Uptake, translocation, and transformation of silver nanoparticles in plants

Abstract

Silver nanoparticles (AgNPs) have been globally applied in consumer products because of their antimicrobial properties. Broad applications inevitably release AgNPs into the natural environment. Moreover, AgNPs are produced naturally in soils. Plant uptake of AgNPs is the first step of their transfer along food chains, which ultimately raises concerns about human health. This review systematically summarizes the current knowledge on the uptake process of AgNPs in plants which is regulated by the physical properties of nanoparticles (e.g., size, surface coating, and morphology), environmental conditions (e.g., soil redox conditions, soil components, co-contaminants, and symbiotic microorganisms), and plant species (e.g., monocotyledon and dicotyledon). After internalization, AgNPs are translocated within plants and undergo biotransformation, including aggregation, oxidative dissolution, sulfidation, chlorination, and complexation with organic matter such as thiolates. Little is known about whether the internalized AgNPs and the transformed products will be accumulated in edible tissues of plants, which can raise the possibility of Ag to enter the food chains. Knowledge gaps about detailed mechanisms of transformation and translocation of AgNPs in planta still limit our understanding of Ag fate in plant–soil systems. This review intends to give a comprehensive assessment of the interaction between AgNPs and plants, highlighting that an integrated investigation of the full life cycle of AgNPs in plant–soil systems is needed to ensure safe application of nanoparticles.

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Danyu Huang

Danyu Huang received her Bachelor's degree in Environmental Science from Nanjing University. She is currently a Ph.D. candidate at Nanjing University under the supervision of Prof. Dongmei Zhou. Her research interests include the environmental fate of nanoparticles and the formation of reactive oxygen species in paddy soils.

Fei Dang

Fei Dang received her Ph.D. in Marine Environmental Science from Hong Kong University of Science and Technology in 2011. Since 2013 she has been an associate professor in the Institute of Soil Science, Chinese Academy of Sciences. Her research focuses on the biogeochemistry of trace metals and metallic nanoparticles, including their fate, bioavailability and trophic transfer, in the environment, as well as the application of nanotechnology.

Yingnan Huang

Yingnan Huang received her Bachelor's degree in Environmental Science from Shaanxi Normal University. She is currently a postdoctor at the Institute of Soil Science, Chinese Academy of Sciences, after receiving her Ph.D from the same institute. Her research interests include the biogeochemistry of heavy metals and the environmental fate and implications of nanoparticles and microplastics in soils.

Ning Chen

Ning Chen received his Ph.D. in Environmental Science from the Institute of Soil Science, Chinese Academy of Sciences in 2018. Thereafter, he has been an assistant researcher in the School of Environment at Nanjing University. His research focuses on the formation of reactive oxygen species and its implications for element or contaminant transformation during geochemical processes.

Dongmei Zhou

Dongmei Zhou is a professor at the School of the Environment at Nanjing University. He received his Ph.D. in Chemistry from Nanjing University in 1997, and worked in the Institute of Soil Science, Chinese Academy of Sciences until April, 2020. His current interests include the transportation and transformation of natural and engineered nanoparticles in the subsurface, biogeochemistry of heavy metals in the environment and remediation of soils contaminated with heavy metals and organic contaminants. He has published over 350 SCI papers.

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Environmental significance

The release of engineered AgNPs into the environment has raised concerns about their adverse impacts on plants, the basic components of ecosystems. The uptake of AgNPs in plants (especially crops) changes the fate of Ag in the environment and poses a risk to human health through trophic transfer. In this critical review, we reviewed the mechanisms regarding the uptake, translocation, transformation, and accumulation of AgNPs in plants, and their subsequent transfer along food chains. Critical issues and concerns were put forward to have a better understanding of nanoparticle–plant interaction. These findings will be helpful to explore the fate of AgNPs in terrestrial systems, especially in agricultural soils.

1. Introduction

Development of nanomaterial-based agrochemicals, such as nanofertilizers and nanopesticides, has sparked a technological revolution in the sustainable modern agricultural industry.^1–7 Nanomaterials offer great potential to enhance agrochemical delivery, suppress pathogen activity, and improve crop yield and quality.^8–10 Recently, silver nanoparticles (AgNPs) have been the focus of intense research due to their broad spectrum of antimicrobial properties.^11,12 AgNPs are used as nanopesticides in agricultural activities to control plant pathogens, which has led to their direct contact with plants.^13–19 Moreover, AgNPs are incorporated into a great number of consumer products including textiles, cosmetics, paints, and food packaging.^20,21 More than 50% of the biocidal silver products (e.g., disinfectants, algicides and water filters) registered in the U.S. Environmental Protection Agency contain AgNPs, with an estimated global production of hundreds of tons per year.^22,23 Daily use of consumer products introduces AgNPs into wastewater and later, intact AgNPs as well as transformed Ag species (mainly silver sulfide (Ag₂S)) can enter the agriculture environment via wastewater irrigation or sludge fertilizer usage.^24–29 Overall, the diverse applications inevitably increase AgNP release and anthropogenic input has been regarded as a new source of Ag to natural environments, making soil a major sink for these nanoparticles. Of particular concern are the potential biological impacts of nanoparticles on plants, which act as a major entry point of contaminants into food chains.^30–32

Researchers have made efforts to investigate the complex interaction between silver and plants. A bibliometric analysis was performed based on the associated studies from Web of Science (WoS) between 1992 and 2021. The time zone diagram of keywords focusing on the research evolution of AgNPs over 30 years is presented in Fig. 1. From 1992 to 2001, most of these studies focused on the accumulation and toxicity of dissolved silver in plants. From 2002 to 2011, with the rapid expansion of nanotechnology, studies were concentrated on the bioavailability of AgNPs and their plant uptake. From 2012 to 2021, the translocation and transformation of AgNPs in plants have been brought into focus. The uptake of AgNPs by plants plays a crucial role in the fate of Ag in the environment and is influenced by various factors, including exposure pathways, particle properties, soil components, plant species, etc.^33–36 However, the possible transformation of AgNPs in biological surfaces makes the uptake processes more complicated. After entering plants via different exposure pathways, AgNPs may aggregate into larger particles, form a biomolecule corona, or transform into various Ag species, such as AgCl, Ag₂S and Ag-thiols, which possess different translocation patterns compared with the pristine particles.^33,37,38 In the recent decade, models have been expanded from model plants (e.g., Arabidopsis) to crops (e.g., wheat and rice), as shown in Fig. 1, highlighting the possible transfer of AgNPs through crop uptake to humans.^39,40 Although the interaction between nanoparticles and plants has attracted much attention, to date, insufficient knowledge still limits our understanding of the uptake, transformation, and translocation of AgNPs in different plants.

Fig. 1 Time zone diagram of keyword co-occurring networks of papers concerning “AgNPs–plants interaction” between 1992 and 2021. The bibliometric analysis was performed using CiteSpace (version 5.7 R5) based on the database from Web of Science (WOS) between 1992 and 2021. The topic search used syntax “TS = ((silver OR Ag OR “particulate Ag” OR “Nano Ag” OR ((silver or Ag) AND (nanoparticle* OR particle*))) AND (plant) AND (uptake) AND (toxic*))”. Circle size is proportional to the number of publications. Co-citation rings and links within the same decades are shown in a unique color. The inset shows the circle size for the maximum and minimum number of records.

The worldwide application of nanotechnology, with the goals of sustainable agriculture and global food security, should be pursued together with comprehensive environmental risk assessments of nanomaterials to ensure ecological safety. Challenges and barriers exist to understand the fate of nanomaterials (such as AgNPs) in agroecosystems, including retention and transformation in soils, plant uptake, in planta transformation, accumulation, and trophic transfer. In this review, we discussed the current state of art and perspectives for the interaction between AgNPs and plants, focusing on the factors that affect uptake. The translocation, biotransformation, and accumulation of AgNPs inside plants have been summarized. Concerns over the incompleteness of experimental methods are also raised. Although research on the trophic transfer of AgNPs is inadequate, a deeper understanding of the fate of AgNPs in planta may be informative to evaluate their phytotoxicity and risks to the environment and human health.

2. Non-anthropogenic sources of AgNPs in plant-soil systems

Engineered AgNPs are introduced into plant-soil systems mainly through the usage of AgNP-containing nanopesticides, wastewater irrigation, and sludge application.^41–43 Although anthropogenic input is considered as the major source of AgNPs, the natural generation of AgNPs in soil cannot be neglected. In the environment, Ag exists mainly as Ag₂S, which was believed to be chemically inert.^44,45 However, the unheeded biotic or abiotic transformation of Ag₂S has led to the release of Ag⁺ and the generation of AgNPs.^46,47 Indeed, AgNPs have been discovered in silver-contaminated soils, where anthropogenic input (e.g., AgNPs in medical and consumer products) was unlikely.^48–50 These issues raise critical concerns regarding the background levels of naturally generated AgNPs in soils, which may be underestimated and can readily confound the quantification of Ag contamination induced by human activities.⁵¹ However, there are few studies on the natural formation of AgNPs in soils. Although natural formation processes and mechanisms of AgNPs have been widely documented in aquatic systems,^52–54 extrapolating these results to terrestrial systems is difficult due to significant distinctions between these two media. In this review, we proposed two main mechanisms for natural AgNP formation from Ag⁺ in soils, involving abiotic and biotic reduction.

Natural generation of AgNPs via abiotic reduction is of great concern, which is governed by multiple factors including light, natural organic matter (NOM), oxygen, temperature, pH, and co-existing ions (e.g., Fe²⁺/Fe³⁺).^53–61 Particulate organic matter (POM), typically comprising >50% soil organic matter, contributed to 11–31% of natural AgNP generation at the soil surface under natural conditions.⁶² The redox-active phenolic groups within POM are responsible for the formation of AgNPs both in the dark and under solar irradiation. However, the photoirradiation pathway prevails against the direct electron transfer pathway, due to the production of reductive superoxide anion radicals (O₂˙⁻) from phenol-like groups on insoluble humin under light exposure.⁶² These findings offer fresh insights into the interplay between POM and Ag, which seems to favor POM-rich soils as a sink for natural AgNPs.

A few studies have revealed the mechanisms of how NOM reduced Ag⁺ into AgNPs in natural scenarios (especially in water bodies) and found that light irradiation was the crucial factor. NOM can directly reduce Ag⁺ through ligand-to-metal charge transfer or indirectly by transferring electrons from their phenolic groups to dissolved oxygen to generate O₂˙⁻.^55,60,61 Without light irradiation, the redox-active functional group of soil organic matter can directly reduce Ag⁺ into AgNPs.^55,63 Charge transfer from the ligand to the metal has also been observed where Ag⁺ was firstly bound to the carboxylic group (–COO⁻) of HA to form Ag-HA complexes and then reduced into AgNPs by the transferred electrons.⁶⁴ Whether ligand-to-metal transfer or O₂˙⁻ dominates the reduction process remains unclear but it is suggested to be relevant to the inherent redox reactivity of NOM.^53,55,60,65 Different sources of NOM exhibit distinct reduction abilities, mainly due to the different contents of quinone and phenolic groups.^55,60

Given that the standard redox potential of Ag⁺/Ag⁰ is 0.8 V, smaller value redox couples (e.g., Fe²⁺/Fe³⁺) may be able to reduce Ag⁺ to AgNPs in thermodynamic feasibility.^66–68 Ferrous iron can directly reduce Ag⁺ under sunlight irradiation or indirectly by generating O₂˙⁻ under aerobic conditions.^68,69 The Fe²⁺/Fe³⁺ redox couple can also act as an electron shuttle to promote the electron transfer from NOM to Ag⁺, thus enhancing the formation of AgNPs.^67,70 Despite dissolved Fe²⁺, ferrous iron is also presented as Fe(II)-bearing minerals in natural soils.⁷¹ Green rusts, layered Fe(II)/Fe(III) hydroxides, have also been found to reduce Ag⁺ into AgNPs under dark conditions.^72,73 Notably, given the heterogeneity in soil environments (NOM associated with minerals), the abiotic pathways for formation of AgNPs could be more complex in nature.

Although not fully understood, the natural formation of AgNPs in soil via biotic pathways also has significant implications for the environmental fate of Ag. The potential contribution of microorganisms has been early discovered in a silver mine, in which the living bacteria reduced Ag⁺ into AgNPs.⁷⁴ Later, extracellular production of AgNPs by fungus and protozoan has also been observed.^75–78 The biotic reduction mechanisms are complicated but can be divided into two categories: enzyme-mediated and non-enzyme-mediated reduction. AgNPs can be synthesized by enzymes, especially nitrate reductase.^79,80 In the extracellular region of microorganisms, reductive O₂˙⁻ generated by oxidoreductases (e.g., NAD(P)H oxidases) is responsible for AgNP production.⁷⁶ Besides, non-enzyme mediated reduction is also suggested because of the redox ability of extracellular polymer substances (EPS).^52,81,82 Reducing saccharides containing hemiacetal groups and proteins containing cysteine, as components of EPS, can reduce Ag⁺ into AgNPs.^81,83 However, most of these studies were conducted in pure culture systems; thus it is hard to extrapolate these conclusions to a real soil environment and to evaluate the contribution of microorganisms to natural generation of AgNPs.

In addition to microorganisms, root exudates of plants can promote in vitro AgNP formation at the root surface within a few hours.^84–86 For example, the intact root surface of 11 diverse families of angiosperm plants shows potential to reduce Ag⁺ into AgNPs (5–50 nm) within 24 h, independent of microorganisms.⁸⁶ Root exudates containing reducing sugars and low molecular weight (0–3 kDa) organic acids have been identified as electron donors for the light-induced formation of AgNPs.⁸⁵ The released chlorine ions from the root surface could promote these processes by generating photoreactive semiconductor AgCl which is thereby converted to AgNPs under irradiation.^61,84,85 With the presence of plant root exudates, the formation of AgNPs was observed to follow a pseudo-first-order (k = 0.3466 h⁻¹)⁸⁵ or a second-order kinetics reaction (k = 1.11 mM⁻¹ h⁻¹).⁸⁴ Therefore, generation of AgNPs in the root zone will lead to direct exposure of plants and further AgNP uptake via roots.

3. Uptake of AgNPs in plants

The uptake of nanoparticles in plants has been regarded as their major entry point to food chains.^30–32 Thus, it is essential to obtain mechanistic insights into the uptake processes. Progress has been made in elucidating the uptake mechanisms of AgNPs. Multiple influencing factors (e.g., exposure pathway, environmental conditions and plant species) have been demonstrated in Fig. 2.

Fig. 2 Schematic diagram of the uptake of AgNPs in plants and the influencing factors.

3.1 Uptake pathway of AgNPs

Foliar uptake and root uptake are two major uptake pathways of AgNPs in plants. Spraying agrochemicals directly onto plant leaves is an effective and economic approach in agricultural management.^1,87,88 As nanopesticides, AgNPs are applied to fight against plant pathogens and insect pests through foliar exposure.^17–19 Natural generation of AgNPs in soils, together with the disposal of Ag-containing sewage sludge or wastewater in agricultural soil, will lead to root exposure to AgNPs.^85,89,90 Petiole feeding and trunk injection of nanoparticles are also applied in crop disease control but have not received much attention because of the limited applicable plants (normally trees).⁹¹

3.1.1 Foliar uptake. Plants leaves can take up AgNPs via cuticular and stomatal pathways.⁹² The waxy hydrophobic cuticle has small polar pores (∼2 nm),^93,94 suggesting that particles below 2 nm in size can penetrate directly through the cuticle into plant tissues. For larger particles, the uptake through stomatal openings is supposed to be feasible, because the estimated equivalent pore radius of stomata is larger than 20 nm.⁹³ The observed stomatal size ranges from a few to tens of micrometers, varied between different plant species.^95–98 The stomatal density (number of stomata per unit of area) is also dependent on the plant species and environmental conditions (e.g., atmospheric CO₂ concentration and light intensity), in ranges of dozens to hundreds of pores per mm.^99–102 Other leaf surface features, such as hydathode pores (a few to several μm) that allow direct access of nanoparticles to vasculature,¹⁰³ and trichomes, although they have not yet been demonstrated as a route for nanoparticle uptake, may also play a role in nanoparticle internalization.^104–106

Several studies have shown the presence of AgNPs in leaf stomata and other plant tissues with the aid of high-resolution microscopy (e.g., confocal laser scanning microscopy¹⁰⁷ and transmission electron microscopy¹⁰⁸), synchrotron-based X-ray imaging techniques (XAS),³⁷ and single-particle inductively coupled plasma mass spectrometry (sp-ICP-MS).¹⁰⁹ Using SEM and μ-XANES, Larue et al. observed that AgNPs (38.6 nm) aggregated into larger particles (2–3 μm) on the surface of lettuce (Lactuca sativa L.) leaves and small AgNPs were internalized in leaf tissues including the epidermis, mesophyll, and vascular tissues. They speculated that AgNPs can be entrapped by the cuticle and then enter the leaf through stomata.³⁷ Recently, He et al. reported that stomata were the key to internalizing AgNPs into plant leaves.¹¹⁰ Whether the cuticular or stomatal pathway dominates the AgNP uptake through leaves still needs further investigation for different plant species. Cuticle thickness, stoma size, and density may control the uptake of AgNPs.¹⁰⁵ Abundant stomata on leaves may allow rapid and efficient uptake of nanoparticles.¹¹¹ For instance, an increased uptake of copper oxide nanoparticles (CuO NPs) (up to 6.8–fold) was recorded in wheat leaves with open stomata.¹¹² With stomatal aperture diameter reduction (from ∼9 μm to ∼5 μm), the Zn concentrations in wheat leaf apoplast and cytoplasm decreased by 33.2% and 8.3% upon foliar exposure to zinc oxide nanoparticles (ZnO NPs), indicating the noticeable role of stomata in foliar exposure.¹¹³

Leaves can absorb AgNPs with size in the range of 10–40 nm (Table 1), but the precise size exclusion limits for AgNPs in different plants have not been quantitatively determined. The properties of both nanoparticles and the leaf surface regulate their interaction, as reflected in the uptake rate variation.^105,114,115 In terms of other NPs, Hu et al. found that low surface tension (∼22 mN m⁻¹) would allow rapid foliar uptake (<10 min) of carbon dots with hydrodynamic size larger than 2 nm.¹¹⁶ Kranjc et al. found that plants with a low foliar surface free energy (SFE) were more likely to retain platinum nanoparticles than plants with high SFE.¹¹⁷ Recently, Gao et al. reported that the SiO₂ shell enhanced the uptake of ZnO NPs in tomato (Solanum lycopersicum) leaves while no Zn uptake was observed with pristine ZnO NPs, although the mechanisms were unknown.¹¹⁸ The classical Derjaguin-Landau-Verwey-Overbeek (DLVO) model^91,119 or new empirical models such as nanoparticle-leaf interaction empirical models proposed by Hu et al.¹¹⁶ will be helpful to predict the interaction between nanomaterials and the plant leaf surface. Albeit with few publications, systematic investigation on the role of plant leaf physiology (for instance, hydrophobicity/hydrophilicity and roughness) in nanoparticle uptake is needed to determine the factors that control the interaction between AgNPs and the leaf surface and to investigate the uptake mechanisms.

Table 1 Summary of studies on AgNP uptake, translocation, accumulation, and toxic effects in plants

Nanoparticles	Initial size/nm	Surface potential/mV	Plant species	Exposure condition	Uptake rates	Uptake rate constants	TFshoot/root	Translocation and accumulation	Observed toxicity	Ref.
“—” represents information is not available.
PVP-AgNWs	43 nm diameter × 1.8 μm length	—	Lettuce (Lactuca sativa L.)	Root exposure, hydroponic, 0.086 mg L^−1, 18 d		0.136 ± 0.006 d^−1 (particulate Ag)	0.010 ± 0.001	—	Inhibited the growth of plants significantly with EC50 values ranging from 0.32 to 0.49 mg L^−1	124
PVP-AgNPs	13.4 ± 4.9	−19.1 ± 1.9	Wheat (Triticum aestivum L.)	Root exposure, hydroponic, 0.1–10 mg L^−1, 8 h	—	4.3 ± 0.6 to 5.2 ± 0.6 L kg^−1 h^−1 (particulate Ag)	—	Translocated from roots to shoots	—	126
PVP-AgNPs	14.5 ± 0.7	−18.4 ± 2.1	Wheat (Triticum aestivum L.)	Root exposure, hydroponic, 2–30 mg L^−1, 8 h	8.0–39.0 mg kg^−1 h^−1 (particulate Ag)	1.1 ± 0.1 L kg^−1 h^−1 (particulate Ag)	—	Aggregated and accumulated in the cytoplasm of root apical meristem cell	Destroyed plasma membrane integrity and caused cell death in root tips	123
PVP-AgNPs	28.3	−31.5	Green alga (Chlorella vulgaris)	Hydroponic, 0.5–5.0 mg L^−1	—	0.233 ± 0.024 L g^−1 d^−1 (particulate Ag)	—	Localised in starch granules within the chloroplast of C. vulgaris	IC50 value of 9.3 ± 0.1 μg L^−1	138
PEG-AgNPs	22.0	−21.0	Green alga (Chlorella vulgaris)	Hydroponic, 0.5–10 mg L^−1	—	0.339 ± 0.020 L g^−1 d^−1 (particulate Ag)	—	Localised in starch granules within the chloroplast of C. vulgaris	IC50 value of 49.3 ± 5.2 μg L^−1	138
Cit-AgNPs	22.0	−31.6	Green alga (Chlorella vulgaris)	Hydroponic, 0.5–4.0 mg L^−1	—	0.246 ± 0.031 L g^−1 d^−1 (particulate Ag)	—	Localised in starch granules within the chloroplast of C. vulgaris	IC50 value of 9.2 ± 1.0 μg L^−1	138
PVP-AgNPs	12.2 ± 3.1	−18.8 ± 1.8	Rice (Oryza sativa L.)	Root exposure, hydroponic, 10 mg L^−1, 2 d	—	—	0.0013 ± 0.0044	Translocated from roots to shoots	—	188
PVP-AgNPs	9.37 ± 1.83	−24.5 ± 0.3	Rice (Oryza sativa L.)	Root exposure, hydroponic, 2–20 mg L^−1, 5 d	—	—	0.0024–0.0123	Translocated from roots to shoots. Accumulated in the middle lamella of roots	—	189
PVP-AgNPs	10	—	Soybean (Glycine max)	Root exposure, hydroponic, 1 mg L^−1, 7 d	—	—	0.05	Translocated from roots to stems and leaves	Decreased transpiration rates, mediated oxidative stress, increased ROS, and MDA contents	194
AgNPs	15–20	−7.54	Cowpea (Vigna unguiculata L.)	Root exposure, hydroponic, 0.6 mg L^−1, 14 d	—	—	0.0047 (cowpea)	Translocated from roots to shoots	Decreased root elongation rates and fresh biomass	209
			Wheat (Triticum aestivum L.)				0.0134 (wheat)
PVP-AgNPs	12.2 ± 3.8	−9.25 ± 0.19	Rice (Oryza sativa L.)	Root exposure, hydroponic, 1 mg L^−1, 4 h	34.4 mg kg^−1 h^−1 (total Ag)	—	—	—	—	219
AgNPs	20	−15.4–−9.5	Lettuce (Lactuca sativa L.)	Root exposure, hydroponic, 0.1–10 mg L^−1, 15 d	—	—	0.009–0.037	Translocated from roots to shoots	Decreased fresh biomass of roots and shoots	255
									Increased the content of O2^− and MDA in shoots and H2O2 in roots
PVP-AgNPs	10	—	Wheat (Triticum aestivum L.)	Seed exposure, 1–10 mg L^−1, 5 d	—	—	0.038	Accumulated in the cell wall surface in the outer cells of the root apex	Reduced length and fresh weight of roots and shoots	287
PVP-AgNPs	20	−8.8 ± 0.65	Tomato (Lycopersicon esculentum)	Root exposure, hydroponic, 10–30 mg L^−1, 7 d	—	—	0.38–0.62 (particulate Ag)	Translocated form roots to shoots and leaves	Upregulated membrane transporters H^+-ATPase, potassium transporter, and sulfate transporter	283
							0.75–0.81 (total Ag)	Aggregated in root cell wall	Resulted in larger xylem cells

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3.1.2 Root uptake. After reaching the root surface, smaller AgNPs (<40 nm) can directly pass through the structure of the cell wall,^107,120,121 while larger AgNPs may enter the cytoplasm through endocytic uptake, pore formation or wounds,¹²² but direct evidence is still lacking. It is noteworthy that the size limitation of uptake should be determined by the minimal size of AgNPs in the experimental suspensions but not the average diameter.

A fundamental issue is to differentiate the relative contribution of particles and dissolved ions during root uptake because AgNPs may dissolve in the experimental medium. A variety of methods have been used to prove the direct uptake of AgNPs.^123–126 Conventional experiments were conducted by exposing individual plants to AgNPs or Ag⁺ ions separately. Some studies reported that plants exposed to AgNPs accumulated higher content of Ag compared to those exposed to Ag⁺ at the same dosages,^127,128 while others found that there is more Ag in plant tissue upon exposure to Ag⁺ and it was the ionic Ag released from the dissolution of AgNPs that were responsible for the uptake.^129,130 These contradictory results may be explained by the interference of the possible AgNP dissolution in the exposure medium or at the biological interface. Using dual stable isotope tracing (¹⁰⁷AgNO₃ and ¹⁰⁹AgNPs), Yang et al. confirmed the direct uptake of AgNPs and found that AgNPs were the main Ag species accumulated in rice roots when they were exposed to particles and ions at 50 μg L⁻¹ simultaneously for 14 days.¹²⁵ They suggested that Ag⁺ ions mainly located on the root surface, possibly due to the combination of free Ag⁺ ions with hard and soft ligand residues on the cell wall (e.g., hydroxyl, carboxyl, amino, and thiol groups), thus limiting the internalization of Ag⁺ ions. Wu et al. also found that the uptake of particles denoted as PVP-coated silver nanowires (AgNWs, 43 nm diameter × 1.8 μm length) accounted for more than 85% of accumulated Ag in lettuce for 18-day exposure.¹²⁴ Our group found that the direct uptake of AgNPs by 15-day wheat seedlings dominated relative to dissolved Ag uptake when the dissolution of AgNPs was less than 1.2%, suggesting that the relative contribution of particulate uptake varies as a function of AgNP dissolution.¹²⁶

3.2 Uptake kinetic model

In recent decades, empirical biodynamic models have been developed to describe the uptake kinetics of nanoparticles in organisms (especially invertebrates).^131–137 To date, the uptake kinetic models of AgNPs have only been applied to a few plants, including wheat,^123,126 lettuce,¹²⁴ and green alga.¹³⁸ The linear relationship of accumulated Ag concentration in plant tissues and exposure time was observed in these studies. Thus, a kinetic model for AgNP uptake in plants can be simplified as follows:^124,126

d[Ag]_plants/dt = k_u,total × [Ag]_total

k_u,total × [Ag]_total = k_u,NP × [Ag]_NP + k_u,diss × [Ag]_diss

where k_u,total, k_u,NP, and k_u,diss represent the overall uptake rate constants of AgNP suspensions, nanoparticles and dissolved Ag⁺, respectively; [Ag]_total, [Ag]_NP, and [Ag]_diss represent the concentration of total Ag, AgNPs and dissolved Ag⁺ in the exposure medium, respectively. k_u can be calculated as the slope of uptake rates and the corresponding exposure concentrations.¹³⁹ In this model, the elimination rate of Ag is assumed to be negligible for higher plants. This dynamic model can distinguish the contribution of nanoparticles' uptake and dissolved ions' uptake and is suitable for higher plants. Given the possible elimination process, Ribeiro et al. and Zhang et al. suggested an empirical model for the uptake and elimination of AgNPs in algae:^140,141

Uptake: C_Algae(t) = k_u/k_e × C_media × (1 − e^(−k_e×t))

Elimination: C_Algae(t) = k_u/k_e × C_media × (1 − e^{(−k_e×(t−t_c))} − e^(−k_e×t))

where C_Algae(t) is the silver concentration in the algae at time t; k_u and k_e represent the uptake rate constant and elimination rate constant of total silver, respectively; C_media is the silver concentration in the exposure media.

The uptake rate constants will help to predict the uptake tendency of different Ag species in plants. Although there are several concerns over the application of uptake kinetic models, for example, whether the uptake rate constants obtained from simplified hydroponic experiments can be used to predict the plant uptake of AgNPs in complex soil matrices, these results are a first step towards the development of a dynamic modeling approach to assess the uptake of AgNPs in plants.

3.3 Factors affecting uptake processes

The physicochemical properties of both particles and soil govern the fate of metal nanoparticles in plant-soil systems. In most studies, hydroponic experiments were conducted to investigate the effect of a certain factor, which have provided a foundation to explore plant uptake of nanoparticles in more complex realistic soil matrices.

3.3.1 Properties of AgNPs. The physicochemical properties of nanoparticles, for instance, size, morphology, surface coating, and charge, affect their interaction with biological surfaces. Particle size is a crucial factor as smaller nanoparticles have a higher tendency to be internalized by plants.^34,38 More Ag accumulated in plant tissues after exposure to smaller particles than larger particles at the same dosage.^142,143 For example, poplars (Populus deltoides × nigra) accumulated more Ag upon exposure to 5 nm AgNPs than 25 nm AgNPs (0.1 mg L⁻¹) after 7-day hydroponic exposure.¹⁴³ Torrent et al. found that lettuce (Lactuca sativa L.) roots accumulated more Ag upon exposure to AgNPs with small size (75 nm PVP-AgNPs and 60 nm citrate-AgNPs) than larger size (100 nm PVP- and citrate-AgNPs).¹⁴⁴ Similar results were observed for other metal nanoparticles (e.g., CeO₂ NPs and ZnO NPs) in different plants (e.g., cucumber and common bean), indicating that nanoparticles with smaller size are more bioavailable to plants.^92,145–147 However, size-specific dissolution of AgNPs has been reported, with greater dissolution for smaller particles.^148,149 Thus, higher Ag content in plant tissues upon exposure to smaller AgNPs may be ascribed to the direct uptake of particles as well as the released Ag⁺.^150,151

Coating changes particle surface properties (e.g., surface charge and hydrophobicity/hydrophilicity) to provide electrostatic repulsion between individual nanoparticles to prevent aggregation, which also makes nanoparticles more mobile and more phytoavailable than bare nanoparticles.^152–154 Frequently used coating agents in AgNP synthesis include polyvinylpyrrolidone (PVP), gum Arabic (GA), citrate, cetyltrimethylammonium bromide (CTAB), etc.^155–157 Surface coating modulates the interaction between nanoparticles and biological surfaces, which affects the potential uptake of nanoparticles.^158–160 Due to the negative charge in the root surface,^161,162 positively charged nanoparticles are more adhesive to the root surface than negatively charged nanoparticles.^119,163,164 For instance, AgNPs modified with a cationic stabilizer such as CTAB (5.6 nm, zeta potential (ζ) = 42.5 mV) can induce more Ag uptake in onion (Allium cepa L.) roots compared to citrate-AgNPs (61.2 nm, ζ = −39.8 mV) and PVP-AgNPs (9.4 nm, ζ = −4.8 mV) after 72 h of hydroponic root exposure.¹⁵⁷ The silver content in the leaves of tobacco (Nicotiana tabacum L.) exposed to 100 μM CTAB-AgNPs (56 nm, ζ = 44.67 mV) for 7 days was 8.84 ± 1.33 μg g⁻¹, higher compared to those exposed to citrate-AgNPs (24 nm, ζ = −23.78 mV) (3.65 ± 0.9 μg g⁻¹).¹⁶⁵ The uptake rate constants in green algae were similar for PVP-AgNPs (0.233 L g⁻¹ d⁻¹) and citrate-AgNPs (0.246 L g⁻¹ d⁻¹), corresponding to their similar zeta potential (−31.5 mV vs. −31.6 mV), which are also reflected in semblable toxicity.¹³⁸ A recent study found that the uptake rate constants of polyethylene-coated AgNPs (positively charged) (9.56–13.28 L g⁻¹ h⁻¹) were ∼20 times higher than those of negatively charged AgNPs (negatively charged) (0.36–0.55 L g⁻¹ h⁻¹) for freshwater algae (Chlorella vulgaris).¹⁴¹ Similarly, the uptake rate of CdSe/CdZnS quantum dots with cationic coating was 10 times faster than those with anionic coatings, possibly due to electrostatic attraction to the negatively charged root cell wall.¹⁶⁶ Recently, Yan et al. reported that the uptake pathway of AgNPs in a freshwater phytoplankton (Chlamydomonas reinhardtii) depended on the surface coating. Citrate-AgNPs (ζ = −23.75 mV) were internalized mainly through the apical zone of the cell near the flagella, whereas the aggregation-induced emission fluorogen-coated AgNPs (ζ = −46.3 mV) were internalized through endocytosis.¹⁶⁷ These findings indicate the critical role of surface coating in the uptake processes of AgNPs in plants.

Multiple morphologies of AgNPs are created in engineered applications including spherical silver nanoparticles,¹⁶⁸ silver nanocubes,¹⁶⁹ and silver nanowires.¹⁷⁰ Besides, naturally formed AgNPs in soil are nearly spherical.⁶² Studies mainly focused on physiological alterations of plants,^171–173 ignoring underlying variations in uptake and accumulation of AgNPs with different morphologies. Morphology-dependent impacts on organisms and communities (including algae and bacteria) have been observed in a lotic ecosystem, highlighting the ecological risk of Ag nanoplates.¹⁷⁴ Toxicity differences in ryegrass (Lolium multiflorum) may be ascribed to the increased uptake of a certain morphology of AgNPs.¹⁷¹ Thus, AgNPs may display morphology-based uptake patterns in plants, which has not been explored yet.

Regulation of AgNP uptake in plants becomes possible through manipulating particle properties, especially surface charge. However, although the crucial role of particle properties has been proposed based on laboratory investigation, whether these pristine characteristics have a vital effect on the realistic uptake remains unclear, due to the possible physical and chemical transformations of nanoparticles in natural environments. A recent study based on machine learning found that the composition and size of nanoparticles were the major parameters affecting the root concentration factor (the ratio of nanoparticle concentrations in root versus growth medium) in hydroponic systems, while soil organic matter and clay contents were the most influential ones in soil systems.¹⁷⁵ The uptake dependencies of AgNPs on size and surface charge may be weaken by the agglomeration process and over-coating of NOM under realistic environmental conditions.¹⁷⁶ Hence, the interplay between nanoparticles and surrounding environments should be fully investigated when extrapolating the results from hydroponic experiments to soil systems.

3.3.2 Environmental factors. In a typical plant-soil system, the interaction between AgNPs and plants will be affected by multiple environmental factors. Once they entered the soil, AgNPs are retained by soil components or undergo biotic and abiotic processes. Soil physical-chemical properties play a major role in the mobility of AgNPs.^177–181 The soil-water distribution coefficient (K_D) values of citrate-AgNPs increased from 100 to 10 000 L kg⁻¹ between pH 4 and 8, indicating the strong soil sorption capacity of AgNPs.¹⁸² Upon root exposure to 0.15 mg kg⁻¹ AgNPs for 8 days, high Ag fluxes and accumulated Ag were observed in tall fescue (Festuca arundinacea) that grew in loam soil with high carbonate content, whereas the lowest Ag uptake was observed in plants grown in clay loam,¹⁸³ probably due to the preferential adsorption of surface-charged AgNPs on the oppositely charged sites of clay minerals.^184,185

The maximum retention capacity (Q_max = 0.38–0.55 mg g⁻¹), the retained amount of AgNPs on soil, was also positively correlated to iron oxide content.¹⁸⁶ For wetland plants, the iron plaque layer formed in the root surface can act as a barrier to inhibit the direct uptake of nanoparticles.¹⁸⁷ Decreasing bioconcentration factors (BCFs) of AgNPs were observed for rice (Oryza sativa L.) with an increasing amount of iron plaque on the root surface.¹⁸⁸ By contrast, another study found that iron plaque oxidized AgNPs into AgCl and Ag⁺-thiol complexes, and thus increased Ag uptake in rice seedlings.¹⁸⁹ Such contrasting effects of iron plaque were ascribed to its influence on the dissolution of AgNPs. The iron plaque generated in the rhizosphere is a mixture of (oxyhdr)oxides, mainly composed of ferrihydrite, goethite, and lepidocrocite.^190,191 Our recent study found that electrostatic attractions between AgNPs and iron oxides (goethite and hematite) led to heteroaggregation of nanoparticles and thus significantly inhibited the dissolution of AgNPs.¹⁹² Despite its effects on dissolution, whether iron plaque can act as a physical barrier to inhibit the direct uptake of AgNPs remains to be answered.

Co-existing heavy metals in natural environments potentially influence the uptake of AgNPs. For instance, Cu pre-exposure (0.5–2.5 mg L⁻¹ for 4 days) reduced AgNP uptake rates by 1.3–3.9 times in wheat seedlings, probably due to the cell death in root tips and the decline of non-protein thiols in roots.¹⁹³ Cao et al. found that the co-exposure of AgNPs (1 mg L⁻¹) and Sb(V) (100 mg L⁻¹) led to significantly higher Ag accumulation in roots, stems and leaves of soybean and speculated that Sb(V) could lead to oxidative dissolution of AgNPs to release more bioavailable Ag⁺.¹⁹⁴ The mutual impacts of AgNPs and heavy metal can be attributed to various physical, chemical and biological processes in the rhizosphere, which ultimately lead to different plant uptakes of both substances.^193–196 In agroecosystems, research efforts have also been focused on the co-exposure of nanomaterials with organic contaminants (e.g., organic pesticides and fertilizers).^197–202 Co-exposure of organic pollutants can affect the uptake of AgNPs in plants. For example, the accumulated Ag in aerial tissues of zucchini (Cucurbita pepo) exposed to AgNPs alone was 85.4% higher than plants co-exposed to AgNPs and imidacloprid, suggesting that the uptake of AgNPs was suppressed by imidacloprid co-exposure.²⁰³ Li et al. found that diclofop-methyl, a common post-emergence herbicide, reduced Ag⁺ release from AgNPs and thus, the Ag content in shoots and roots of Arabidopsis thaliana was reduced by 15.2% and 9.4% with the presence of 1 mg L⁻¹ diclofop-methyl.¹⁹⁸ Therefore, the interaction of AgNPs with coexisting contaminants should be considered for risk assessments in agroecosystems.

In soils, AgNPs will undergo oxidative dissolution and transform into more stable silver complexes such as Ag₂S, which was less bioavailable due to its low solubility.^{29,177,204,205} In flooded soil, most of the Ag was transformed into Ag₂S (>95%) within 2 days, due to the decreasing soil Eh.⁴⁶ Decreased bioavailability of AgNPs with a Ag₂S shell has been demonstrated.^206–208 The silver bioconcentration factor for ryegrass was 0.061 in soil amended with pristine AgNPs, compared to 0.003 in soil with sulfidized AgNPs.⁹⁰ Higher Ag content in roots of rice, lettuce, alfalfa, and wheat has been observed upon exposure to AgNPs than Ag₂S NPs, which can be explained by the stronger dissolution ability and smaller particle size of the used AgNPs.^{188,209–211} However, Niu et al. found that sulfate-reducing bacteria (SRB) transformed AgNPs (20 nm) into Ag₂S NPs with smaller particle sizes (<10 nm), thus leading to higher concentration of silver-containing nanoparticles with smaller size in the roots and stems of Scirpus triqueter.²¹² These results highlighted the bioavailability of Ag₂S at the nanoscale.^89,209,213

Natural organic matter significantly affects the dissolution of nanoparticles.^214–218 For example, the thiol group of NOM was effective in reducing AgNP bioavailability by inhibiting particle dissolution.²¹⁹ A negative relationship was observed between the NOM concentration and AgNP uptake rate for rice (Oryza sativa L.) seedlings: the uptake rate of total Ag decreased from 34.4 to 13.6 mg kg⁻¹ h⁻¹ with increasing NOM concentration from 0 to 79.8 mg L⁻¹.²¹⁹ Additional humic acids (HA) (10–100 mg L⁻¹) inhibited particle dissolution and reduced Ag accumulation in the roots and leaves of duckweed (Lemna minor L.) exposed to 100 mg L⁻¹ AgNPs for 15 days.²²⁰ A recent study found that HA adsorption changed the surface properties of nanoparticles, including the effective size, hydrophobicity, and surface charge.²²¹ NOM may associate with the nanoparticle surfaces, acting as a coating agent to lower the zeta potential of AgNPs, and thus reduce their contact with plant roots via charge repulsion.^220,222 In the aquatic environment, HA can complex with AgNPs via carboxylate groups and C–O and C–O–C bonds.²²⁰ Yang et al. reported that a NOM-corona can be formed on the AgNP surface within 20 minutes, following a two-step (i.e., fast and slow processes) first-order adsorption model.²²³ The adsorption equilibrium constants of HA on bare-, citrate-, and PVP-AgNPs were 0.18 ± 0.01, 0.35 ± 0.03, and 0.80 ± 0.18 L mg⁻¹ C, respectively, implying the high affinity of HA toward AgNPs.²²³ The corona formed by adsorption of diverse biomolecules (e.g., NOM, proteins, and metabolites) on the surface of nanoparticles will influence the retention and plant uptake of AgNPs, as well as other nanoparticles.^224,225 For instance, in sandy soil poor in organic matter, Ce fluxes in fescue (Festuca arundinacea) were ∼2.1 times higher (6.6 ± 0.7 ng m² s⁻¹) following exposure to 1 mg kg⁻¹ citrate-coated CeO₂ NPs compared to those exposed to bare CeO₂ NPs.¹⁵⁴ However, when plants were cultivated in clay soil rich in organic matter, similar phytoavailability of bare and coated CeO₂ NPs was observed, indicating that the potential coating of NOM could change the mobility and phytoavailability of nanoparticles.^{154,226–228} Given that the composition and physicochemical properties of NOM vary greatly as a function of the origin and maturity level of the materials,^215,229 the heterogeneity of NOM makes the assessments that are based on the average characteristics of unfractionated NOM unrepresentative to describe interactions between specific components and nanoparticles.^230,231

Additionally, the eco-coronas formed at the nanoparticle surface have different molecular components because of the incredible diversity of biomolecules in the soil environment.²²⁴ Plant-derived biomolecules (e.g., organic acids, amino acids, and phenolics) in root exudates can also be adsorbed onto particle surfaces to influence the stability of nanoparticles.^232,233 For example, a lower zeta potential (−28.7 ± 0.9 mV vs. −14.3 ± 0.7 mV), decreased metal ion release rate (0.002% h⁻¹vs. 0.016 % h⁻¹), and smaller particle size (146.3 ± 17.9 nm vs. 5919.0 ± 696.5 nm) of Mn₃O₄ NPs were observed in the soybean root exudate medium than in pure water after 5 days of incubation, indicating that the surface charge, dissolution, and aggregation state of NPs were considerably dependent on the constituents of the exposure medium.²³⁴ Given that the constituents of root exudates vary with different plants, long-term root exposure under more realistic field conditions is required to decipher the role of root exudates in the fate of nanoparticles.

Although studies have revealed the impacts of AgNPs on soil and plant-associated microbial communities,^235–242 the role of a diverse array of symbiotic microorganisms (including rhizosphere and phyllosphere microbes) in the transformation and uptake of AgNPs in plants is largely unknown. Studies revealed that arbuscular mycorrhizal fungi, which form a symbiotic relationship with over 90% of terrestrial plants, could alleviate AgNP stress (via increased growth and nutrient uptake, etc.) and thus decrease Ag uptake and accumulation in plants.^243–245 Noori et al. found that tomatoes inoculated with mycorrhizal fungi (Rhizophagus intraradices) accumulated 14% less Ag compared to non-mycorrhizal tomatoes upon exposure to 36 mg kg⁻¹ of 2 nm AgNPs for 2 weeks, and suggested that mycorrhizal colonization could decrease Ag accumulation via downregulating the expression level of membrane transport proteins.²⁴⁶ The mutual interactions between mycorrhizal fungi and AgNPs are complex because of the large variation in plant and fungal species, as well as the changeable environmental factors.²⁴⁷ Besides, little is known about whether phyllosphere microbial communities (as well as their metabolites) could affect the foliar uptake of AgNPs. Thus, more research is needed to understand how microbes influence nanoparticle uptake in plants in a typical plant–soil system.

3.3.3 Uptake variation between plant species. Different uptakes of AgNPs were observed in a variety of plant species.^36,248,249 The AgNP uptake rates of 15-day wheat (Triticum aestivum L.) seedlings increased from 8.0 to 39.0 mg kg⁻¹ h⁻¹ upon hydroponic exposure to 2 to 30 mg L⁻¹ AgNPs.¹²³ Compared with wheat, 15-day rice (Oryza sativa L.) seedlings had a higher total Ag uptake rate (34.4 mg kg⁻¹ h⁻¹) even at a lower exposure dosage (1 mg L⁻¹ AgNPs).²¹⁹ The Ag contents in wheat roots were several times higher than those in sunflower roots, suggesting different AgNP uptake potential between monocotyledon and dicotyledon.²⁵⁰ The uptake rate constant of AgNPs of algae (Chlorella vulgaris) (0.233 ± 0.024 L g⁻¹ d⁻¹)¹³⁸ was higher than of wheat (1.1 ± 0.1 L kg⁻¹ h⁻¹),¹²³ indicating lower AgNP phytoavailability for higher plants. The uptake of other nanoparticles (e.g., CeO₂) in plants was also suggested to be species dependent.²⁵¹ For a given plant, plant age has a minor influence on the uptake of AgNPs because the overall uptake rate constants of 15- and 30-day wheat seedlings were similar (4.3 ± 0.6 L kg⁻¹ h⁻¹vs. 5.2 ± 0.6 L kg⁻¹ h⁻¹),¹²⁶ but a long-term experiment is required to quantify the uptake at different life stages.

The root surface area and number of lateral roots affect the sensitivity of plants to nanoparticles.^187,252 Differences in leaf surface properties (e.g., leaf area, size of stomata, and cuticle thickness) give plants different capacities to take up nanoparticles.^92,119,253 These morphological and physiological features are modulated by environmental factors and will change at different growth stages, which consequently change the nanoparticle uptake ability of plants. Many studies were carried out at the initial stage of plant growth, which cannot represent the real behavior of AgNPs in the full life cycle and may exaggerate the adverse effects of AgNPs. In addition, experiments were usually done with small annual plants, such as Arabidopsis, lettuce, rice, wheat, tomato, etc.^{107,123,211,254,255} The different anatomical features of plant species may result in diverse uptake and translocation patterns. For example, after 48 h of hydroponic exposure to 50 mg Ce per L as CeO₂ NPs, Ce existed throughout the leaf of dicot plants (tomato and lettuce) but was mainly located in the vasculature of monocot plants (corn and rice), probably due to the larger airspace volume in dicot leaves.¹⁶³ The anatomical structure of plant tissues as well as the metabolic processes will change under biotic and abiotic stimuli or stresses (e.g., plant diseases and insect pests, flooding, drought, soil salinity and extreme temperatures),^256–258 and thus affect the uptake of nanoparticles. Rossi et al. found that the cerium concentration in leaves of Brassica napus L. was 150% higher in salt stressed (100 mM NaCl) plants than unstressed plants upon exposure to 200 mg kg⁻¹ CeO₂ NPs, although the mechanism is unclear.²⁵⁹ Therefore, field trials evaluating the responsive AgNP uptake behaviors of plants under more climatically relevant conditions are needed.¹

Studies have observed the toxic effects of AgNPs on plants, such as inhibiting seed germination, reducing biomass, and decreasing transpiration rates (Table 1), and have revealed the underlying mechanisms of AgNP phytotoxicity, including oxidative stress, cytotoxicity and antioxidative responses.^260–262 Omics-based approaches offer new opportunities to investigate the molecular mechanisms of nanoecotoxicology, and have succeeded in identifying certain responses that point to potential toxicity pathways and to action modes of nanoparticles.^263–265 Recently, Huang et al. observed 21 dysregulated metabolites in corn leaves and 53 in wheat leaves after 3 weeks of root exposure to 200 and 1000 mg MoO₃ NPs per kg vermiculite, and demonstrated the value of metabolomics in studying early-stage plant responses to nanoparticle exposure.²⁶⁶ Thus, using multi-omics techniques, a thorough understanding of plant responses to AgNP exposure can also be achieved to optimize both functionality and safety in AgNP application.

4. Translocation and accumulation of AgNPs in plants

Nanoparticles internalized by roots or leaves can be transferred from the exposed surfaces to the vascular system through the apoplastic or symplastic pathway. AgNPs were observed in epidermal cells,²⁵² columella cells,²¹⁰ or meristem cells in roots,¹²³ typically in the cell wall,^{33,107,267,268} which serves as a barrier between particles and the protoplast. After crossing the pores of the cell wall, AgNPs can move into the intercellular space between the cell wall and plasma membrane through the apoplastic pathway,^269,270 verified by the existence of AgNPs in the middle lamella (i.e., intercellular layer).^{125,189,268,271} After passing through the epidermis and the cortex via the apoplastic pathway, nanoparticles will be blocked by the Casparian strip, a special structure in the endodermis, but some can penetrate the plasma membrane and enter the cytoplasm of endodermal cells via the symplastic pathway.^272–274 Once inside the cells, AgNPs can be transported symplastically through plasmodesmata,^107,123 the narrow strands of cytoplasm with 30–50 nm in diameter that penetrate cell walls to interconnect adjacent cells.^275–278 The direct cell-to-cell transport through the symplastic pathway can deliver AgNPs to the vascular bundles, the main transportation system throughout the whole plant.^107,279,280 In the vascular bundles, AgNPs could be transported upward (from roots to stems or leaves) through the xylem or downward (from leaves to roots) through the phloem.^281,282 The perforation plate of the vessel and sieve plate of the sieve tube play a crucial role in the translocation of nanoparticles as they inhibited the transportation of most PVP-AgNPs and citrate-AgNPs but not GA-AgNPs.⁹¹

Translocation factors (TF_shoot/root, calculated as the ratio of Ag level in shoots to that in roots) differed with particle properties and plant species (Table 1). Small Ag particles tended to transfer upward more feasibly (TF_shoot/root = 0.75 ± 0.06 for small particles (20 nm) vs. 0.06 ± 0.007 for bulk Ag) in tomato that were exposed to 10 mg L⁻¹ Ag for 7 days.²⁸³ Souza et al. also found that the smallest AgNPs (30 nm), rather than larger AgNPs (85 and 110 nm), could translocate from roots to leaves of Lemna minor.¹⁵⁰ The translocation of nanoparticles in plants is also partially governed by their surface properties such as surface charge. For example, several studies have reported that negatively charged nanoparticles had higher TF_shoot/root, indicating that these nanoparticles are more advantageous to transport from roots to shoots.^{163,164,284,285} The TF values in cucumber (Cucumis sativus) exposed to the polyacrylic acid-CeO₂ NP (negative charged) group were significantly higher than those exposed to the chitosan-CeO₂ NP (positive charged) group at equivalent dosage (50, 200, and 1000 mg L⁻¹) for 14 days.²⁸⁶ Silver content in citrus leaves ranked the highest with branch feeding GA-AgNPs (71.48 ± 108.81 μg kg⁻¹) compared with PVP-AgNPs (58.71 ± 69.15 μg kg⁻¹) and citrate-AgNPs (34.48 ± 27.05 μg kg⁻¹), which indicates that GA coating may enable high transport efficiency for nanoparticles.⁹¹ The translocation of AgNPs within plants is also modulated by the internal environment of plants.^143,189,287 Generally, the TF_shoot/root of total Ag is less than 0.05 in most plants such as wheat (0.013–0.038),^34,209,287 soybean (0.017–0.05),^34,194 rice (0.001–0.012),^188,189 and lettuce (0.009–0.037)^124,255 (Table 1). The internalized AgNPs were found to be hard to transport in some plant species. For example, less than 1% of AgNPs were transferred from alfalfa (Medicago sativa) roots to shoots after 6-day root exposure.²¹⁰ Galazzi et al. found that about 82.5% and 17.2% Ag were maintained in roots and stems while only 0.2% was transferred to leaves of soybean (Glycine max) after exposure to 50 mg kg⁻¹ AgNPs for 14 days.²⁸⁸ Fernandes et al. observed Ag accumulation mainly in belowground tissues of a salt marsh plant, Phragmites (Phragmites australis), after exposure to 10 mg L⁻¹ AgNPs for 7 days.²⁴² On the contrary, high TF_shoot/root values of particulate Ag (0.38–0.62) were observed in tomato exposed to 10–30 mg L⁻¹ AgNPs for 7 days.²⁸³ For ligneous plants, such as downy oak (Quercus pubescens Willd.), scots pine (Pinus sylvestris L.) and black poplar (Populus nigra L.), more than 50% of the total Ag was accumulated in the stem when exposed to foliar treatment.²⁸¹ It should be mentioned that, due to the limitation of analytical methods, the TF_shoot/root values calculated in most studies were based on the concentrations of total Ag instead of those of AgNPs, which may deviate from the actual translocation of nanoparticles inside plants.

Multi-scale techniques are integrated to trace the distribution and translocation of nanoparticles in plants, such as autoradiography,²⁸⁹ γ-spectrometry,²⁸⁹ surface-enhanced Raman spectroscopy,^290,291 laser ablation-single particle-inductively coupled plasma mass spectrometry,²⁹² and synchrotron-based techniques.²⁰⁹ The knowledge on the tissues where AgNPs accumulated is crucial to evaluate the possibility of these nanoparticles to enter food chains. However, few studies have investigated the accumulation of AgNPs in edible parts of plants (e.g., grains and fruits). Although the accessibility of these analytical platforms maybe limited, much work is still required involving the dynamic uptake and translocation of nanoparticles in plants over the life cycle (particularly the maturation stage).

5. Transformation of AgNPs in plants

Within plants, AgNPs will undergo physical or chemical transformation such as aggregation, oxidative dissolution, chlorination, sulfidation and complexation with organic ligands (Fig. 3). Studies have reported that internalized AgNPs aggregated into larger nanoparticles in different plants, including soybean,³³ rice,¹⁸⁸ wheat,¹²³ lettuce,²⁹³ tomato,²⁸³ and Arabidopsis,²⁶⁸ while others found that AgNPs were subjected to a range of biochemical reactions, leading to the accumulation of transformed products (Table 2).

Fig. 3 Schematic diagram of the possible transformation of AgNPs in plants.

Table 2 Summary of studies on transformation mechanisms of AgNPs and observed metal species in plants

Nanoparticles	Plant species	Exposure pathway	Qualitative analysis techniques	Analyzed samples	Transformation	Main transformed products	Ref.
PVP-AgNPs	Rice (Oryza sativa L.)	Root	sp-ICP-MS	Leaves	Aggregation	AgNPs with larger size (18.6 nm vs. 41.5 nm)	33
PVP-AgNPs	Soybean (Glycine max)	Root	sp-ICP-MS	Leaves	Aggregation	AgNPs with larger size (18.6 nm vs. 30.2 nm)	33
Uncoated AgNPs	Lettuce (Lactuca sativa L.)	Foliar	μXRF	Leaves	Aggregation	Ag agglomerates (38.6 nm vs. 2–3 μm on the leaf surface)	37
PVP-AgNPs	Wheat (Triticum aestivum L.)	Root	sp-ICP-MS	Roots	Aggregation	AgNPs with larger size (15.6 nm vs. 32.9 nm)	123
PVP-AgNPs	Wheat (Triticum aestivum L.)	Root	sp-ICP-MS	Roots, shoots	Aggregation	AgNPs with larger size (13.4 nm vs. 29.1 nm (roots), 34.3 nm (shoots))	126
PVP-AgNPs	Rice (Oryza sativa L.)	Root	sp-ICP-MS	Roots, shoots	Aggregation	AgNPs with larger size (12.2 nm vs. 24.9 nm (roots), 27.8 nm (shoots))	188
Citrate-AgNPs	Arabidopsis (Arabidopsis thaliana)	Root	sp-ICP-MS	Roots	Aggregation	AgNPs with larger size (12.8 nm vs. 20.7 nm)	268
PVP-AgNPs	Tomato (Lycopersicon esculentum)	Root	sp-ICP-MS	Roots, stems, leaves	Aggregation	AgNPs with larger size (20 nm vs. 41 nm (roots), 30 nm (stems), 25 nm (leaves))	283
PVP-AgNPs	Lettuce (Lactuca sativa L.)	Foliar, root	sp-ICP-MS	Leaves	Aggregation	AgNPs with larger size (16.5 nm vs. 27.6–32.5 nm (foliar exposure), 29.8–36.5 nm (root exposure))	293
PVP-AgNPs	Rice (Oryza sativa L.)	Foliar	TEM-EDS	Leaves	Oxidative dissolution, chlorination	AgCl NPs (33.0–48.9 nm)	33
Uncoated AgNPs	Lettuce (Lactuca sativa L.)	Foliar	μ-XANES	Leaves	Oxidative dissolution, chlorination, complexation with organics	Epidermis: Ag–glutathione (31–85%), AgCl	37
						Parenchyma: Ag–glutathione (100%)
PVP-AgNPs	Rice (Oryza sativa L.)	Root	LC-ICP-MS	Shoots	Oxidative dissolution	Ag^+	125
PVP-AgNPs	Rice (Oryza sativa L.)	Root	XANES	Roots	Oxidative dissolution, chlorination, sulfidation, complexation with organics	Ag2S (22.1%), Ag^+–cysteine (9.4%), AgCl (39.8%)	189
AgNPs	Cowpea (Vigna unguiculata L.)	Root	XANES	Roots, stems, leaves	Oxidative dissolution, complexation with organics	Roots: Ag–glutathione (48%), Ag-histidine (21%)	209
						Stems: Ag–glutathione (13%)
						Leaves: Ag–glutathione (50–73%)
AgNPs	Wheat (Triticum aestivum L.)	Root	XANES	Roots, shoots	Oxidative dissolution, complexation with organics	Roots: Ag–glutathione (65%), Ag-histidine (4%)	209
						Shoots: Ag–glutathione (72%), Ag-histidine (6%)
PVP-AgNPs	Wheat (Triticum aestivum L.)	Root	μ-XANES	Roots	Oxidative dissolution, complexation with organics	Cell wall of the endodermis: Ag–thiols (77%), other Ag ionic species (26%)	252
						Cell wall of the cortex: Ag–thiols (86%), other Ag ionic species (14%)
PVP-AgNPs	Duckweed (Landoltia punctata)	Foliar, root	EXAFS	Roots	Oxidative dissolution, sulfidation, complexation with organics	Ag2S (64%), Ag–thiols (53%)	294
PVP-AgNPs	Green algae (Chlamydomonas reinhardtii)	Cell	XANES, EXAFS	Cytoplasm	Oxidative dissolution, sulfidation, complexation with organics	Ag2S (34%), Ag–thiols (51%)	295
AgNPs	Common bean (Phaseolus vulgaris)	Seed	μ-XANES	Seed coat	Oxidative dissolution, complexation with organics	Ag–thiols	296

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5.1 Silver species in plants

Using multiple advanced analytical techniques (e.g., XAS), researchers are able to trace the ultimate transformation products of internalized metallic NPs. Several Ag species including Ag₂O,³⁸ AgCl,^33,37,189 Ag₂S,^189,294,295 and Ag-thiolate complexes^{37,189,209,252,294–296} were observed within plants. The presence of Ag(I) indicates the oxidative dissolution of AgNPs. Dissolved oxygen produced by photosynthesis and reactive oxygen species (ROS) generated from oxidative stress may increase the redox levels in plant tissues and oxidize the surface silver of AgNPs into Ag₂O (Ag–O– speciation), and finally lead to the release of Ag⁺.^40,297 The effects of other redox-active substances on the oxidative dissolution of AgNPs have not yet been explored in planta. Besides, endogenous organic acids and thiol-containing proteins (e.g., cysteine) inside plants can promote the dissolution of AgNPs.²⁹⁸

Organic thiols, as strongly binding ligands for Ag⁺ (K_f ≈ 10¹³),²⁹⁹ will combine with the dissolved Ag to form Ag-thiol complexes. Secondary nanoparticles including AgCl-NPs and Ag₂S were also observed, which were considered as stable detoxification products stored in plants.^33,37 For instance, the majority of AgNPs primarily transformed into Ag₂S and Ag-thiol complexes in duckweed (Landoltia punctata) tissues.²⁹⁴ In rice roots, the content of Ag₂S, Ag-thiols, and AgCl counted for >71% of total Ag.¹⁸⁹

Moreover, in vivo reduction of Ag⁺ into metallic Ag nanoparticles is also feasible due to the existence of reducing substances (e.g., polysaccharides, components of the plant cell wall as well as products of photosynthesis)³⁰⁰ and antioxidant compounds in plants.^301–303

5.2 Concerns and challenges in investigating AgNP transformation in plants

Remarkably, although different Ag species originating from AgNPs have been determined in plants, the transformation remains a complicated process with many scientific challenges that need to be addressed.

(1) A basic but less noticed criterion for studying nanoparticle biotransformation inside plants is to exclude the interference of ionic species produced from nanoparticle dissolution in the culture medium or at the nano-plant surface. Whether the secondary metal species are derived from directly absorbed nanoparticles or ions remains unclear due to the lack of suitable methodology to monitor the dynamics of Ag species at environmentally relevant concentrations. Besides, the newly formed metallic nanoparticles during the in vivo reduction of Ag⁺ also bring confusion when investigating the translocation patterns of nanoparticles.

(2) Diverse transformed products observed in plant tissues indicate that the transformation processes are influenced by multiple factors, including the properties of particles and the internal environments, which have been rarely investigated.³⁰⁴ Surface coatings of AgNPs influence their affinity to organic compounds with redox properties that are ubiquitous in plants.^{119,286,305,306} The secretion of root cells and constituents of sap inside vascular bundles may lead to aggregation, dissolution, and biomolecule corona coating for AgNPs.⁹¹ These properties are influenced by plant species, stage of plant growth, and environmental factors.⁹¹ It remains unclear how the complex internal environment of plants impacts the transformation of AgNPs. In vitro simulation experiments can be an effective approach to investigate the possible transformation of nanoparticles in plants.

(3) It remains unclear where the transformation of AgNPs takes place. The transformation of AgNPs could occur in the root epidermis with abundant organic acids as well as vascular bundles that contain organic compounds and inorganic salts.²⁵² In AgNP-exposed wheat roots, Ag was mostly present as metallic Ag in the epidermis.²⁵² However, 86% and 14% of Ag was present as Ag-thiols and other ionic Ag species in the cell wall of the cortex and the proportion of these two types of Ag changed to 77% and 26% in the cell wall of the endodermis.²⁵² Another study found that AgNPs can penetrate the seed coats and undergo oxidative dissolution to form Ag-thiolate complexes in parenchyma cells of common bean (Phaseolus vulgaris), probably because of the intrinsic differences in the organic composition and structure between the external and internal layer of the seed coat.²⁹⁶

Due to the lack of methodologies to identify nanoparticles at a subcellular level, less is known about the transformation within plant organelles (e.g., chloroplasts and mitochondria).^304,307 In animal cells, lysosomes, the organelles responsible for sequestration of intracellular metal (in both ionic and nanoparticulate forms), may regulate the dissolution of AgNPs.^35,307 For example, AgNPs were accumulated in lysosomes of zebrafish cells and then dissolved to release Ag⁺ because of an acidic microenvironment in lysosomes (pH ≈ 4.5).³⁰⁸ In plant cells, dissolution of nanoparticles may also happen in lytic vacuoles containing hydrolytic enzymes, which is far from being understood. Wang et al. found that Ag₂S was formed inside the cytoplasm of algae but no sulfidation of AgNPs occurred outside the cytoplasm, suggesting the presence of sulfidation in the cytoplasm.²⁹⁵ Dai et al. identified the transformation products of CuO NPs in plant cells (Nicotiana tabacum) and found that reduction and sulfidation firstly occurred in the cell wall and then intracellularly in the protoplast and mitochondria.³⁰⁹ Although transformed Ag species have been observed in different plant tissues, the dynamic transformation of AgNPs during transportation in the whole plants, particularly inside plant cells, is not well understood.

(4) It is noteworthy that the transformed Ag species have different toxicities.^209,249 The observed adverse impacts in plants may be ascribed to the transformed products in some cases, although oxidation of AgNPs and formation of other Ag species are deemed to be the detoxification processes to reduce particle stress.³⁰⁴ Various biotransformation products generated in different plant tissues may lead to dynamic and multiple exposures, which should be further evaluated. In addition, the translocation pattern of metal inside plants may change, due to the difference in translocation ability of transformed products.³⁰⁹ The translocation factors of Ag₂S-NPs were lower than those of AgNPs in wheat,^209,252 but were higher than those of AgNPs in rice.¹⁸⁸ Our group found that Ag₂S-NPs were translocated upward to soybean leaves via root exposure and the accumulated Ag₂S-NPs in leaves were assimilated by snails, indicating the considerable trophic availability of Ag₂S-NPs.³² In view of the complicated transformation in plants, the question remains whether internalized AgNPs or the transformed products will be transferred to edible portions of mature plants, such as fruits and grains.

(5) An increasing number of studies in vitro have found that biomolecules (proteins, lipids, etc.) were ready to form a corona on the surface of AgNPs,^310–313 which has not been observed in plants. The corona changes the particle surface properties and has an appreciable impact on the aggregation, dissolution, and biochemical transformation of AgNPs, which has been described in non-plant systems (for example, marine waters and gastrointestinal fluids) elsewhere.^314–318 For instance, Miclăuş et al. found that the protein corona could modulate the chemical transformation of AgNPs.²⁹⁷ The strongly attached protein prevents the diffusion of released Ag⁺ and acts as a site for sulfidation at the surface of AgNPs. On the contrary, the weakly attached proteins transport Ag⁺ away from the particle surface and thus reduce the formation of Ag₂S-NPs.²⁹⁷ As for plants, the abundant proteins, lipids, and carbohydrates in phloem may allow the corona to form around AgNPs.^92,105,119 Borgatta et al. observed that a 5.1 ± 0.2 nm thick corona, composed primarily of proteins, was formed around the CuO NPs (50 mg L⁻¹) that were incubated in pumpkin xylem fluid for 3 h.³¹⁹ Kurepa et al. observed the bio-corona formed on TiO₂ NPs in Arabidopsis thaliana leaf and the layer was enriched with metabolites such as flavonoids and lipids.³²⁰ Bing et al. reported that the tested plant proteins (i.e., glutenin, gliadin, zein, and soy protein) could form 4–60 nm thick coronas on the TiO₂ NP surface and thus changed the surface potential and morphology of the particles.³²¹ The composition and properties of coronas formed in leaves, vascular systems and root tissues are different due to the complex biological matrices inside a wide range of plant species.³²² The effects of the corona on the translocation and biotransformation of AgNPs in planta remain to be understood. Sufficient proteomic and metabolomic information of plants, integration of multi-scale analytical techniques, and development of computational analyses are required to predict the possible transformation of nanoparticles in planta and such advances will enable further study of biological effects of nanoparticles on plants.^322,323

6. Transfer of AgNPs in food chains and risk of dietary intake for humans

Nanoparticles taken up by plants can be transferred to primary consumers via food chains.^324–326 For instance, ryegrass (Lolium perenne) can accumulate up to 0.2 mg kg⁻¹ Ag after growing in AgNP amended soil for 3 weeks and the internalized Ag can be transferred to a primary consumer, snail (Cantareus aspersus).⁹⁰ AgNPs existed in all aquatic organisms in Taihu Lake of China and the biomagnification of AgNPs with a trophic magnification factor (TMF) of 1.21 was found, proving the trophic transfer of AgNPs in natural aquatic food webs.³²⁷ Thus, trophic transfer of AgNPs exists in aquatic and terrestrial systems and acts as a potential pathway of AgNP exposure for organisms at different trophic levels.^31,328–330

Parent-progeny transfer of nanoparticles is possible because the internalized nanoparticles via root uptake were detected in the harvested seeds.^331,332 The existence of Ag in edible parts (e.g., grains and fruits) leads to the potential risk to food chains.^39,197,333 The total Ag content was found to be highest in dry fruits, nuts, and seeds, (734 ng kg⁻¹), followed by cereals and cereal products (375 ng kg⁻¹) and potatoes (292 ng kg⁻¹), and the estimated dietary daily intake of Ag was 0.013 μg kg⁻¹ body weight per day.³³⁴ It is worth noting that the safety standard of maximum Ag levels in vegetables, fruits, grains, or other agricultural products is still lacking. The accumulation of engineered nanoparticles in plant tissues has raised the concern about the potential chronic exposure of terrestrial animals and humans to them through food chains.

7. Conclusions and perspectives

The application of engineered nanomaterials in consumer products has increased the concern about their potential risk to the ecosystem and human health. In addition to anthropogenic input, the natural generation of AgNPs in the environment, especially in the root zone, also makes them more accessible to plants. Studies on the ecological risk of AgNPs have revealed the potential transformation of nanoparticles in complex aquatic or terrestrial environments as well as particle-specific toxicity to living organisms through direct contact, but the trophic transfer of nanoparticles after uptake in plants is seldom investigated.

An increasing number of studies have found that multiple factors were governing the plant uptake of AgNPs, including particle properties (e.g., size and surface charge), soil components (e.g., clay, carbonates, iron oxides, NOM, and symbiotic microorganisms) and plant species. A better understanding of AgNPs uptake kinetics in plants will help to predict more accurately the dynamic accumulation of Ag in plants. However, given the shortcomings of the current studies (e.g., short-time exposure and immature plants), long-term exposure experiments, combined with uptake kinetics investigation, are required to verify the role of these factors in natural scenarios.

Internalized AgNPs have been observed in leaves and stems after root exposure, suggesting that AgNPs can be transferred inside plants through the vascular system. However, whether Ag could accumulate in seeds and fruits in the form of nanoparticles is currently unknown due to the lack of investigation. Moreover, the transformed products of AgNPs (e.g., AgCl, Ag₂S, and Ag-thiols) may also change the translocation and accumulation of Ag in plants. Although these Ag species have been observed inside plants, little is known about the actual elemental component, content, and morphology of the transformed products. Questions about which factors affect the transformation, where the transformation takes place, and whether these transformed products are accumulated in edible tissues remain to be answered. Given that the transformed products formed at different plant tissues may be variant, the discrimination of Ag species in edible parts is essential to evaluate the risk of Ag entering the food chain.

A combination of innovative qualitative and quantitative techniques, computational simulations, and conceptual models is helpful to deliver in-depth details on the fate of AgNPs inside plants and to reveal the complex mechanisms of nanoparticle-plant interaction. To date, methods to investigate the uptake, translocation, and accumulation of AgNPs (as well as other NPs) inside plants are still limited. As the applications of nanoparticles continue to develop, a comprehensive understanding of the uptake and in planta fate of AgNPs is needed to predict the bioavailability of Ag and its potential to enter food chains, which helps to evaluate risks to wildlife and human health.

Author contributions

All the authors have contributed to the discussion and the writing of this manuscript.

Conflicts of interest

There are no conflicts of interest to declare.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (41430752 and 41771526). We thank the anonymous reviewers for their comments and suggestion on this manuscript.

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