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Annual Review of Food Science and Technology

Uptake of EngineeredNanoparticles by Food Crops:Characterization, Mechanisms,and ImplicationsChuanxin Ma,1,2 Jason C. White,1 Jian Zhao,3

Qing Zhao,4 and Baoshan Xing2

1Department of Analytical Chemistry, Connecticut Agricultural Experiment Station,New Haven, Connecticut 06504, USA2Stockbridge School of Agriculture, University of Massachusetts, Amherst,Massachusetts 01003, USA; email: bx@umass.edu3Institute of Coastal Environmental Pollution Control, Ocean University of China,Qingdao 266100, China4Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China

Annu. Rev. Food Sci. Technol. 2018. 9:129–53

First published as a Review in Advance onJanuary 12, 2018

The Annual Review of Food Science and Technology isonline at food.annualreviews.org

https://doi.org/10.1146/annurev-food-030117-012657

Copyright c© 2018 by Annual Reviews.All rights reserved

Keywords

biotransformation, disease suppression, engineered nanoparticles, foodsafety, molecular responses, nutrient alteration

Abstract

With the rapidly increasing demand for and use of engineered nanoparticles(NPs) in agriculture and related sectors, concerns over the risks to agricul-tural systems and to crop safety have been the focus of a number of investi-gations. Significant evidence exists for NP accumulation in soils, includingpotential particle transformation in the rhizosphere and within terrestrialplants, resulting in subsequent uptake by plants that can yield physiologicaldeficits and molecular alterations that directly undermine crop quality andfood safety. In this review, we document in vitro and in vivo characterizationof NPs in both growth media and biological matrices; discuss NP uptakepatterns, biotransformation, and the underlying mechanisms of nanotoxic-ity; and summarize the environmental implications of the presence of NPs inagricultural ecosystems. A clear understanding of nano-impacts, includingthe advantages and disadvantages, on crop plants will help to optimize thesafe and sustainable application of nanotechnology in agriculture for the pur-poses of enhanced yield production, disease suppression, and food quality.

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ANNUAL REVIEWS Further

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INTRODUCTION

Engineered nanoparticles (NPs) have unique physiochemical properties, including nanoscale size(≤100 nm), a high ratio of surface area to volume, and enhanced activity (Nel et al. 2006). NPsare widely used in agriculture for the purposes of soil monitoring, nutrient supply, and diseasesuppression (Asli & Neumann 2009). The soil system is considered to be the primary sink forterrestrial NP accumulation, and evidence for particle accumulation and biotransformation insoils and sediments has been reported (Tou et al. 2017). In the past decade, a number of studiesevaluating NP-induced phytotoxicity have been conducted in both liquid and solid substrates underlaboratory and greenhouse conditions (Rizwan et al. 2017). Importantly, the majority of publishedstudies on NP phytotoxicity have been conducted at relatively high concentrations, which isnecessary when determining inherent hazards across different materials (Holden et al. 2016). Acommon finding is that nanotoxicity to terrestrial plants is highly dependent on dose, species,and exposure scenario (substrate, temperature, and environment) (Ma et al. 2015b). Althoughprevious studies have demonstrated that NP transformation can significantly alter the parentNP and that these altered NP derivatives are available for uptake by and are toxic to plants,mechanistic understanding regarding biomodification of NPs in vivo and in vitro remains elusive.Notably, several recent studies have reported that certain NPs, when used at appropriate doses,can act as effective nutrient sources to support crop growth (Anderson et al. 2017). However,at excessive concentrations, nanotoxicity to plants in terms of biomass reduction, photosyntheticsystem damage, and defense mechanism disruption occurs (Rizwan et al. 2017). Clearly, thoroughinvestigations of NP characterization and accumulation by terrestrial plants are critical to thesustainable application of nanotechnology in agriculture and food production (Anderson et al.2017, Jain et al. 2016).

In this review, we focus on NP applications in agriculture and report on NP fate and behaviorin a plant-soil system from three main perspectives: (a) characterization of bare (uncoated) andfunctionalized NPs and assessment of the potential of coated NP applications in agriculture;(b) summary of NP uptake patterns, plant responses, and potential uptake mechanisms; and (c) theenvironmental implications of NPs in agricultural systems and a discussion of future perspectivesof nanotechnology applications in agriculture.

NANOPARTICLE CHARACTERIZATION

NP characterization has become an integral part of studies focused on the interactions betweenNPs and terrestrial plants (Figure 1). In vivo or in vitro observation of different types of NPs,including bare and functionalized particles, has been widely reported. In this section, novel tech-niques for NP characterization, biological factors that influence NP properties, and the importanceof functionalized NPs in agricultural applications are discussed.

Dynamic light scattering is one of the most widely used analytical methods for determining theimpact of environmental factors (such as pH, ionic strength, organic matter, and environmentalparticles) on the particle size distribution, aggregation state, and band gap energy of NPs (Wanget al. 2016b). However, the NPs should be dispersed within a clear, low-viscosity liquid (such aswater) to avoid interference from other particles or polymers in the system. Transmission electronmicroscopy (TEM) with energy dispersive spectroscopy (EDS) can visually image NPs in planttissues and cells (Le Van et al. 2016). However, this qualitative technique cannot determine theNP concentration in the matrix of interest. Inductively coupled plasma (ICP)-based detection hasbeen widely used for NP quantification in biological matrices. Traditional ICP–mass spectrometry(MS)/optical emission spectrometry can determine the total amount of metals in NP-treated planttissues, which are typically digested by concentrated acid and hydrogen peroxide (H2O2). However,

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Heteroaggregation Homoaggregation

Soil phase

Biologicalphase

Soil factorspH, CEC, organic matter, soil texture

NP dissolutionMn+

NOM-coated NPs

Sulfidation

Metal complex

NP transformation(physical, chemical, and biological)

NP stabilityNP bioavailability

NP toxicity

NP uptake

NPNP Coated NP

Mn+

Mn+

Metal complex

Effects of biometabolites on NP biotransformation

Toxicity assessment

NP characterizationIn situ observation: TEM, SEM, AFM,synchrotron-based XRF

Qualification: SERS, FTIR

ICP-based quantification: ICP-MS/OES,FFF-ICP-MS, SP-ICP-MS, MC-ICP-MS

Speciation: synchrotron-basedtechniques

Corona

Figure 1Schematic overview of nanoparticle (NP) characterization in soil and biological matrices. In the soil phase,soil physiochemical properties have significant impacts on NP aggregation and transformation, which candirectly determine bioavailability and toxicity to terrestrial plants. In the biological phase, NPbiotransformation can alter NP toxicity and affect plant defense mechanisms. Thus, NP characterizationrequires novel and robust techniques. Abbreviations: AFM, atomic force microscopy; CEC, cation exchangecapacity; FFF, field-flow fractionation; FTIR, Fourier transform infrared spectroscopy; ICP-MS, inductivelycoupled plasma mass spectrometry; MC, multiple collector; NOM, natural organic matter; OES, opticalemission spectrometry; SEM, scanning electron microscopy; SERS, surface-enhanced Raman spectroscopy;SP, single particle; TEM, transmission electron microscopy; XRF, X-ray fluorescence.

this method cannot differentiate NPs from other metal forms (such as soluble or bulk metals).Advanced techniques such as field-flow fractionation ICP-MS and single-particle ICP-MS haverecently been developed. These methods can be used to separate and characterize the NPs inenvironmental systems and biological samples from the microgram to the kilogram level (Majedi& Lee 2016, Wang et al. 2016b). The intrinsic labeling of engineered NPs with stable isotopesis another useful tool that can be exploited by multiple collector–ICP-MS to characterize anddetect NPs in the environment and biota (Majedi & Lee 2016, Molina et al. 2014, Yin et al. 2017).Additional techniques such as atomic force microscopy (Liu et al. 2009), Fourier transform infraredspectroscopy (Wang et al. 2012a), and surface-enhanced Raman spectroscopy (Guo et al. 2015)have also been applied to NP characterization and detection in biological matrices. However, eachtechnique has some drawbacks in terms of cost, purification, time, labor, limit of detection, andother factors; therefore, multiple overlapping techniques are typically required to fully characterizeNPs in biological matrices.

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The importance of transformation in NP toxicity, bioavailability, and stability in the environ-ment and biota has also been addressed (Lowry et al. 2012). Synchrotron-based X-ray fluorescencemicroscopy can examine the composition or speciation of targeted elements and assess possiblemetal speciation from NP transformation in situ (Hernandez-Viezcas et al. 2013). This tech-nique provides a unique interpretation of nanotoxicity and possible plant defense mechanisms inresponse to particle exposure. However, in addition to characterizing the NPs themselves, it isnecessary to examine the surface coatings of NPs as affected by interactions with biological mater-ials such as root exudates and extracellular polymeric substances (EPSs) in the rhizosphere, bothof which could significantly alter the stability and bioavailability of NPs to plants (see the sectiontitled Role of Biological Metabolites for Nanoparticle Biotransformation) (Anderson et al. 2017).For example, Lundqvist et al. (2008) reported that NP surface properties and size could largelydetermine the protein corona. In reality, it is more accurate to describe this as the biomolecularcorona, as other biological molecules, such as phospholipids, biosurfactants, and polysaccharides,may be present at the particle surfaces. A separate study found the important roles of the pro-tein corona in affecting silica (SiO2) NP uptake by human cells (Lesniak et al. 2012). Thus, anunderstanding of the kinetic relationship between the biomolecular corona and NP surface prop-erties could help us to resolve many of the questions on molecular mechanisms of NP-inducedtoxicity in biota and provide a new understanding and vision for NP functionalization in agricul-tural and biomedical applications (Anderson et al. 2017, Jiang et al. 2013). Importantly, due tothe complexity of substrates and organisms in plant-soil systems, NP physicochemical propertiesshould be characterized before, during, and after exposure in both soil and plants to achieve amore thorough understanding of NP fate. However, conducting these analyses is difficult, laborintensive, and confounded by a lack of robust analytical techniques. Future work should also placea greater emphasis on metabolomics to generate meta-information regarding the levels of organiccompounds secreted in the rhizosphere in response to NP exposure.

MECHANISMS

Nanoparticle Exposure Patterns

Studies investigating NP exposure to terrestrial plants fall into two categories based on the exposureroute. First, NPs may be introduced to the plant system via root exposure, which simulates soilcontamination in the environment. Second, due to their potential benefits in agriculture, NPs havealso been applied to crops via foliar spray for the purposes of plant growth enhancement and diseasesuppression. The NP exposure route significantly influences particle uptake and accumulation byterrestrial plants. In addition, the substrate selection not only determines plant growth but alsoinfluences NP behavior. Many different types of substrates, including solid, semisolid, and liquidmedia, have been used for NP phytotoxicity tests. For example, in a hydroponic system, differentstrengths of Hoagland’s solution (or customized Hoagland’s solution) have been the most commonliquid media used for NP toxicity assays. With solid substrates, common growth media used ingreenhouse or growth room studies include promix, vermiculite, and natural soils, all of whichare significantly more complex than aqueous growth solutions. Here, factors such as soil texture,organic matter, soil pH, cation exchange capacity (CEC), and a range of other properties (Corneliset al. 2014) must be considered, as they all can uniquely impact NP behavior, bioavailability, anduptake by plants (Figure 1).

Owing to their high surface area and small size, NPs are highly reactive and homoaggregatewith NPs of similar size or heteroaggregate with natural colloids (Rodrigues et al. 2016) (Figure 1).For homoaggregation, previous studies have demonstrated that factors such as pH, ionic strength,

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and chemical composition exert a major role in controlling NP fate. For example, Baalousha (2009)reported that the increase of Fe oxide NP aggregation was dependent on NP concentration, pH,and natural organic matter content. When pH values were close to the point of zero charge, thehomoaggregation of Fe oxide NPs increased and maximum aggregation was achieved at low pHs(Baalousha et al. 2008). Similarly, the aggregation of silver (Ag) NPs was enhanced in the presenceof 10-mM Ca2+ due to ion binding and electrostatic screening effects. Conversely, ionic strengthand pH seem to have had no impact on the aggregation of polyvinylpyrrolidone-coated Ag NPs(Badawy et al. 2010); this could be ascribed to polyelectrolytes enhancing steric stabilization as afunction of the charged groups (Levard et al. 2012, Stankus et al. 2010). For heteroaggregation,Cornelis et al. (2013) reported that rapid aggregation of negatively charged polyvinylpyrrolidone-coated Ag NPs with positive sites on maghemite/montmorillonite (two common soil colloids)occurred, suggesting that natural colloids could significantly reduce the NP mobility and associatedrisk from off-site transport. Kaolinite particles heteroaggregated with nanoscale zero-valent iron(nZVI) at pH values ranging from 6 to 8, suggesting that charge heterogeneity on the surface of theclay minerals is sensitive to pH. However, the excess polyelectrolyte reduced nZVI aggregationand deposition onto soil particles (Kim et al. 2012).

Additionally, the process of NP dissolution is influenced by growth substrates, and this in-teraction can significantly alter overall NP phytotoxicity. For example, when comparing Ag NPdissolution in water versus bacterial growth medium, Maurer-Jones et al. (2013) found that 28%of Ag NPs dissolved in the bacterial medium in the predominant (87.8%) form of Ag(NH3)2

+,whereas only 13% of Ag NPs dissolved directly in the water. Similarly, bovine serum albumincould chelate Ag+ released from Ag NPs or prevent NH3-dependent dissolution by binding tothe surface of the NPs; in either case, subsequent nanotoxicity to an ammonia-oxidizing bacteria(Nitrosomonas europaea) was reduced (Ostermeyer et al. 2013). Given that substrate properties cansignificantly alter NP surface characteristics and aggregation, it is clear that the substrate shouldbe fully characterized prior to investigating NP uptake and distribution by terrestrial plants.

Nanoparticle Uptake and Distribution in Plants

NP accumulation and distribution are closely related to the NP-induced phytotoxicity to plants.Thus, we compare the NP uptake and distribution in plants from the aspects of particle size andsurface coatings as well as possible metal speciation within plant tissues.

Distribution and accumulation of nanoparticles in plants. Uptake and accumulation ofemerging contaminants by plants represent the first step to understanding the distribution and fateof the target contaminant within biota as well as an important basis for subsequent toxicity testingand food safety assessment (Figure 2a). In this section, we compare the uptake and distributionof NPs from the perspective of functionalized NPs versus bare/uncoated NPs, particle size, andmetal forms; we summarize the patterns of NP uptake and their possible biotransformation withinplant tissues as well as in the rhizosphere.

Coated versus uncoated nanoparticles. Because of their high surface-to-volume ratio, NPs canreadily interact with a range of moieties and functional molecules; this activity results in greaterdispersibility and stability, which can be exploited for a range of specific functions ( Jiang et al.2013). Ma et al. (2015b) reviewed the bioaccumulation of unmodified metal-based NPs in higherplants and reported that the bioaccumulation factor (defined as the ratio of the concentration ofmetal in roots or shoots to that in the substrate) of Ag and cerium (Ce) in plants treated withNP-amended Hoagland’s solution was higher than corresponding values in soils. However, a

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e

Vacuole Divalent metaltransporters

NPs

K+ channel

Protonpump II

Protonpump I

NP dissolution

NP sequestration

–COOH,–SH, –OH

AQP

H2O

a

Biotransformation

NPs

NPdissolution

Nodule

NP uptake andtransformation in

a plant-soil system

Legumeplant

c

Abscisic acid

Cytokinins

Jasmonates Gibberellin

Auxins

Brassinosteroids

Hormonehomeostasis

Defensive genes andhormone synthesis-

related genes

Nucleus

Phytohormone regulation

Cytosol

NPs

Induced molecularresponses

b NP-induced ROS NPs

NPs

NP dissolution

NP dissolution

NP exposure

ROS(H2O2; O2

.–)Detoxificationof NP-induced

oxidative stresses

Antioxidantenzymes

Thiol compounds(e.g., cysteine, GSH)

Phenoliccompounds

Oxidative defense mechanisms

or

Metabolites inrhizosphere

and in plants

Lower NPbioavailability;

alleviatephytotoxicity

Roles of metabolites for NPbiotransformation and toxicity

NP-induced damages

Vacuole

Membrane damage;electron chain

reaction compromise

Membrane damage; photosynthesis system

alteration; chlorosis

DNA damage andgenotoxicity

NP sequestration;membrane transporter

alteration

Cell membranedamage; ion leakage;

metal transporter/AQP gene alteration

Cell membrane Mitochondria Chloroplast Nucleus

+

d

Golgiapparatus

Endoplasmicreticulum

Lipidmembrane

recycle

Endocytic process

Surface-modified NPs

NPs

NPs NP dissolution

Cysteine,GSH

Thiol complex

Nanotoxicity NP detoxification

Trojan horse mechanism

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discussion of the role of chemical compounds secreted in the rhizosphere in the surface modifi-cation of NPs and whether this alters the bioavailability to plants is limited. With the increasinguse of functionalized NPs in many fields, several recent studies have focused specifically on thecomparison of uptake and accumulation between coated and bare NPs by plants. Here, we focuson the more widely used coatings and how they impact NP uptake by plants.

Barrios et al. (2016) first tested the uptake and translocation of Ce in tomatoes (Solanumlycopersicum L.) treated with either uncoated or citric acid–coated CeO2 NPs; they found that theCe content in 250 and 500 mg/kg surface-coated NP–treated roots was nearly 90% lower than withthe corresponding bare NPs. However, surface modification had no impact on Ce translocationfrom roots to shoots. Iannone et al. (2016) reported that with magnetic iron oxide (Fe3O4) NP–treated wheat (Triticum aestivum L.), the root Fe content in 20 mg/L bare NP–treated wheatwas threefold higher than that seen with citric acid–coated NPs, but no difference was evidentin either aerial tissues or seed. Similar findings were reported for Ni uptake by mesquite plants(Prosopis sp.) treated with nickel hydroxide [Ni(OH)2] NPs coated with citric acid (Parsons et al.2010). Conversely, gum arabic–coated Ag NPs exhibited more toxicity to Lolium multiflorum thanwas observed with the equivalent amounts of Ag+ ions or the supernatant of ultracentrifuged AgNP solution (Yin et al. 2011). Zhu et al. (2012) examined the uptake of three functionalized gold(Au) NPs (6–10 nm) assembled with different surface charges by four plant species and foundthat NPs with positive charges were readily accumulated as compared to the negatively chargedNPs. However, the negatively charged NPs were translocated to a greater extent from the rootsto shoots. Importantly, a mechanistic explanation for this behavior remains elusive.

Particle size and metal forms. Because of the unique properties of NPs, nanoscale size exertsan important effect on NP accumulation by plants. Yin et al. (2011) compared Ag accumulationin shoots and roots of Lolium multiflorum exposed to 6- and 25-nm Ag NPs in a hydroponicsystem; the Ag content in 6-nm Ag NP–treated roots was almost twice that of the 25-nm Ag NP–treated plants. No apparent difference in shoot Ag content was found between the two treatments.Another hydroponic study that focused on Au uptake by tobacco (Nicotiana tabacum L. cv. Xanthi )as a function of NP size (5–15 nm) showed that NP size had no impact on metal accumulation bythe plants ( Judy et al. 2010). de la Torre Roche et al. (2015) compared nano-sized lanthanum oxide(La2O3) particles with equivalent bulk-sized material in soil experiments and reported La contentin the tissues of lettuce (Lactuca sativa). When grown in 350 g of soil, an equivalent amount of Lawas found for bulk and nanoparticulate La2O3–treated soil, but when the soil mass was increasedto 1,200 g, the La content in both shoots and roots was significantly lower compared to thecorresponding bulk treatment, suggesting that the mass of substrate influenced metal uptake anddistribution in plants.

Conversely, another element in the lanthanide series, Ce, exhibited a different pattern of uptakeby plants. Hawthorne et al. (2014) measured the Ce content of zucchini (Cucurbita pepo L.) grown in1,228 mg/kg bulk or nanoparticulate CeO2–treated soil; the results showed that the Ce content in

←−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−Figure 2Plant response upon exposure to nanoparticles (NPs) and their possible transport at the cellular level. (a) NP uptake by plants andpossible biotransformation. (b) Induced levels of ROS result in oxidative stress and activate defense mechanisms, including antioxidantdefense mechanisms and metabolites in the rhizosphere and in plants. (c) Effects of NPs on phytohormones at the molecular andbiochemical levels. (d ) Endocytic processes by which NPs accumulate in plant cells, and (inset) the Trojan horse mechanism, whichexplains NP-induced cytotoxicity. (e) The role of the vacuole in sequestering NPs and alleviating nanotoxicity to plant cells.Abbreviations: AQP, aquaporin; GSH, glutathione; ROS, reactive oxygen species.

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NP-treated roots and stems was approximately five- and twofold greater than the bulk treatment,respectively, but no difference was evident in leaves and flowers. In another study, exposure to1,000 mg/kg bulk and nanoparticulate CeO2 did not result in a significant difference in Ce contentin either the shoots or roots of kidney beans (Phaseolus vulgaris var. red hawk) when grown in asandy loam soil (Majumdar et al. 2016). Collectively, it appears that particle size can contributesignificantly to NP uptake, but the role of other potential factors in the soil matrix (such as soiltexture or amount, as discussed above) or as part of the exposure scenario in altering the NP fateand behavior in the soil or in planta remains unknown.

In addition to the effect of size, NP dissolution can also affect accumulation by plants. To dis-tinguish the ionic dissolution effect from NPs themselves, appropriate ionic controls are necessarywhen evaluating NP uptake by and toxicity to plants (Bradfield et al. 2017, Dimkpa et al. 2015a,Doody et al. 2016, Ebbs et al. 2016). For example, Wang et al. (2016d) measured copper oxide(CuO) NP dissolution in water prior to investigating Cu uptake and toxicity in treated Arabidopsisthaliana; the results demonstrated that the Cu content in shoots and roots of different A. thalianaecotypes exposed to NPs was several-fold higher than with ionic Cu or bulk particle treatments.Similar findings were also reported in hydroponic Crambe abyssinica roots exposed to Ag NPs orAg+ ions (in the form of AgNO3), although these differences were not found in the shoots (Maet al. 2015a). Attempts to differentiate NP from ionic uptake are confounded by the fact that theprocess of NP dissolution is dynamic and dependent on many environmental factors (as discussedin the section titled Nanoparticle Exposure Patterns). When measuring NP dissolution in thepresence of plants, Yue et al. (2017) found that maize (Zea mays) accelerated La3+ release intowater as compared to plant-free controls, suggesting that exuded biomolecules or associated mi-crobial activity can play an important role in altering NP dissolution and dramatically alter NPuptake by plants. Additional studies in this area are highly recommended.

Carbon-based nanomaterials. The uptake and accumulation of carbon-based nanomateri-als (CNMs) by plants have been reported among many different species (Canas et al. 2008,Khodakovskaya et al. 2012, Larue et al. 2012, Lin et al. 2009, Miralles et al. 2012). The seedlingsof six crop species, including cabbage (Brassica oleracea), carrot (Daucus carota), cucumber (Cucumissativus), lettuce, onion (Allium cepa), and tomato, were exposed to functionalized and bare carbonnanotubes (CNTs) for up to 2 days, and scanning electron microscopy (SEM) images showedno visible CNT uptake in plant tissues (Canas et al. 2008). When examining the accumulationof multiwalled carbon nanotubes (MWCNTs) by plant cells using confocal imaging and TEMtechniques, Serag et al. (2010) found that MWCNTs, and especially those with a length less than100 nm, penetrated the protoplast cell membranes and localized in cell organelles such as vacuole,plastid, and nucleus. Similarly, Baoukina et al. (2013) reported that short pristine CNTs insertedthemselves into lipid membranes and the distribution of CNTs could be controlled by modifyingthe functional groups on the surface of the tubes. Importantly, most methods for determiningCNM accumulation are qualitative, such as SEM, confocal imaging, microwave-induced heating(Irin et al. 2012), TEM, and Raman spectroscopy. Several of these techniques are also limited interms of their use in biological samples due to method sensitivity and/or insufficient detectionlimits. Recently, Zhao et al. (2017b) used radiolabeled MWCNTs to investigate the uptake ofMWCNTs by A. thaliana and three common crops, including rice (Oryza sativa L.), maize, andsoybean (Glycine max). The results showed that the accumulation of MWCNTs in dicot plants(A. thaliana and soybean) was nearly 1.5- to 3-fold greater than in the monocot plants (rice andmaize). A recent review evaluating CNM quantification in biological matrices discussed the chal-lenges of distinguishing CNMs from the background carbon of soils and biological materials(Bjorkland et al. 2017). In addition, the development of robust extraction procedures for CNM

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measurement is still quite limited (Doudrick et al. 2013). The use of radiolabeled CNMs to deter-mine uptake by plants is perhaps the most promising technique, although the use of radioisotopescan present some unique challenges. In summary, based on the current literature on CNM uptakeby plants, it seems that the accumulation of CNTs in plants is possible but levels are quite lowand translocation may well be negligible (Bjorkland et al. 2017).

Nanoparticle presence and transformation in plants. TEM-EDS and SEM-EDS are twocommon and direct techniques to observe and locate NPs within plant tissues. Previous studieshave demonstrated that NPs can move through both symplastic and apoplastic pathways, reachingthe cortex; depending on NP properties and the plant species, the particles may then be transportedthrough the aerial tissues by both xylem and phloem (Ma et al. 2015b). Nhan et al. (2015) collectedxylem sap from 100 and 500 mg/L CeO2 NP–treated cotton (Gossypium) and detected aggregatedNPs in the sap using TEM. Similar findings were also reported for the sap collected from CuONP–treated maize and the observed NP aggregates were further confirmed by EDS (Wang et al.2012b). Importantly, CuO NPs were able to translocate back to the maize roots via phloem (Wanget al. 2012b). Sun et al. (2014) used fluorescently labeled mesoporous silica NPs to visualize Si NPtransport in plants and reported on the important role of the Casparian strip in minimizing NPpenetration into the xylem vessels. At the cellular level, a number of studies have demonstrated thatNPs can traverse plant cell walls and localize in the cytosol or within cell organelles. For example,Ji et al. (2017) reported that TiO2 NPs were present on chloroplast membranes in 1,000 mg/LTiO2 NP–treated rice; Ti presence was confirmed by EDS. In addition, CeO2 NPs were alsofound in the chloroplast, vacuole, and plasma membrane of cotton treated with different CeO2

concentrations under hydroponic conditions (Nhan et al. 2015). Similar evidence was also foundin CuO NP–treated maize (Wang et al. 2012b) and nickel oxide (NiO) NP–treated tomato (Faisalet al. 2013). However, the role of environmental factors (e.g., ionic strength, pH, organic matter)can be significant and may cause NP aggregation, thereby reducing accumulation in the plant andresulting in notable analyte deposition on the surface of the root epidermis (Zhang et al. 2011).

Plants have evolved to take up a variety of essential mineral elements from the growth substrate.Coincidentally, plants inevitably accumulate nonessential constituents, such as heavy metals andmetalloids, and emerging contaminants, such as NPs; some of these analytes can have adverseeffects on plant growth and subsequently reduce crop yield. Importantly, these emerging contam-inants can be affected by environmental factors that can directly or indirectly change the speciationof the contaminants, subsequently altering toxicity and bioavailability to terrestrial plants. Conse-quently, it is important to visualize elemental localization at the cellular and subcellular levels andto characterize analyte speciation by using synchrotron-based techniques, such as X-ray fluores-cence and X-ray absorption spectrometry (Zhao et al. 2014). Synchrotron-based techniques candifferentiate the in situ NP speciation in plants and further our efforts to understand the potentialmechanisms by which NPs accumulate and cause phytotoxicity (Castillo-Michel et al. 2017).

Previous studies have demonstrated that NPs can be transported from roots to abovegroundtissues via xylem, followed by transfer to the phloem and transfer back to the roots (Nhan et al.2015, Wang et al. 2012b). Recently, Ma et al. (2017) examined Ce speciation in the xylem andphloem of 200 and 2,000 mg/L CeO2 NP–treated cucumber seedlings using a root-split systemunder hydroponic conditions. The results showed clear biotransformation of CeO2 NPs, withapproximately 15% of Ce(IV) being reduced to Ce(III) in the roots and 20% to Ce(III) in theshoots. However, only CeO2 NPs were detected in the phloem of the untreated (blank sidewithout the addition of CeO2 NP) cucumber roots. A separate study demonstrated that CeO2 NPbiotransformation did not happen in cucumber roots after an incubation time of 3 h, implyingthat NP biotransformation requires specific conditions in the plant rhizosphere to facilitate the

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reduction of Ce(IV) to Ce(III) (Ma et al. 2015c). Hernandez-Viezcas et al. (2016) reported that theCe in 500 mg/L CeO2 NP–treated mesquite (Prosopis juliflora velutina) roots accumulated mainlyin the epidermis, remaining in the form of Ce(IV), indicating little overall biotransformation.After foliar spray of Ag NPs on lettuce, Larue et al. (2014) found that NPs were oxidized andAg+ ions formed Ag complexes with thiol-containing molecules. Similarly, in Ag NP–treated andAg2S NP–treated rice roots, the majority of Ag speciation was in the form of Ag-thiol complexesand Ag2S (Pradas del Real et al. 2017). Larue et al. (2016) similarly demonstrated that in AgNP–exposed lettuce, 33% of the NPs were in the form of Ag-glutathione (GSH), whereas 48%remained as elemental NPs. Significant evidence suggests that thiol-containing molecules bindwith Ag released from NPs as a defense mechanism to alleviate nanotoxicity to terrestrial plants(Ferretti et al. 2009). Such a phenomenon was also evident in a Ag NP– and Ag2S NP–treatedaquatic plant (Landoltia punctata) (Stegemeier et al. 2017). Interestingly, metal sulfidation was alsoobserved in CuO NP–treated rice during a life-cycle study (Peng et al. 2017).

In addition, NP biotransformation in the soil rhizosphere is important for understanding NPspeciation in plants. Peng et al. (2017) found that Cu speciation in soil CuO-NP treated for ricegrowth was mainly in the forms of Cu2S and Cu adsorbed on goethite during the flooding conditionand maturation stage. Another study of Ag NPs entering soils via sludge showed that more than79% of the total introduced Ag NPs were transformed to Ag2S, which significantly reduced Aguptake by plants (Wang et al. 2016c). In an Ag NP–treated and AgNO3-treated anaerobic versusaerobic paddy soils, more than 90% of Ag NPs were converted to Ag2S in the presence of organicmatter under the anaerobic conditions (Li et al. 2017). To date, NP-related biotransformation inplants has been studied under high-dose conditions (up to 4,000 mg/L), and most studies havebeen conducted in hydroponics to avoid possible confounding environmental factors. Althoughevidence for NP accumulation and speciation changes in the edible or reproductive portion ofcrop plants has been confirmed (Hernandez-Viezcas et al. 2013, Peng et al. 2017, Wang et al.2016d), questions related to the kinetics of NP biotransformation in the rhizosphere and in plantaremain unanswered. In addition, the role of root exudates and microbial secreta in modifying ortransforming NPs prior to plant uptake is largely unexplored.

Role of Biological Metabolites for Nanoparticle Biotransformation

In the rhizosphere, biological factors such as root exudates and microbial EPSs play a role inNP biotransformation by altering their surface properties, speciation, and bioavailability to plants(Figure 3). However, studies evaluating the composition of root exudates and EPSs in the pres-ence of NPs are limited. A metabolomics analysis of root exudates in Cu NP–treated cucumberrevealed that the presence of Cu NPs significantly elevated the amino acid content, which servedto sequester Cu NPs, and decreased the level of citric acid, which lowered the bioavailability ofCu2+ ions (Zhao et al. 2016a). In plants, the alteration of metabolites could also directly or indi-rectly affect NP biotransformation. For example, exposure of lettuce to Cu(OH)2 nanopesticidesvia foliar application demonstrated that the levels of a copper chelator, nicotianamine, increasedby 12- to 27-fold relative to the control, implying Cu(OH)2 NP detoxification via chelation pro-cesses (Zhao et al. 2016c). Additionally, evidence of elevated polyamines suggests the triggering ofplant defense mechanisms (Zhao et al. 2016c). Similarly, the presence of Cu(OH)2 nanopesticidessignificantly changed arginine and proline metabolic pathways, as well as the levels of fatty acidsand polysaccharides in exposed cucumber (Zhao et al. 2017a). Changes in plant metabolites uponexposure to different NPs may play an important role in altering the NP speciation and subsequenttoxicity to plants; however, a mechanistic understanding of these metabolite-driven processes islacking.

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Microbialcommunity inrhizosphere

Chelators(biosurfactants)

Organic acids(glucuronic acid and citric acid)

Hormones and enzymes(IAA and ACC)

Secretion from bacteria NPs and secretion interactions

Effects of microorganisms on NPs

NPs may impact the secretion anddiversity of microorganisms

Phase II

Rootexudates

Carbohydrates

Amino acids

Organic acids

Biotransformationstatus II

Mobilization orimmobilization

–COOH, –SH, –OH

Biotransformationstatus II

Mobilization orimmobilization

–COOH, –SH, –OH

Main components of root exudates NP and exudate interactions

NPs may alter the compositions and levels of root exudates

Root exudates may biotransform NPs or ionsreleased from NPs and affect NP uptake by plants

Phase I

Phase III

Rhizosphere ina plant-soil system

Ionsfrom NPs

NPs

Figure 3Interactions between biological compounds in the rhizosphere and nanoparticles (NPs). Phase I: The role of rhizosphere root exudatesin NP biotransformation and how the presence of NPs affects the level of root exudates. Phase II: NPs can significantly change thecomposition of the microbial community and subsequently alter the secretion of extracellular substances; in turn, these extracellularsubstances can potentially be involved with NP biotransformation (a hidden detoxification mechanism for xenobiotic compounds in therhizosphere). Phase III: In addition to their individual impacts on plants and microorganisms, the presence of NPs can also potentiallyinterfere with the mutually beneficial relationships between plants and microorganisms (such as nutrient uptake, biocontrol factors, andhormones). Abbreviations: ACC, 1-aminocyclopropane-1-carboxylate; IAA, indole-3-acetic acid.

Soil microorganisms in the rhizosphere also contribute to NP biotransformation and bioavail-ability to plants. In the rhizosphere of the clusterbean (Cyamopsis tetragonoloba L.), ZnO NP expo-sure increased the rhizospheric microbial population by 11–14% and biostimulated the activitiesof acid phosphatase, alkaline phosphatase, and phytase by 73.5%, 48.7%, and 72.4%, respectively(Raliya & Tarafdar 2013). A study of bacterial (Pseudomonas chlororaphis O6) colonization in theroots of CuO NP–treated bean (P. vulgaris) demonstrated that NP inhibited ferric reductase by50% but cupric reductase activity was increased by threefold compared with the control (Dimkpaet al. 2015b). This alteration in enzymatic activities may be indirect evidence that biomoleculesin the rhizosphere could be involved in NP biotransformation prior to plant uptake. Questions

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regarding the mechanistic interaction between plants and microorganisms as affected by NPs andas they affect NPs certainly point to the need for further study.

Plant Responses upon Exposure to Nanoparticles

As noted above, with the increasing use of NPs, potential adverse effects on ecosystem functionand specifically on terrestrial plants have become a common topic of investigation. In this section,plant responses to exposure to different types of NPs are summarized at the physiological andmolecular levels; also, the potential links between NP uptake and plant responses are discussed.

Molecular and biochemical responses. Molecular and biochemical analysis can help to furthermechanistic understanding of plant responses upon exposure to different types of NPs (Figure 2b).The induction of excess amounts of reactive oxygen species (ROS) in NP-treated plants is a com-monly reported finding (Mukherjee et al. 2014, Panda et al. 2011, Speranza et al. 2013, Zhaoet al. 2012). As a key metabolite, ROS are required in many important signaling reactions inplants, but they are also by-products in aerobic metabolism and can induce oxidative damagein plants (Mittler 2017). Thus, the roles of enzymatic and nonenzymatic antioxidants in scav-enging/counteracting ROS have been characterized in a large number of studies. For example,Ma et al. (2016) investigated antioxidant defense mechanisms in A. thaliana upon exposure tonanoparticulate CeO2 and indium oxide (In2O3); they detected ROS overproduction and eleva-tion of defense-related antioxidant activities, suggesting the occurrence of oxidative stress andthat antioxidant enzymes had a role in minimizing adverse effects. A similar antioxidant defensemechanism response was evident not only at the protein level, for example, in CeO2 NP–treatedrice (Rico et al. 2013a,b) and NiO NP–treated tomato (Faisal et al. 2013), but also at the tran-scriptional level (Burklew et al. 2012, Kaveh et al. 2013, Pagano et al. 2016). For example, Chenet al. (2016) reported the upregulation of genes encoding superoxide dismutase and catalase inneodymium oxide (Nd2O3) NP–treated pumpkin (Cucurbita maxima). In addition to the findingson commonly recognized ROS scavengers, the importance of GSH in enhancing plant tolerance toNP exposure has been explored in several studies. When the bacterial γ-glutamylcysteine synthasegene was overexpressed in Crambe abyssinica, transgenic plants exhibited a stronger tolerance to AgNPs and AgNO3 exposure as determined by fresh biomass and chlorophyll content, suggestingan important role of GSH in NP detoxification (Ma et al. 2015a). At the transcriptional level, therole of genes involved with GSH biosynthesis or GSH metabolism was characterized in nanopar-ticulate Ag–treated wheat (Dimkpa et al. 2012); nanoparticulate Ag–treated, CeO2–treated, andIn2O3–treated A. thaliana (Kaveh et al. 2013, Ma et al. 2013); and nanoparticulate Nd2O3–treatedpumpkin (Chen et al. 2016). Other nonenzymatic antioxidants such as anthocyanin and phenoliccompounds, as well as stress-related proteins (e.g., heat shock proteins), have also been reportedas having well-characterized roles in response to other types of abiotic stress (heat, drought, andcold) (Apel & Hirt 2004, Wang et al. 2004).

Phytohormones are signal molecules produced within plants and serve to regulate/mediatemany metabolic processes in plant growth and development (Stamm & Kumar 2010). The mainclasses of phytohormones include abscisic acid (ABA), brassinosteroids, gibberellins, ethylene,auxins, cytokinins, jasmonates, and peptide hormones (Bai et al. 2010). The levels of phytohor-mones upon exposure to different types of NPs have been considered as important end points toassess nanotoxicity in plants (Figure 2c). For example, ABA is not only a plant growth regulatorbut also a signaling molecule that mediates abiotic stress in plants (Mittler & Blumwald 2015,Zhu et al. 2015). Yue et al. (2017) determined the levels of ABA in La2O3 NP–treated maize atdifferent time points and found that the hormone levels were approximately two- to fourfold and

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three- to sixfold greater than in control shoots and roots, respectively; the authors suggested thatABA might act as a trigger to regulate aquaporin (AQP) genes, which can control water uptake byplants. Conversely, exposure to different concentrations (0–300 mg/L) of pristine MWCNTs ver-sus those coated with either Fe or FeCo resulted in significant decreases in ABA levels in the shootsand roots of rice; additionally, the levels of other hormones such as jasmonates, gibberellins, andauxins were also decreased in the rice seedlings relative to the control, leading to reduced yield inthe exposed seedlings (Hao et al. 2016). Other studies have also demonstrated the phytohormonedisruption upon exposure to NPs, such as nanoparticulate titanium oxide (TiO2)–treated rice ( Jiet al. 2017), CeO2-treated and Fe2O3-treated cotton (Le Van et al. 2015a,b), and Fe2O3-treatedpeanut (Arachis hypogaea) (Rui et al. 2016). Thus, analysis of phytohormone levels can provideimportant information relative to response and uptake of NPs by plants.

Regarding plant responses at the genetic level, two main techniques have been applied to in-vestigate specific gene regulation and the occurrence of DNA damage in plants upon exposure todifferent types of NPs: DNA damage assays and the quantitative real-time polymerase chain reac-tion. Liu et al. (2017) analyzed transcriptional levels of genes of the sulfur assimilation pathway,including sulfate adenylyltransferase, adenosine-5′-phosphosulfate reductase, and sulfite reduc-tase, in 200 mg/L TiO2 NP–treated shoots and roots of A. thaliana. The results demonstratedthat the majority of changes in the three genes were evident in the roots, which were in directcontact with the NPs (Liu et al. 2017). NP translocation from roots to shoots via xylem does occur,which suggests that NP accumulation may occur with water acquisition. Thus, investigation ofthe regulation of AQP genes in exposed plants could indirectly explain NP uptake and translo-cation, water transpiration, and plant defense mechanisms. Yue et al. (2017) characterized fourAQP families, including plasma membrane intrinsic proteins, tonoplast intrinsic proteins, Nod26-like intrinsic proteins, and small and basic intrinsic proteins in La2O3 NP–treated maize shootsand roots. Significant downregulation of AQP genes was consistent with the water transpirationresults, implying that reduction of water uptake might be one of the possible plant defense mech-anisms used to restrict NP uptake (Yue et al. 2017). Molecular responses of genes related to plantgrowth and nutrient transport have also been reported. NP dissolution could trigger changes in thetranscriptional levels of genes involved with metal uptake, which could subsequently induce eithernutrient surplus or deficiency. Several studies have indicated that the presence of nanoparticulateCeO2 and Au induced the downregulation of iron-regulating genes (iron-regulated transporter) inA. thaliana (Ma et al. 2016, Taylor et al. 2014). The transcriptional levels of genes encoding auxinsignaling (AXR2 and SLR1) in A. thaliana treated with CuO NPs were upregulated at differenttime points, suggesting that NPs can inhibit plant growth through lateral root inhibition (Wanget al. 2016d).

DNA damage provides direct evidence of NP-induced genotoxicity. Atha et al. (2012)measured the total amount of three oxidatively modified bases, 7,8-dihydro-8-oxoguanine(8-OH-Gua), 2,6-diamino-4-hydroxy-5-formamidopyrimidine (FapyGua), and 4,6-diamino-5-formamidopyrimidine, in radish (Raphanus sativus) and perennial ryegrass (Lolium perenne) uponexposure to CuO NPs and reported significant increases of all three compounds. Other techniquessuch as the comet assay (Faisal et al. 2013, Ghosh et al. 2010), mitotic index, and induction ofmicronuclei (by nanomaterials) under light microscopy (Patlolla et al. 2012) have also been usedto demonstrate that NPs can cause genotoxicity in plants, with subsequent physiological alterationor toxicity. Techniques to evaluate global tests such as proteome and transcriptome analysis havebeen applied to explore the molecular responses of NP-treated plants (Landa et al. 2015, Majumdaret al. 2015, Marmiroli et al. 2014). The global responses of NP-treated plants can exhibit a com-prehensive scenario of gene/protein regulations upon NP exposure, which can further provideuseful information for plant detoxification or tolerance to the emerging NPs in the environment.

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Physiological responses. Plant physiological responses are often the most visible evidence forNP-induced abiotic stress in plants. One of the most useful parameters that can indicate phy-totoxicity is plant biomass. A large number of studies have demonstrated that different types ofmetal- or carbon-based NPs can have both positive and negative effects on plant biomass, with re-sults dependent on plant growth substrates, NP type, dose, exposure scenario/duration, and plantspecies (Ma et al. 2015b). For example, the total biomass of lettuce grown in a sandy loam soilamended with TiO2 and Fe3O4 NPs (0–250 mg/kg) was largely similar to the control, althoughthe shoot biomass in the treatments with 50 mg/kg TiO2 and Fe3O4 NPs showed a notable bios-timulation (Zahra et al. 2015). Alternatively, ZnO NP–treated maize dry biomass was reducedin a dose-dependent fashion (Wang et al. 2016a). Other important parameters are chlorophyllcontent and net photosynthetic rate, which are typically positively correlated with fresh biomass.For example, in a life-cycle soil experiment, the presence of CeO2 and ZnO NPs had no apparentimpact on the photosynthetic system of corn as determined by net photosynthesis, transpirationrate, and stomatal conductance (Zhao et al. 2015). The total chlorophyll content in Ag NP–treatedtransgenic Crambe abyssinica was significantly higher than in the wild-type plant, suggesting thetolerance of transgenic plants to contaminant exposure (Ma et al. 2015a). Exposure to other NPssuch as TiO2 and Fe2O3 significantly elevated the chlorophyll content in cucumber and peanut,respectively (Rui et al. 2016, Servin et al. 2013). In summary, the physiological and molecularresponses of plants upon exposure to NPs are intimately linked to NP accumulation. NP uptakecan directly or indirectly trigger in vitro or in vivo plant responses; in turn, plant responses cansubsequently alleviate the nanotoxicity or decrease the NP uptake via a number of characterizedand uncharacterized pathways, which are discussed below.

Possible Transport Mechanisms of Nanoparticles at the Cellular Level

Investigation of NP transport and localization in plant cell organelles is important in understand-ing the mechanisms by which NPs cause adverse effects in plants as well as to the design of newnanomaterials for a range of purposes, including as agrochemical delivery systems. Endocytosis hasbeen identified as the main mechanism by which plant cells take up nanomaterials (Figure 2d).Serag et al. (2010) used Catharanthus roseus protoplasts and confocal imaging and TEM tech-niques to investigate the process by which MWCNTs penetrate the cell membrane. The resultssuggested that MWCNTs could enter the protoplast via endocytosis, in which several cell or-ganelles, including partially coated reticulum and Golgi complex, were involved in repair of theplasma membrane (Figure 2d). Additionally, MWCNT distribution in the plant cells was sizedependent; most MWCNTs less than 100 nm in length were observed in the vacuole, plastid, andnucleus (Serag et al. 2010). Using plant cells (Nicotiana tabacum L. cv. Bright Yellow), Liu et al.(2009) found that fluorescently labeled single-walled carbon nanotubes (SWCNTs) could pene-trate the plant cell wall and accumulated mainly in the vacuole without resulting in measurablecytotoxicity. Another study demonstrated that SWCNTs could be trapped by the bilayered lipidmembrane of A. thaliana chloroplasts, with subsequent enhanced photosynthetic activity (Giraldoet al. 2014). Endocytosis for nanomaterial relocalization within plant cells was also evident forquantum dots and silica NPs (Etxeberria et al. 2006, Torney et al. 2007).

Vacuoles are the largest (more than 80% of the total cell volume) organelle in plant cells andare the frequent sink for solute uptake via endocytosis (Figure 2e). Many studies using TEMobservation and fluorescence images have demonstrated that both metal- and carbon-based NPscan be sequestered in the vacuole (Bao et al. 2016, Huang et al. 2016, Serag et al. 2010). How-ever, research on the transport processes of NPs across the vacuolar membrane upon exposure islimited. The membrane protein channels (e.g., AQP) and two vacuolar proton pumps are known

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Food safetyassessment

Potential risks toecosystems

Nanotoxicity(microorganisms,

plants, and animals)

Risks to terrestrialfood chains

Adverse impactson agriculture

(crop yield, quality; nitrogen fixation;

carbon sequestration)

Applications insoils and agriculture

Step I Step II

Soil remediation(metal immobilization)

Nanofertilizer(mineral nutrient sources;

carrier; slow release)

Disease suppression(inhibition of

microbial infection)

Figure 4Flow chart of the environmental implications of nanoparticles (NPs) in agriculture. Prior to any NP application in agriculture, the fateand behavior of NPs and their toxicity to biota should be fully characterized and their risks to food safety and human health evaluated.Although the benefits of NPs in soil remediation and their potential impacts on crop growth have been investigated, the study of theeffects of NP accumulation on edible crops and the terrestrial food chain should be further evaluated in a comprehensive fashion.

to take up most solutes (Martinoia et al. 2000). NP dissolution could be coupled with binding bymetal transporters in the vacuolar membrane as well as with conjugation by thiol-containing com-pounds (GSH); this is a known metal detoxification pathway in higher plants (Dhankher et al. 2002,Ma et al. 2016). Analysis of vacuolar membrane AQPs at both protein and genetic levels couldbe used to study the uptake of emerging contaminants by plant vacuoles (Yue et al. 2017). Oneproposed mechanism of NP uptake by plant cells is called the Trojan horse mechanism, whichmaintains that NPs are internalized within plant cells and then release high levels of metal ionsthat result in cytotoxicity (Singh & Ramarao 2012). Ag NP uptake and transformation in microglia(BV-2) and astrocytes (alanine aminotransferase) demonstrated that this Trojan horse mechanismoccurred in NP uptake; Ag-thiol complexes suggested that large amounts of Ag+ ions were dis-solved and detoxified by compounds such as cysteine and GSH (Hsiao et al. 2015) (Figure 2d). Asdiscussed above, the contaminant sequestration takes place in vacuoles, where thiol compounds canconjugate xenobiotic compounds and alleviate their cytotoxicity. Thus, an in-depth understandingof the membrane transporters involved with NP mobilization into plant vacuoles is needed.

IMPLICATIONS

Potential Risks and Benefits to Ecosystems

A flow chart of the environmental implications of NPs is shown in Figure 4. This chart presentstwo steps, the potential risks of NPs to ecosystems and NP applications in agriculture; these twosteps can also mutually interact.

Risks to ecosystems. Evidence for NP-induced toxic effects on biota, including microorgan-isms, plants, and animals, in the soil environment has been extensively reported. Ge et al. (2016)

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reported that MWCNTs and graphene moderately affected the soil microbial community aftera one-year exposure; metal-based (CeO2 and ZnO) NPs significantly altered the compositionof the soil bacterial community, but the presence of soybean modified these effects on bacteria(Ge et al. 2014). In agriculture, the symbiotic relationship between legumes and rhizobium isof critical importance for nitrogen fixation. The inhibition of nodulation in Medicago truncatulaafter exposure to NP mixtures (TiO2, ZnO, and Ag) was a result of phytotoxicity rather thanmicrobial toxicity (Chen et al. 2015). A recent study reported that the presence of nanoparticulateAg and aged Ag2S had no apparent impact on the symbiosis between nitrogen-fixing bacteria andM. truncatula ( Judy et al. 2016). Given the limited and conflicting literature on this important topic,the potential impacts of NPs on nitrogen fixation in agriculture clearly need further study. NPtrophic transfer via a terrestrial food chain is another process that provides important informationon NP fate and behavior in the agroecosystem. Servin et al. (2016) demonstrated that weatheringof CuO NPs in soil increased the bioavailability of Cu within a food chain of lettuce, crickets(Acheta domesticus), and lizards (Anolis carolinensis), implying a potential unknown risk to humanhealth. Earthworms (Eisenia fetida) are also commonly used to investigate NP trophic transferin soil. Although 2,000 μg/kg Ag resulted in significant Ag accumulation in earthworm tissues,there were no decreases in the survival rate of earthworms; however, this high level of accumula-tion presents concerns relative to possible nanotoxicity through the food chain (Mukherjee et al.2017).

Benefits to contaminated soils. Several recent studies have focused on using the unique prop-erties of NPs to remediate or immobilize heavy metals or metalloids in contaminated soils. Ithas been reported that nZVI, acting as an electron donor, promoted arsenic transformation andreduced As(V) to As(III) and As(0) in 24 h (Ramos et al. 2009). Another mechanism of As re-mediation by iron oxide NPs is complexation with As in soils and sediments (Waychunas et al.2005). The addition of different types of commercial nZVI to As-, Hg-, and Cr-contaminatedsoils significantly immobilized these metals, implying a potentially promising strategy to enablethe reuse of metal-contaminated land (Gil-Dıaz et al. 2016, 2017; Wang et al. 2014). Many typesof contaminants coexist in soils, and the interactions among these analytes can directly determinepollutant fate and behavior in soil biota and plants. An increasing number of studies have inves-tigated the effects of co-contamination by NPs and other emerging contaminants (heavy metals,antibiotics) on higher plants; a common finding was that the presence of either metal- or carbon-based NPs can significantly reduce the accumulation of heavy metals, pesticides, and antibioticsin plants, suggesting that nanotechnology for soil remediation may be an efficient and sustainableapproach to recovering land for agricultural use (Cai et al. 2017, Deng et al. 2017, Liu et al.2017).

Crop Yield, Quality, and Safety as Affected by Nanoparticles

Safety concerns over NP applications in agriculture have been addressed in a number of studies.Alteration of crop yield and quality as affected by NP exposure has been evaluated by measuringthe content of mineral nutrients, fatty acids, and amino acids in the edible portion of crops. Forexample, Ebbs et al. (2016) measured the contents of Zn, Cu, and Ce in corresponding metaloxide NP–treated carrot and reported that exposure to all three NPs had no significant impacton dietary intake as calculated by the oral reference dose for chronic toxicity. Another long-termstudy demonstrated that the presence of nanoparticulate CeO2 and ZnO did not alter the contentsof macro- and micronutrients in maize (Zhao et al. 2015). However, metabolomic analysis in CuONP–treated cucumber fruit showed that nanoparticulate CuO exposure significantly altered the

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content of metabolites such as proline, glycine, and citric acid and interfered with C and Nmetabolic pathways (Zhao et al. 2016b). Determining the fatty acid profiles in A. thaliana, Yuanet al. (2016) reported that nanoparticulate CuO could elevate the degree of fatty acid saturationin plant cells as a result of NP-induced oxidative stress. This suggests that the potential risks tohuman health through compromised crop quality by way of altered biomolecule content is an areain need of increased research.

Potential Applications for Disease Control and Mineral Nutrient Enhancement

Nanomaterials, as novel fertilizers, have great potential in agriculture to sustainably increasefood production and quality. Because of their antimicrobial properties, nanomaterials can alsoeffectively suppress certain plant pathogens. In this section, we summarize potential applicationsof nanomaterials for disease suppression and nutrient enhancement in agriculture.

Disease suppression. Because of their unique properties, foliar application of NPs can effec-tively suppress both bacterial and fungal infection of plants. For example, because of photocat-alytic surface properties, TiO2 NPs can inhibit pathogenic disease and potentially enhance plantbiomass (Paret et al. 2013). CuO NPs resulted in greater protection from Phytophthora infestansin tomatoes as compared to the corresponding bulk particle (Giannousi et al. 2013). Notably,carbon-based NPs seem to have less impact on microbial inhibition. Ge et al. (2016) reported thatMWCNTs and graphene could result in soil DNA and altered bacterial communities after a one-year exposure in soils; however, alterations were not significant across the treatments, suggestingmoderate impact on soil microbial inhibition. Further investigation into the mechanistic basis fordisease suppression by NPs and systematic evaluation of the compatibility of NPs for sustainabledisease control should be addressed.

Nutrient enhancement. NPs can also be designed as carriers to enhance the delivery of fertil-izers. It is a common finding that the presence of metal-based NPs via soil amendment or foliarspray can significantly increase plant biomass and crop yield. For example, nanoparticulate ZnOfoliar spray notably stimulated clusterbean (Cyamopsis tetragonoloba L.) growth as determined byphenotype and fresh biomass (Raliya & Tarafdar 2013). Similarly, Fe2O3 NPs acted as a poten-tial iron fertilizer for peanut (Rui et al. 2016). In addition to micronutrient enhancement, recentstudies have also explored the design of new platforms for the slow release of nitrogen during cropgrowth. Under laboratory conditions, urea-coated hydroxyapatite NPs released urea 12 timesmore slowly (at a ratio of 6:1) than the pure urea, and crop yields increased by 60% compared tothe control (Chhowalla 2017, Kottegoda et al. 2017). Monreal et al. (2016) proposed a conceptualmodel for nanofertilizers whereby the nutrient deficiency in plants is detected through the use ofcoatings (biosensors embedded in polymer) on the surface of the micronutrient sources (nanopar-ticulate ZnO, CuO, and MnO) and nutrients are slowly released as a function of plant demand.Another idea is to incorporate NPs into microgels for nutrient-controlled release after foliar deliv-ery (Meurer et al. 2017). Although the efficiency of these novel techniques for NP assembly for thepurpose of nutrient enhancement still needs to be further evaluated, it is clear that NP applicationsas fertilizer delivery platforms could dramatically enhance agricultural efficiency and output.

CONCLUSIONS AND FUTURE DIRECTIONS

Numerous studies have demonstrated that inorganic NPs can be taken up by plants, and thismay have either beneficial or detrimental effects. NP uptake may occur through a variety of

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mechanisms, depending on plant type, environmental conditions, and NP characteristics (suchas composition, size, shape, charge, and surface chemistry). These NP characteristics may bechanged by their interactions with components in the environment, which may alter their uptakeand biological activity. Further research is required to better understand the relationship betweenspecific NP characteristics, their uptake by plants, and their potential biological effects. Thisknowledge could then be utilized to avoid potential environmental damage or negative healthimpacts associated with inorganic NPs and to design NP-based systems to enhance crop yield orquality.

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

This research was supported by the US Department of Agriculture (USDA)–Agriculture andFood Research Initiative (2011-67006-30181), USDA–National Institute of Food and Agricul-ture Hatch program (MAS 00475, MAS 00401, and CONH00146), and Binational AgriculturalResearch and Development Fund (IS-4964-16R).

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Annual Review ofFood Science andTechnology

Volume 9, 2018

Contents

Caenorhabditis elegans: A Convenient In Vivo Model for Assessingthe Impact of Food Bioactive Compounds on Obesity, Aging,and Alzheimer’s DiseasePeiyi Shen, Yiren Yue, Jolene Zheng, and Yeonhwa Park � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Updates on the Cronobacter GenusStephen J. Forsythe � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �23

Role of Proteins on Formation, Drainage, and Stabilityof Liquid Food FoamsGanesan Narsimhan and Ning Xiang � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �45

Diet, Microbiota, and Metabolic Health: Trade-Off BetweenSaccharolytic and Proteolytic FermentationKatri Korpela � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �65

Enzymes in Lipid ModificationUwe T. Bornscheuer � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �85

Radio-Frequency Applications for Food Processing and SafetyYang Jiao, Juming Tang, Yifen Wang, and Tony L. Koral � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 105

Uptake of Engineered Nanoparticles by Food Crops: Characterization,Mechanisms, and ImplicationsChuanxin Ma, Jason C. White, Jian Zhao, Qing Zhao, and Baoshan Xing � � � � � � � � � � � � 129

Lactic Acid Bacteria Exopolysaccharides in Foods and Beverages:Isolation, Properties, Characterization, and Health BenefitsKieran M. Lynch, Emanuele Zannini, Aidan Coffey, and Elke K. Arendt � � � � � � � � � � � � � � 155

Methods for the Control of Foodborne Pathogensin Low-Moisture FoodsAlma Fernanda Sanchez-Maldonado, Alvin Lee, and Jeffrey M. Farber � � � � � � � � � � � � � � � � 177

Effective Prevention of Oxidative Deterioration of Fish Oil:Focus on Flavor DeteriorationKazuo Miyashita, Mariko Uemura, and Masashi Hosokawa � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 209

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Advances in Understanding the Molecular Basis of the MediterraneanDiet EffectDolores Corella, Oscar Coltell, Fernando Macian, and Jose M. Ordovas � � � � � � � � � � � � � � � � � 227

Shelf Life of Food Products: From Open Labelingto Real-Time MeasurementsMaria G. Corradini � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 251

Dietary Advanced Glycosylation End-Products (dAGEs) andMelanoidins Formed through the Maillard Reaction: PhysiologicalConsequences of their IntakeCristina Delgado-Andrade and Vincenzo Fogliano � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 271

Stability and Stabilization of Enzyme Biosensors: The Key toSuccessful Application and CommercializationJose I. Reyes-De-Corcuera, Hanna E. Olstad, and Rosalıa Garcıa-Torres � � � � � � � � � � � � � � � 293

Visualizing 3D Food Microstructure Using Tomographic Methods:Advantages and DisadvantagesZi Wang, Els Herremans, Siem Janssen, Dennis Cantre, Pieter Verboven,

and Bart Nicolaı � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 323

Omega-3 Polyunsaturated Fatty Acids and Their Health BenefitsFereidoon Shahidi and Priyatharini Ambigaipalan � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 345

Natural Diversity in Heat Resistance of Bacteria and Bacterial Spores:Impact on Food Safety and QualityHeidy M.W. den Besten, Marjon H.J. Wells-Bennik, and Marcel H. Zwietering � � � � � � 383

Use of Natural Selection and Evolution to Develop New StarterCultures for Fermented FoodsEric Johansen � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 411

Milk Glycans and Their Interaction with the Infant-Gut MicrobiotaNina Kirmiz, Randall C. Robinson, Ishita M. Shah, Daniela Barile,

and David A. Mills � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 429

Synbiotics for Improved Human Health: Recent Developments,Challenges, and OpportunitiesJanina A. Krumbeck, Jens Walter, and Robert W. Hutkins � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 451

Tailoring Delivery System Functionality Using MicrofluidicsGiovana Bonat Celli and Alireza Abbaspourrad � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 481

Conversion of Agricultural Streams and Food-Processing By-Productsto Value-Added Compounds Using Filamentous FungiLauryn G. Chan, Joshua L. Cohen,

and Juliana Maria Leite Nobrega de Moura Bell � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 503

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FO09-TOC ARI 22 February 2018 7:0

Use of Electrohydrodynamic Processing for Encapsulation of SensitiveBioactive Compounds and Applications in FoodCharlotte Jacobsen, Pedro J. Garcıa-Moreno, Ana C. Mendes,

Ramona V. Mateiu, and Ioannis S. Chronakis � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 525

Formation, Structure, and Functionality of Interfacial Layersin Food EmulsionsClaire C. Berton-Carabin, Leonard Sagis, and Karin Schroen � � � � � � � � � � � � � � � � � � � � � � � � � � � 551

Recent Past, Present, and Future of the Food MicrobiomeFrancesca De Filippis, Eugenio Parente, and Danilo Ercolini � � � � � � � � � � � � � � � � � � � � � � � � � � � � 589

Recent Advances in the Application of Cold Plasma Technologyin FoodsChaitanya Sarangapani, Apurva Patange, Paula Bourke, Kevin Keener,

and P.J. Cullen � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 609

Errata

An online log of corrections to Annual Review of Food Science and Technology articles maybe found at http://www.annualreviews.org/errata/food

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