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Journal of Agricultural and Food Chemistry Review

Figure 5. Carbon-based nanomaterials and their influence on the plant growth in vitro and in vivo. (A) Different types of carbon nanostructures. (B)
Phenotype of tomato seeds after 5 days of carbon nanoparticle exposure. (C) Carbon nanoparticles induce tobacco callus culture growth. (D) Effect
of the CNT on the phenotype of tomato plants, where wild type is a control, whereas CNT watering means that the CNT was exposed with watering
to the plants. Abbreviation: control, control media; AC, activated carbon; helical, helical MWCNTs; long, long MWCNTs; short, short MWCNTs;
and CNT, carbon nanotube. Panels A−C are adapted with permission from ref 162. Copyright 2016 IOP Publishing, Ltd. Panel D is adapted with
permission from ref 161. Copyright 2013 Wiley-VCH Verlag GmbH & Co.

significant agricultural importance (provided that the nanoma- plant age, nanoparticle exposure concentration, and physico-
terials are of optimized properties, discussed in a subsequent chemical properties, and, thus, require continuous validation
section) for improving plant growth, development, and with a diverse range of crops and in various arable soils as well
productivity but also for addressing the challenges of Zn as subsequent effects on the food chain.
malnutrition by agronomic fortification.29,57 2.5. Silica (Si/SiO/SiO2/Silicon). Upon a literature survey
2.4. Iron Oxide. Iron (Fe) is an essential dietary nutrient based on Google Scholar, PubMed, and Web of Science, the
and is important for crop growth and development. Iron is oldest report of nanoparticle influence on plant growth and
involved in chlorophyll biosynthesis and required for certain development was found to be from 2004.71 These researchers
enzyme functions, notably, heme proteins (e.g., cytochromes shook roots of 200-year-old Changbai larch (Larix olgensis)
found in chloroplast and mitochondria), and involved in the seedlings in nanostructured silicon dioxide (TMS). They
electron transfer system.58 Therefore, the primary symptom of observed that 0.5 ppm of TMS promoted seedling growth.
Fe deficiency is chlorosis in young plant leaves that affects Reports of abiotic stress tolerance in plants as a result of silicon
normal physiological function and nutritional quality.59 The (or silica nanoparticles) have been reported by other groups.
most abundant form of Fe in soils is ferric oxide (Fe2O3) or For example, nano silica conferred tolerance in tomato plants
hematite, which is extremely insoluble; thus, Fe uptake by the grown under salinity stress72 as well as tolerance against
plant is often low. Conventionally, Fe uptake is dependent drought in wheat.73 Furthermore, it also enhanced the
upon the ability of the plant to reduce Fe3+ (ferric) to the Fe2+ photosynthetic rate, biomass production, and grain yield and
(ferrous) form and remove it from the complex or chelating maintained leaf water content. Mechanistically, silica nano-
compound (often phytosiderophores). Considering the food particles form a binary film in the cell wall that provides
chain, Fe deficiency not only affects plant growth and osmotic adjustments. Silica nanoparticles also stimulate
development but also leads to Fe deficiency in animals and antioxidant enzymes, leading to resistance against biotic and
humans.56,60 Therefore, it is important to increase the use abiotic stresses and resulting in better seedling growth.71,74,75 In
efficiency of Fe fertilizers. Iron oxide nanoparticles have been addition, Si nanoparticles reduce sodium uptake and trans-
widely used for various applications, including catalysis and location while increasing potassium uptake and translocation
medicine.61 Previous studies showed that Fe oxide nano- under salt stress.76,77 Salinity and drought are major challenges
particles delivered to plants through soil or foliar spray can be in agriculture that limit crop production. Therefore, the
taken up and transported in corn,62 pumpkin,63 and water- beneficial impacts of silica and silicon nanoparticles on plant
melon.49,64 Fundamental studies on the use of Fe oxide growth and development can potentially address adverse effects
nanoparticles on various crops, including lettuce,23 wheat,65 of climate changes, such as uneven rainfall and rising
clover,66 soybeans,67,68 rice,69 and peanut,70 show that Fe temperatures, that lead to enhanced evaporation of water
nanoparticles improve several agronomic traits, including grain from the soil surface.
yield, nutritional quality, Fe biofortification, biomass, and 2.6. Titanium (TiO2, Rutile/Anatase). Since its commer-
biochemical parameters, such as chlorophyll content, photo- cial production, TiO2 has been used as a pigment in paints and
synthesis, light absorption, and nitrogen and phosphorus in sunscreens as a result of its photocatalytic water-splitting
metabolism. The findings based on magnetization studies under ultraviolet (UV) light.78 The photocatalytic activity of
suggest that iron oxide nanoparticles can be taken up by plants nanoscale TiO2 converts light energy into electrical or chemical
as intact particles and that they eventually undergo dissolution energy under sunlight. Therefore, scientists see the potential to
in the plant to affect plant development. Thus, Fe nanoparticles enhance photosynthesis while using engineered TiO2 nano-
may be an ideal substrate to complement or replace traditional particles; it is one of the most studied nanoparticles for
chelator-based iron fertilizers. However, results are limited by investigating plant responses to seed germination, plant growth,
various factors, such as type of soil, soil chemistry, plant species, plant pest management, pesticide degradation, advanced water
6493 DOI: 10.1021/acs.jafc.7b02178
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Figure 6. Synthesis of nanoparticles. Principally, two methods, bottom-up approach (molecules form clusters and eventually stable cluster or
particles) and top-down approach (breakdown of big particles into small particles), are used to engineer nanoscale particles with controlled
physicochemical properties.

Table 2. Comparative Summary of Nanoparticle Synthesis Approaches187

nanoparticle synthesis method
gas phase liquid phase solid phase
feature aerosol biological chemical physical
advantages single step, good control over environmentally benign precise control on morphology of the rapid and scale-up
particle size and shape metal nanoparticles synthesis
synthesis of controlled surface coating with natural macro- and
nanocomposite micro-biomolecules
monodispersity within a few percent biocompatible
and scalable
passivation of the surface
limitations large aggregates could be formed rate of particle synthesis is low surface coating with harmful chemicals broad polydispersity and
need natural resources comparatively lesser biocompatibility poly-shape
broad polydispersity and poly-shape

purification, and sensor technology to detect pesticide carbon are intrinsically linked, regardless of the carbon source:
residues.79 TiO2 nanoparticles have been tested on various carbon dioxide from the air or organic carbon in soil.
crops, such as lettuce,23 spinach,80−82 Lemna minor,83 tomato,28 Engineered carbon nanomaterials [one dimensional (1D),
wheat,84 watermelon,49 beans,85 and millets.86,87 These studies two dimensional (2D), or three dimensional (3D)], such as
conclude that TiO2 nanoparticles increase (a) plant biomass/ graphene, fullerenes, and carbon nanotubes, have attracted
yield, (b) chlorophyll content, (c) photosynthetic activity, (d) considerable attention as a result of their exceptional
nutrient contents, and (e) germination rate. However, the plant physicochemical properties and stability. It has also been
responses depended upon plant type, exposure concentration, reported that carbon nanotubes can be taken up by plants to
and nanoscale properties. The main reason for enhanced influence growth and development.95−98 A range of studies
physiological activities is thought to be due to an increase in have been reported on the positive influence of carbon
nanomaterials/structures on plants (Figure 5). These studies
nitrogen metabolism and ribulose-1,5-bisphosphate carboxy-
conclude that carbon nanomaterials increase root length,
lase/oxygenase (RuBISCO), a key photosynthetic enzyme
stimulate seed germination, and plant biomass.99−103 Most of
activity that leads to more CO2 assimilation.82,88−91 The studies the available literature report best outcomes with carbon
demonstrate that exposure of plants to TiO2 nanoparticles nanotubes [single-walled carbon nanotube (SWCNT) > multi-
enhances growth by increasing photosynthesis/light absorp- walled carbon nanotube (MWCNT) > carbon nanotube
tion.48,79,83,85,88,92 However, it remains to be seen whether TiO2 (CNT)], followed by fullerenes and graphene. For further
nanofertilizers can be produced by the fertilizer industry and details on carbon-based nanomaterials, readers are directed to
acceptable to farmers, considering that it is not an essential recently published reviews on carbon nanomaterial application
element for plants. in agriculture by Vithanage et al.,104 Mukherjee et al.,105 and
2.7. Carbon-Based Nanomaterials. Carbon is a major Zaytseva and Neumann.106 These reviews discussed the
constituent of all living things; carbon bonds with other atoms contrasting effects of carbon nanostructures on agriculturally
and provides the structure to biomolecules, i.e., protein, important plants.
carbohydrates, and fat. Plants also use carbon in the form of
carbon dioxide during photosynthesis to convert photoenergy 3. SYSTEMATIC STUDY: SYNTHESIS, DELIVERY,
into carbohydrates.93 Plants use carbon for their own growth INTERACTION, AND FATE
and development and also for providing nourishment to other The influence of nanomaterials on plants depends greatly upon
living organisms. Farmers use manure or decomposing plant the intrinsic properties and extrinsic interactions of the
biomass in farm field/garden to fertilize plants as a result of its nanoparticles. This is, presumably, one reason among many
rich carbon source.93,94 Thus, it is clear that plant growth and that the literature has shown contrasting results from the same
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Figure 7. Aerosol-mediated nanoparticle delivery to a watermelon plant. (a) Schematic diagram of the experimental setup. (b) Watermelon plants
used in this work. (inset b) Typical watermelon leaf. (c) TEM micrograph showing the presence of nanoparticles inside the leaf after applying
nanoparticles for 3 days. (d) Schematic diagram of nanoparticle transport inside watermelon plants. The figure is adapted and modified with
permission from ref 49. Copyright 2013 Springer.

class of particles. For examples, TiO2 nanoparticle exposure to 3.2. Nanoparticle Delivery, Uptake, Translocation,
corn seeds delayed germination,107 whereas they show a non- and Biodistribution. In general, agrochemicals are delivered
significant effect on rice seed germination108 and improved seed to plants in three ways: seed treatment, soil amendment, or
germination of wheat.84 In the following sections, we discuss foliar spray. Engineered nanoparticles have several consequen-
some of the factors needed to be examined while comparing a ces when applied via the soil, particularly when particles are
nanoparticle type and its influence on plants. mixed in the soil: the exposure and localized concentration of
3.1. Synthesis of Nanoparticles/Nanofertilizer. Direct the particles become much higher than the indirect exposure
fabrication or synthesis of nanoscale materials is becoming during foliar spray or subsequent translocation to the roots that
increasingly important in life sciences, medical, agricultural, contribute significantly lower amounts to plant sinks. Moreover,
environmental, and related emerging applications. While some high exposure concentrations may influence soil or rhizosphere
nanomaterials are available commercially, there is need for microbial communities120−123 and induce agglomeration or
stringent control on resultant particle characteristics and aggregation as a result of soil physicochemical properties that
customization of samples, especially when new application may limit the particle uptake by plants.124−126 Comparative
investigations of nanoparticle delivery to plants by spraying on
areas are to be developed. Nanomaterials are regularly being
the leaves versus soil amendment indicate that foliar application
synthesized by both “wet” methods, such as sol−gel, hydro-
has significant advantages for nanoscale nutrient uptake.48−50,68
thermal, homogeneous precipitation, biosynthesis using
Furthermore, lab-scale experiments demonstrated that an
enzyme and protein template, and reversed micelle meth- effective aerosol spray helps to generate monodisperse particles
ods,28,109−113 and “dry” synthesis approaches, such as aerosol- and avoid soft agglomeration during foliar application.
based processes,114−119 ranging from single-element nano- Foliar application of nutrients and pesticides has been
particles, oxide semiconductors, other metal oxides, metals, practiced for years.127 As a matter of principle, soil application
metal alloys, polymers, and doped and composite nanoparticles. or seed treatment of the fertilizer is performed on the basis of
A basic scheme of nanomaterial synthesis from the bottom-up nutrient deficiency in the soil, whereas foliar (aerosol)
or top-down approach is illustrated in Figure 6. Nanoparticles application is performed on the basis of nutrient deficiency
to be used as fertilizers require a synthesis approach capable of symptoms exhibited by plants.128 The major consequence for
producing mass scale particles with controlled physicochemical foliar applications are that they require higher leaf area index,
properties at low cost. To this end, a comparative summary of low exposure dose, potentially multiple application times, and
different methods for nanoparticle synthesis is summarized in timing of the application based on weather to avoid loss of
Table 2. nutrients.129 An aerosol of engineered nanoparticles inhaled by
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Figure 8. Mechanistic understanding of nanoparticle transport within plant cells. The representation describes how nanoparticles transport through
apoplast and symplast pathways in plant cells, along with the pressure gradient or mass flow of the photosynthate product. The inset represent the
favorable transport of the nanostructure (rod shape) more through the apoplast pathway than the symplastic pathway. NPs = nanoparticles. The
color gradient in the phloem represents the mass concentration of photosynthate with nanoparticles. The figure is adapted with permission from ref
50. Copyright 2016 Frontiers Media.

humans or other animals may cause toxicity. However, this supported their ICP−MS data with microscopic or X-ray
outcome is dependent upon the particle concentration in the spectroscopic studies of plant parts to demonstrate the
atmosphere, weather conditions of the day/time, exposure presence of actual particles. However, a major limitation of
concentration, and physicochemical properties of the par- the electron microscopy of plant tissue is non-representative
ticles.25,27,130−133 To ensure safe foliar application of nano- results as a result of imaging of a very tiny fraction of the whole
fertilizers, it is recommended to use appropriate personal plant.48,50,139 Aerosol-mediated foliar application increases
protection equipment, such as mask, gloves, and eye uptake of nanoparticles by circumventing the cuticle, the
protection.134−136 primary barrier of the plant cell.49,50 The subsequent transport
In the aerosol, particles maintain an effective particle size, are of nanoparticles from shoot to root is then achieved by the
monodisperse, and are relatively more stable than particles in vascular system−phloem transport pathways, a bidirectional
conventional suspension spray or soil application that undergo pathway along the photosynthate gradient. Cellular transport of
agglomeration as a result of particle−particle or particle−soil nanoparticles is carried out by both the apoplast and symplast
interaction.49,50 Nanofertilizer properties are particularly pathways. The apoplast pathway favors transport of larger
important for foliar delivery, whereby size exclusion may limit particles (∼200 nm), while the symplastic pathway favors
uptake via the stomatal pathway.137 It has been demonstrated smaller (<50 nm) particles (Figure 8).140
that stomatal uptake is enhanced through control of the 3.2.1. Target Delivery and Controlled Release of Nano-
nanofertilizer particle size combined with an aerosol delivery scale Material to Plant. Since the advent of the use of
method, as illustrated in the past.50 Furthermore, it was shown nanomaterials in different applications, they have been
that foliar delivery of iron and magnesium nanofertilizers to pea extensively used in nanomedicine, where the nanoparticles are
(Vigna unguiculata) caused significant positive effects on plant used as either therapeutic agents or target drug delivery
growth and development.138 Similarly, aerosol-mediated nano- vehicles.141 Similarly, nanomaterials can be tailored for precise
particle delivery, penetration, and translocation in water- delivery to plants.10,13,49,50,63 However, the desired progress for
melon49,50 and tomato28 have also been demonstrated (Figure target or localized delivery of the nanoscale nutrient or
7). The results revealed that nanoparticles of diameter less than nanofertilizer has yet to be made. Torney et al.142 used
100 nm generated by an aerosol process enter the leaf through mesoporous silica nanoparticles of 3 nm pore size for the
the stomatal pathway, passing through the phloem and reaching delivery of a gene and its chemical inducer into isolated tobacco
the root of watermelon plants. It is worth noting that, in many plant cells and intact leaves. Subsequently, gold nanoparticle
cases, plant parts are analyzed for studying nanoparticle capping was used to avoid the leaching out of the loaded gene
transport using the ICP−MS technique, which analyzes ions and its inducer at the non-specific site. Similarly, aptamers,
and not the particles. However, many other studies have also oligonucleotide or peptide molecules that bind to specific target
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Figure 9. Illustration of various unit processes and their interconnectivity to realize the concept of sustainable agriculture by addressing the FEW
nexus. In this illustration, four basic concepts are proposed: (a) water and energy recovery from wastewater, (b) nano-enabled agricultural processes,
(c) sustainable water reuse and aquifer recharge, and (d) nanotechnology-based sensing and system integration and modeling.

molecules, can be potentially used for the surface functionaliza- coupled to a microbial electrochemical cell (for “green”
tion of nanofertilizer, where the nutrient in the nanostructure is production of disinfectants, such as peroxides), (b) utilization
released in response to plant signals in the rhizosphere.143,144 of nitrogen- and phosphorus-rich discharges for the production
The future possibilities for target delivery of essential nutrients, of nanofertilizers through novel aerosol methodologies, (c)
pesticides, and genetic materials using nanomaterial will offer water discharge (from the step described in a) reuse and as-
new possibilities in the agricultural revolution.144,145 produced nanofertilizers (from step b) for use in hydroponic
3.2.2. Nanoscale Enabled Food−Energy−Water (FEW) and conventional soil-based agricultural systems, (d) managed
Nexus: A Futuristic Perspective. Regional to global demands discharge from the agricultural system to a natural soil aquifer
for FEW will place a range of significant resource limitations treatment system and reuse of the treated water, and (e) novel
and pressures that will require the development of new sensor-based network to monitor and integrate processes for
alternative methods and technologies. Strategic developments real-time and simulation-based system optimization and
and investments to address these realities must be underpinned control.
by a fundamental understanding of the interconnectivity of the 3.3. Transport Models for Nutrient Uptake in Plants.
FEW nexus if successful management, including technology There are several studies that have used models to address the
development, is to be achieved at any scale. In the context of uptake of nutrients and their transport in different regions of
FEW systems, there are tremendous opportunities to create the plant. The uptake process includes the movement of
novel approaches, including new technologies, for optimizing nutrient ions through the soil toward the root surface, transport
linkages between these systems. These include using treated of ions through the membranes of root surface cells, radial
wastewater for agricultural purposes, enhancing crop yields, and transport of ions toward the root xylem vessels, and transport
recharging aquifers while being less energy-intensive (or even in the xylem and distribution of ions in the above ground parts
net-neutral). Sustainable energy and resource harvesting from of the plant.146 Many recent studies have combined the model
wastewater management processes necessitates a shift from the of nutrient uptake for a single root (mesh of root hairs) with
current centralized wastewater management to a scientifically the rate of root growth to predict total nutrient uptake over a
robust controlled decentralized framework. We propose an period of time. The water and solute movement through soil is
integrated system approach, illustrated in Figure 9. with the described by the Richards equation and the convection−
following perspectives to address the FEW nexus for sustainable dispersion equation in most of the recent models. Different
agriculture: (a) anaerobic digester (for energy harvesting) empirical relations have been used in the models to address the
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nutrient uptake at the surface of the root. In many models, risks that they may pose as well as finding sustainable ways to
nutrient uptake has been described by the Michaelis−Menten manufacture nanoscale materials to be used in agriculture.
equation.147,148 Uptake increases with an increasing nutrient Some of the major concerns regarding nanoscale technology
concentration in a curvilinear fashion, approaching maximum and its use in agrochemicals that need to be addressed are
uptake. Kinetic parameters of the Michaelis−Menten equation summarized as follows: (1) scaling up the synthesis/
vary with plant species, plant age, soil temperature, and other manufacturing/designing of safe nanomaterials that are
parameters. Therefore, for modeling, these parameters need to environmentally benign and sustainable for agricultural
be determined separately by controlled experiments, often production and also designing novel nanoparticles for
posing a challenge and is a scientific gap that needs to be controlled release and enhanced nutrient uptake rate, (2)
addressed. characterizing nanostructures, formulations, or emulsions for a
The initial nutrient transport models in plant tissues were of detailed understanding of nanoscale properties with respect to
steady-state source−sink type, with flow driven by an size, shape, chemical composition, crystal phase, porosity,
osmotically generated pressure gradient.149,150 Diffusional hydrophilicity/hydrophobicity, surface charge, stability, dis-
transport of nutrients has generally been neglected in most of solution, agglomeration/aggregation, and valence of the surface
these models because they have been considered to be layer, (3) establishing precise delivery of nanomaterials and
insignificant, relative to convective transport in the main bulk uptake rates and investigating the metabolic fates of nanoma-
flow. However, diffusion is significant near the vessel terials, (4) developing nanoscale particles that can act as both
boundaries because the convective flux is nearly zero. The fertilizers and pesticides, which provide sustained release and
more recent models include a diffusive transport term in the stability for plant protection management, (5) understanding
transport equation.151 Most models in the literature address nano-biointeractions, transport, and fate of nanoscale materials
only one or two aspects of the fertilizer-to-crop transport in the plant and food chain, including the solubility and
pathway. Also, many parameters used in the models, such as durability of nanomaterials in the plant, soil, and environment,
Michaelis−Menten kinetic parameters, need to be determined (6) optimizing nanomaterial dose−response concentrations for
separately by experiments for different plant types, which poses a wide range of crops (for this, long-term studies, including life
major challenges. Although numerous models have been cycle, transgenerational, and trophic transfer investigations, are
developed to predict the uptake of nutrients, there is a glaring required), (7) optimizing nanoparticle parameters/character-
gap in the present literature, hence opportunities for extending istics, in particular, relationships among exposure concen-
these models to address nanoparticle uptake and transport in tration, dose metrics (number concentration versus surface area
plants. concentration), and their impacts (here, it is important to
address the question related to interlinked characteristics; for
4. FUTURE PREPECTIVES example, a given mass of smaller nanoparticles is more toxic
than a larger size of the same species, but no significant
Owing to the unique physicochemical properties of nanostruc- difference is observed if normalized by the surface area), (8)
tures, their use as agrochemicals (fertilizers or pesticides) for understanding human and environmental exposure to engi-
plant growth and protection is consistently being explored. neered nanoscale particles via dietary uptake or food chain
Most recently, funded projects and future research calls appear contamination, (9) understanding potential environmental risks
to be focusing more on designing safer nanomaterial for and development of mitigation strategies and studying the basis
effective responses while being environmentally friendly. of contradictory results and their reproducibility versus
Nanotechnology research in agriculture is still at a rudimentary reliability regarding the effect of engineered nanoparticles in
stage but evolving swiftly. However, before nanofertilizers can plants using a quantitative structure−activity relationship, (10)
be used on farm for a general farm practice, there is a need for developing common strategies/goals among the leading
better understanding their modes of function according to the institutes/countries to test laboratory-scale nanoproducts in
regulatory frameworks, which can be developed to ensure safe real farm applications for broader technology validation and
use of such agrochemicals. translation, and (11) establishing educational and outreach
The United States Food and Drug Administration (U.S. programs along with research projects to bridge the
FDA) has already issued guidelines for the use of nanomaterials community/users and scientists to address potential customer
in animal feed.152 Manufacturers are also adding engineered (farmers) concerns.
nanoparticles to foods, personal care, and other consumer In summary, the world’s population is expected to exceed 9
products. Examples include silica nanoparticles in baby formula, billion by 2050,3 and this will result in a great need to produce
titanium dioxide nanoparticles in powdered cake donuts, and more food. Scientists are working to develop new ways to meet
other nanomaterials in paints, plastics, paper fibers, pharma- this rising global demand for food, energy, and water and to do
ceuticals, and toothpaste.153−156 Many nanoparticle properties so without increasing the strain on natural resources.
are considered to be of potential risk to human health, viz., size, Nanotechnology represents a promising solution to these
shape, crystal phase, solubility, type of material, and exposure challenges. The development and use of nanofertilizers can be a
and dosage concentrations.24,133,157 Expert opinions indicate potential strategy for promoting plant growth, development,
that food products containing nanoparticles available in the and productivity. Nanotechnology-based fertilizers hold prom-
market are probably safe to eat, but this is an area that needs to ise as smart delivery systems for plant nutrients; fundamental
be more actively investigated.12,158−160 Addressing these issues properties, such as size, surface area, crystal phase, and surface
will require further studies to understand how nanoparticles capping of nanomaterials, not only control nutrient dissolution
behave within the human body once exposed through and reactivity but also control material behavior during
nanofood. Researchers need to conduct life cycle assessments application. While recent reports indicate that nutrient use
of the nanoparticle impact on human health and the efficiency can be enhanced through nanoscale packaging
environment and develop strategies to assess and manage any compared to conventional fertilizers, the development and
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Journal of Agricultural and Food Chemistry Review

use of rationally designed nanoscale macro- and micronutrient (12) Dimkpa, C. O.; Bindraban, P. S. Nanofertilizers: New products
fertilizer technologies remain nascent. Currently, there is for the industry? J. Agric. Food Chem. 2017, DOI: 10.1021/
pressing need for improving nanosynthesis and delivery acs.jafc.7b02150.
capabilities for next-generation fertilizers and their use in (13) Nair, R.; Varghese, S. H.; Nair, B. G.; Maekawa, T.; Yoshida, Y.;
agricultural systems. Kumar, D. S. Nanoparticulate material delivery to plants. Plant Sci.

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2010, 179, 154−163.
(14) Saharan, V.; Khatik, R.; Kumari, M.; Raliya, R.; Nallamuthu, I.;
AUTHOR INFORMATION Pal, A. Proceedings of the 4th Annual International Conference on
Corresponding Authors Advances in Biotechnology (BioTech 2014); Dubai, United Arab
Emirates, March 10−11, 2014; p 23.
*Telephone: +1-314-935-4530. Fax: 314-935-5464. E-mail: (15) Tilman, D.; Cassman, K. G.; Matson, P. A.; Naylor, R.; Polasky,
rameshraliya@wustl.edu. S. Agricultural sustainability and intensive production practices. Nature
*Telephone: +1-314-935-5482. Fax: 314-935-5464. E-mail: 2002, 418, 671−677.
pbiswas@wustl.edu. (16) Carpenter, S. R.; Caraco, N. F.; Correll, D. L.; Howarth, R. W.;
ORCID Sharpley, A. N.; Smith, V. H. Nonpoint pollution of surface waters
with phosphorus and nitrogen. Ecol. Appl. 1998, 8, 559−568.
Ramesh Raliya: 0000-0002-9534-4943 (17) Massachusetts Institute of Technology (MIT). Fighting Peak
Christian Dimkpa: 0000-0003-2143-5452 Phosphorus; http://web.mit.edu/12.000/www/m2016/finalwebsite/
Pratim Biswas: 0000-0003-1104-3738 solutions/phosphorus.html (accessed March 1, 2017).
Funding (18) Dawson, C. J.; Hilton, J. Fertiliser availability in a resource-
limited world: Production and recycling of nitrogen and phosphorus.
Partial support for this work was provided by the McDonnell Food Policy 2011, 36, S14−S22.
Academy Global Energy and Environmental Partnership (19) United States Geological Survey (USGS). http://www.usgs.
(MAGEEP) at Washington University in St. Louis. Ramesh gov/climate_landuse/ (accessed March 1, 2017).
Raliya is thankful for the LEAP Inventor Challenge Award (20) Greene, R. P.; Harlin, J. M. Threat to high market value
given by Skandalaris Center for Interdisciplinary Innovation agricultural lands from urban encroachment: A national and regional
and Entrepreneurship at Washington University in St. Louis. perspecitve. Social Sci. J. 1995, 32, 137−155.
Christian Dimkpa is thankful for the partial support from the (21) Pimentel, D.; Wilson, A. World population agriculture and
United States Agency for International Development (USAID). malnutrition. World Watch 2004, 22−25.
(22) Saharan, V.; Kumaraswamy, R.; Choudhary, R. C.; Kumari, S.;
Notes Pal, A.; Raliya, R.; Biswas, P. Cu-chitosan nanoparticle mediated
The authors declare no competing financial interest. sustainable approach to enhance seedling growth in maize by

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6503 DOI: 10.1021/acs.jafc.7b02178

J. Agric. Food Chem. 2018, 66, 6487−6503