Influence of Surface Charge on the Phytotoxicity, Transformation, and

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Influence of Surface Charge on the Phytotoxicity, Transformation and Translocation of CeO2 Nanoparticles in Cucumber Plants Mengyao Liu, Sheng Feng, Yuhui Ma, Changjian Xie, Xiao He, Yayun Ding, Junzhe Zhang, Wenhe Luo, Lirong Zheng, Dongliang Chen, Fang Yang, Zhifang Chai, Yuliang Zhao, and Zhiyong Zhang ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.9b01627 • Publication Date (Web): 17 Apr 2019 Downloaded from http://pubs.acs.org on April 17, 2019

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ACS Applied Materials & Interfaces

Influence of Surface Charge on the Phytotoxicity, Transformation and Translocation of CeO2 Nanoparticles in Cucumber Plants Mengyao Liu,a,1 Sheng Feng,a,1 Yuhui Ma,b,* Changjian Xie,b Xiao He,b Yayun Ding,b Junzhe Zhang,b Wenhe Luo,b Lirong Zheng,c Dongliang Chen,c Fang Yang,a,* Zhifang Chai,b Yuliang Zhao,b Zhiyong Zhang,b, d, * a

Hebei Provincial Key Lab of Green Chemical Technology & High Efficient Energy

Saving, School of Chemical Engineering and Technology, Hebei University of Technology, Tianjin 300130, China b

Key Laboratory for Biomedical Effects of Nanomaterials and Nanosafety, Institute

of High Energy Physics, Chinese Academy of Sciences, Beijing 100049, China. c

Beijing Synchrotron Radiation Facility, Institute of High Energy Physics, Chinese

Academy of Sciences, Beijing 100049, China. d

School of Physical Sciences, University of the Chinese Academy of Sciences,

Beijing 100049, China. * Corresponding authors. E-mail address: [email protected]; [email protected]; [email protected] Tel: +86-10-88233215; Fax: +86-10-88235294 1

The two authors contributed equally to this article.

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ABSTRACT The physiochemical properties of nanoparticles (NPs), including surface charge, will affect their uptake, transformation, translocation, and final fate in the environment. In this study, we compared the phytoxoxicity and transport behaviors of nano-CeO2 (nCeO2) functionalized with positively charged (Cs-nCeO2) and negatively charged (PAA-nCeO2) coatings. Cucumber seedlings were hydroponically exposed to 0~1000 mg/L of Cs-nCeO2 and PAA-nCeO2 for 14 days and the contents, distribution, translocation and transformation of Ce in plants were analyzed using inductively coupled plasma mass spectrometry (ICP-MS), micro X-ray fluorescence (μ-XRF), and X-ray absorption near-edge spectroscopy (XANES), respectively. Results showed that the seedling growth and Ce contents in plant tissues were as functions of exposure concentrations and surface charge. Cs-nCeO2 were adsorbed strongly on negatively charged root surface, which led to significantly higher Ce contents in the roots and lower translocation factors (TFs) of Ce from the roots to shoots in Cs-nCeO2 group than in PAA-nCeO2 group. The results of μ-XRF showed that Ce elements were mainly accumulated at the root tips and lateral roots, as well as in the veins and at the edge of leaves. XANES results revealed that the proportion of Ce(III) was comparable in the plant tissues of the two groups. We speculated that Cs-nCeO2 and PAA-nCeO2 were partially dissolved under the effect of root exudates, releasing Ce3+ ions as a result. Then the Ce3+ ions were transported upwards in the form of Ce(III)-complexes along the vascular bundles and eventually accumulated in the veins. The other portion of Cs-nCeO2 and PAA-nCeO2 entered the roots through the gap of Casparian strip at root tips/lateral roots and transported upwards as intact NPs, and finally accumulated at the edge of the blade. This study will greatly advance our information on how the properties of NPs influence their phytotoxicity, uptake and subsequent trophic transfer in terrestrial food webs. Key words: nCeO2, surface charge, cucumber, phytotoxicity, transformation, translocation.


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1. INTRODUCTION Cerium (Ce), with a rich electronic energy level structure, is one of the rare earth elements, showing unique physical and chemical properties.1 Cerium oxide (CeO2) is a kind of common rare earth oxide, and at its nanoscale, the oxygen vacancy will exist on the surface of CeO2. In order to stabilize the oxygen vacancy, part of Ce(IV) in CeO2 will be reduced to Ce(III). Nano-CeO2 (nCeO2) has a reversible transition between Ce(III)/(IV), making them attractive candidates for many applications, such as catalysts, solid-state fuel cells, UV-blockers, pharmaceutical field, etc.2-6 With the manufacture and applications, nCeO2 will enter the atmosphere, soil and water from various sources, and interact with environmental species.7,8 Plants are basic components of the entire ecosystem and play an essential role in the fate and transport of NPs in the environment.9 The released nCeO2 will be taken up and accumulated by plants, which might not only affect the growth of plants but also pose a potential risk to food safety.10-12 There have been a lot of studies on the effects of bare nCeO2 on various plant species at the physiological, biochemical and genetic levels.13-16 For example, López-Morenoetal et al. found that nCeO2 could promote the root growth of maize and cucumber, but inhibit the growth of alfalfa and tomato.17 Hong et al. indicated that the activities of antioxidant enzymes (CAT, APX and DHAR) were changed by foliar spray treatment of nCeO2.18 They also pointed out that these changes were one of the reasons for the toxicity of nCeO2 to plants. López-Moreno et al. demonstrated that the DNA integrity of soybean plants was affected by nCeO2, implying their genotoxicity.19 The uptake, translocation and transformation of nCeO2 in plants play critical roles in determining their phytotoxicity and further their fate in the environment. Owing to the development of specialized analytical techniques, such as X-ray absorption near edge structure spectroscopy (XANES), X-ray fluorescence mapping (XRF), and soft X-ray scanning transmission X-ray microscopy (STXM), which are very powerful for analyzing coordination chemistry and mapping of



elements in micron resolution, the distribution and transformation of nCeO2 in plants have been comprehensively studied.20-22 By using STXM-NEXAFS, Zhang et al. investigated the uptake and transformation of CeO2 NPs in hydroponic cucumber plants. They found that Ce existed in the form of CeO2 and CePO4 in the roots, while in the form of CeO2 and carboxylic acid-Ce in the shoots.23 Recently, Ma et al. suggested that the transformation of CeO2 NPs occurred in the root epidermis, which might be caused by the interaction between the root exudates and NPs.24 Although the knowledge about the uptake and transformation mechanisms of nCeO2 in plants has been advanced, the studies were concerned only with the bare nCeO2 and their stability in the culture medium was not considered. When released in the environment, NPs are likely to interaction with natural substances and obtain ultimately a coating with different properties from the original ones. It is well known that surface chemistry of NPs plays a key role in the determination of their phytotoxicity and fate in plants. However, there are very few studies focused on the influence of surface coating on the behaviors of nCeO2 in plants. Several studies compared the effects of uncoated and coated (with alginate or citric acid) CeO2 NPs on crop plants.25,26 Recently, Spielman-Sun et al. synthesized CeO2 NPs with positive/neutral/negative coatings and investigated their uptake, transformation, and translocation in wheat.27 In another study, Li et al. elucidated the subcellular distribution and translocation of the same functionalized CeO2 NPs in tomato plants.28 The impacts of surface charge on the phytotoxicity, uptake and translocation of nCeO2 in plants deserve more investigations with different coating materials and different plant species. In this study, we designed nCeO2 with different surface functional groups and aimed to understand how the surface charge impacts the phytotoxicity, uptake, speciation, and translocation of nCeO2 in a model organism cucumber (Cucumis sativus). The phytotoxicity and oxidative stress induced by the two functionalized nCeO2 were assessed using biomass and H2O2 contents, respectively. The Ce contents


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and translocation in plants were determined using inductively coupled plasma-mass spectrometry (ICP-MS). The distribution and transformation of functionalized nCeO2 in plant tissues were examined by transmission electron microscopy (TEM), XRF, and XANES. This study can provide information on how to control the transport of NPs to specific target parts of plants through functional design, which may help to assess ecological risks and develop agricultural applications.

2. MATERIALS AND METHODS 2.1 Synthesis and Characterization of modified CeO2 NPs Uncoated nCeO2 with a nominal 7 nm primary particle size were synthesized using a precipitation method described previously.29 Then the nCeO2 was functionalized with chitosan (Cs) to confer either a net positive charge (Cs-nCeO2(+)), or with polyacrylic acid (PAA) to confer a net negative charge (PAA-nCeO2(-)) (Figure 1). Cs-nCeO2 was prepared using a modified procedure described by Liu et al.30 Briefly, 2000 mg chitosan was added to 200 ml acetic acid (HAc, 2%) and stirred until completely dissolved (at 50℃ in a water bath). A suspension of nCeO2 (2.5 mg/mL, 400 mL) was mixed with the chitosan solution and stirred at 50℃. Then 12 ml of glutaraldehyde (Ge, 50%) was slowly added to the mixture until the color of the solution changed from white to brown. After about 2 h, the reaction was stopped and the precipitate after centrifugation was washed for 3 times with deionized water. PAA-nCeO2 was obtained by mixing a nCeO2 suspension (50 mL, 5 mg/mL) and a PAA solution (10 ml, 2.5%) and stirring for 3 h. After the reaction, the products were collected by centrifugation and washed for 3 times with deionized water.



Figure 1. Synthesis diagram of nCeO2 with different surface charges

The morphology of Cs-nCeO2 and PAA-nCeO2 was characterized by TEM (Tecnai F30, FEI, Japan). X-ray diffraction (XRD) analysis was performed using X-ray diffractometer analyzer (D8 Advance, Bruker, Germany) with Cu K radiation and a step size of 0.02°. Fourier transform infrared (FT-IR) spectra were recorded on an infrared spectrometer (Vector2, Bruker, Germany). Hydrodynamic diameter and zeta-potential of the nCeO2 and modified nCeO2 in ultrapure water and nutrient solutions (1/4-strength Hoagland’s solution) were respectively determined by dynamic light scattering (DLS, ZetaSizer, Malvern Instruments, UK). The amount of Cs or PAA on the surface of nCeO2 was determined by thermogravimetric analysis (TGA). The dissolution of Cs-nCeO2 and PAA-nCeO2 (1000 mg/L) in 1/4 strength Hoagland’s solution for 14 d was conducted and measured following the procedure in our previous study.31 2.2 Plant Growth Cucumber (Cucumis sativus) seeds, purchased from Chinese Academy of Agricultural Sciences, were sterilized and germinated in the dark at 25 °C for three days. Cucumber seedlings with similar sizes were selected, and each seedling was put into a beaker (250 mL) containing 100 mL of 1/4 strength Hoagland’s solution. The culturing conditions were similar to those described in our previous work.32 At the second leaf stage, the seedlings (five seedlings per treatment) were transferred to the freshly prepared treatment solution containing Cs (40 mg/L), PAA (60 mg/L),


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Cs-nCeO2 (50, 200 and 1000 mg/L), or PAA-nCeO2 (50, 200 and 1000 mg/L), respectively, and allowed to grow for 14 days in a growth chamber. The control plants were grown in pure nutrient solution. At the end of the experiment, the harvested seedlings were washed thoroughly with deionized water. The biomass of roots and shoots was separately determined after drying with an oven (75 °C) to a constant weight. The Ce contents in the plant tissues were measured using ICP-MS (Thermo, U.S.) according to the previous study.32 2.3 Hydrogen peroxide visualization and quantification Visualization

of

the

localization

of

H2O2

was

examined

using

3,

3'-diaminobenzidine (DAB) as reported in previous research.34 Briefly, the excised roots and leaves of the control and treated plants were placed in DAB-HCl (1 mg/mL, pH 3.2~3.8) solution and incubated for 8 h under vacuum. The stained roots were rinsed thoroughly to remove the residual DAB. The stained leaves were transferred into a jar containing absolute ethanol and boiled for approximately 8 minutes to remove chlorophyll and then visualized using a camera. For quantification of H2O2, the samples were ground in liquid nitrogen and solubilized in a mixture of 2 M KOH and DMSO (volume ratio 1:1.167). Using a spectrophotometer (Jasco, Tokyo, Japan), the amount of formazan formed in roots and leaves were measured at 700 nm. 2.4 TEM Observation After a 14 d treatment, the root tips (3 mm) of cucumbers that treated with 1000 mg/L Cs-nCeO2 and PAA-nCeO2 were excised and cleaned. Then the samples were fixed, embedded, and sectioned following the previously described procedures.32 The observation of the sections and compositional analyses of the specific areas in roots were performed using TEM (JEM-1230, JEOL, Japan) combined with energy dispersive X-ray (EDX) spectroscopy (Oxford Instruments, Oxfordshire, UK). 2.5 Elemental mapping by synchrotron-based XRF



Ce localization patterns in the cucumber tissues were mapped using micro X-ray fluorescence (μ-XRF). After treated with 1000 mg/L PAA-nCeO2 and Cs-nCeO2 NPs for 14d, the fresh leaves and roots were cut, thoroughly washed and separately stick to the 3 M tape. The μ-XRF microspectroscopy experiment was performed at 4W1B beamline, Beijing synchrotron Radiation Facility (BSRF), the ring storage energy of which is 2.5 GeV with current intensity from 150 to 250 mA. The incident X-ray energy was monochromatized by a multilayer reflector and was focused down to 2050 μm by the polycapillary lens. The sample was held on a precision motor-driven stage and the two-dimensional mapping was acquired by step-mode with 50 or 100 μm stepwise. The X-ray fluorescence emission lines was detected by Si(Li) solid state detector with live time of 30 s. The data were analyzed using PyMca package. 2.6 Speciation analysis by XANES The dried roots and shoots of cucumber treated with 1000 mg/L PAA-nCeO2 and Cs-nCeO2 NPs were homogenized and pressed into thin slices. Ce speciation in tissues was analyzed by XANES on beam line 1W1B at BSRF. Ce LIII-edge spectra of the roots and shoots were collected using transmission mode and fluorescence mode, respectively. nCeO2 and CePO4 were used as standard compounds. The Ce XANES spectra were normalized using Athena software and analyzed by linear combination fitting (LCF). 2.7 Data analysis The results were displayed as the means ± standard deviation (SD). All statistical analyses were conducted using Statistical Packages for the Social Sciences (SPSS) Version 18.0. One-way analysis of variance (ANOVA) followed by Tukey’s HSD test was performed to examine the statistical differences between the treatments, and p < 0.05 was considered to be a significant difference.

3. RESULTS AND DISCUSSION


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3.1 Characterization of modified CeO2 NPs In this study, we synthesized Cs-nCeO2 and PAA-nCeO2, endowing them with a positive and negative surface charge, respectively. TEM images showed that the modified NPs had similar core sizes (~7 nm) with those of raw nCeO2 (Figure 2). In addition, the sharp edges and lattices of nCeO2 could be clearly seen in TEM images (Figure 2A). But those for both modified NPs became blurred (Figure 2B and C), which might be due to the polymer coating on the surface of the NPs. The XRD patterns of Cs-nCeO2 and PAA-nCeO2 were similar to that of nCeO2 with the cubic fluorite structure (JCPDS card no. 34-0394, Figure S1). The functionalization was further confirmed by the differences in the FTIR spectra between nCeO2 and modified ones (Figure S2). The absorption peak at wave number 2926 cm-1 was presumed to be C-H stretching vibration peak of PAA or Cs. At wave number 1720 cm-1, it might be the stretching vibration peak of carboxyl C=O of PAA. There strong absorption peak at wave number ~1000-1300 and 1618 cm-1 can be attributed to C-O, C-N=, and N-H after crosslinking between Cs and glutaraldehyde. Moreover, Cs-nCeO2 and PAA-nCeO2 were analyzed by TGA (Figure S3) and the amount of Cs and PAA on nCeO2 was calculated to be 3.08% and 5.13%, respectively. The above results proved that there were organic coatings on the surface of nCeO2. On the basis of DLS data (Table 1), the average hydrodynamic diameters of nCeO2, Cs-nCeO2 and PAA-nCeO2 in deionized water were 165.5, 263.4 and 117.3 nm, respectively. The hydrodynamic diameters of Cs-nCeO2 and PAA-nCeO2 suspended in the nutrient solution were similar to those in water. The zeta potential of nCeO2 was positive in water, while was changed to negative in the nutrient solution. In contrast, the electronegativity of Cs-nCeO2 and PAA-nCeO2 was consistent in water and the nutrient solution, which suggested that the NPs were stabilized by the coatings. After 14 days of preservation in the media, they could still maintain their original charges and not be agglomerated (Figure S4). However, the hydrodynamic diameter and zeta potential of uncoated nCeO2 could not be measured in the nutrient



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solution because of the strong aggregation. After incubation for 14 d, the amounts of Ce3+ ions released from Cs-nCeO2 and PAA-nCeO2 were respectively 0.0006% and 0.012% (percent of total Ce), which corroborated the stability of coated nCeO2 in the culture medium.

Figure 2 TEM images of nCeO2 (A), Cs-nCeO2 (B), and PAA-nCeO2 (C). Table 1. The hydrodynamic diameters and zeta potential of three kinds of NPs at 0 and 30 d in deionized water and the culture medium.

in water hydrodynamic

in nutrient solution

diameters

(0 d)

(nm)

in nutrient solution

CeO2 NPs

Cs-nCeO2

PAA-nCeO2

165.5 ± 9.6

263.4 ± 12.0

117.3 ± 7.5

735.8 ± 36.5

289.7 ± 19.2

128.3 ± 14.3

/

322.8 ± 23.6

125.2 ± 13.2

+43.7 ± 3.8

+38.3 ± 1.5

-31.5 ± 1.0

-11.3 ± 3.9

+33.6 ± 0.8

-29.5 ± 2.3

/

+27.9 ± 1.2

-29.1 ± 0.6

(14 d) in water Zeta potential

in nutrient solution (0 d)

(mV)

in nutrient solution (14 d)

/: not determined.

3.2 Effects of modified nCeO2 on plant growth 3.2.1 Effects of modified nCeO2 on biomass


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The biomass of roots and shoots of cucumber under different treatments are displayed in Figure S5. Neither of the two coated nCeO2 affected the shoot weights at all tested concentrations. In contrast, Cs-nCeO2 at 200 and 1000 mg/L promoted the root weights by 45.9% and 37.3% over the control, respectively. We also examined the effects of coating materials (Cs and PAA) on plant growth and found that they had no obvious effects on the growth of cucumber at the coating concentrations (Figure S5). According to the published literature, the positive, negative, and neutral effects of bare CeO2 NPs on the growth of various plant species had been reported.35-39 For instance, Rico et al. reported that the biomass of barley was increased, while the biomass of rice was inhibited when exposed to 500 mg/L of CeO2 NPs.40 Zhang et al. found that the fresh biomass of radish storage roots was enhanced by CeO2 NPs at 10 mg Ce/L.40 Zhao et al. demonstrated that the yield of cucumber was not impacted under the treatment of CeO2 NPs at 400 mg/kg, but the yield was reduced by 31.6% at higher concentration (800 mg/kg) compared to the control.42 We previously found that there was less effect of uncoated CeO2 NPs on the growth of cucumber.24, 32, 34 These findings were inconsistent with the result of this study, which might be related to the surface coatings of the NPs. In order to elucidate the reason why Cs-nCeO2 promoted the root biomass, we further assessed the oxide stress in plants and observed the morphological changes of roots. 3.2.2 Hydrogen peroxide visualization and quantification Reactive oxygen species (ROS) are common byproducts in organism metabolism. Excessive ROS may cause oxidative stress and induce a series of adverse impacts on plants.43 Some studies have shown that nCeO2 can induce oxidative damage to plants because of the ROS generation catalyzed by the surface active sites; on the other hand, the specific ROS scavenging ability of nCeO2 can protect plants from oxidative damage. For instance, Hong et al18 found that the foliar spray of CeO2 NPs changed the activities of antioxidant enzymes in cucumber and induced the production of ROS, which affected the growth of plants. However, Perez et al.



reported that the dextran-modified nCeO2 had antioxidant enzyme mimic activity and could catalyze H2O2 decomposition at pH 7.4.44 As one of the representative of ROS, the contents of H2O2 can reflect the level of ROS in plants. As shown in Figure S6 and S7, DAB stained the cucumber roots and leaf veins of the three groups in brown, which indicated that H2O2 was concentrated in these areas. Further, quantitative analyses showed that there was no significant difference in the contents of H2O2 among the three groups, indicating that the coated CeO2 NPs had little effect on the cucumber leaves. However, the amount of H2O2 in the roots of Cs-nCeO2 group was significantly lower than those of the other two groups, indicating less ROS formation in the former group (Figure S8). Therefore, Cs-nCeO2 adsorbed on the root surface of cucumbers could protect them from ROS damage, which might be one possible reason for Cs-nCeO2 to promote the root growth. 3.2.3 Morphological observation of roots The morphology changes of cucumber roots under the treatments of coated nCeO2 were also observed using light microscope. As can be seen in Figure S6, the control root had a healthy and intact tip, which was similar to that in the presence of PAA-nCeO2 (1000 mg/L). However, for Cs-nCeO2 treatment (Figure S6B), abundant root hairs and adsorbents were observed on the root surface compared with that of the control, although the root was cleaned thoroughly. The different morphologies of roots between the treatments of Cs-nCeO2 and PAA-nCeO2 might be attributed to their different surface charges. The root surface is negatively charged because plant cell walls contain high concentrations of uronic acids.45 Therefore, the positively charged Cs-nCeO2 was more inclined to be adsorbed on the root surface than the negatively charged PAA-nCeO2. The abundant root hairs might increase the surface area of the roots and thus made plants obtain more nutrients from the solution. Moreover, Cs can induce lignin formation46 and some forms of nitrogen in Cs may play as a potential source of nitrogen to influence the plant growth,47 which might also be the reasons why Cs-nCeO2 promoted the root growth of cucumbers.


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3.3 Effects of coated nCeO2 on contents and distribution of Ce in plants 3.3.1 Ce contents in plant tissues To investigate the distribution and translocation of coated nCeO2 in cucumber plants, contents of Ce in the roots and shoots were determined by ICP-MS. As shown in Figure 3A, the contents of Ce in the roots under the treatments of Cs-nCeO2 were significantly higher than those of the PAA-nCeO2 treatments, especially at higher exposure concentrations. It should be pointed out that the total Ce within and outside the root was measured, since ICP-MS can’t distinguish between them. The different Ce contents under the two treatments were likely attributed to the electrostatic interaction between the root surface and charged NPs. It is well known that the plant root epidermis is negatively charged due to the carboxyl groups of organic acids in the root exudates.48 Therefore, positive Cs-nCeO2 was more easily to be adsorbed on the root surface, which led to a high accumulation of Ce. This result was consistent with other studies.49-51 In addition, there was a concentration-dependent of Ce in plant tissues when exposed to Cs-nCeO2. As the exposure concentration increased, the uptake of total Ce significantly increased in both the roots and shoots. In contrast, there was no concentration-dependent effect in PAA-nCeO2 group, which might be due to the electrostatic repulsion between the negative PAA-nCeO2 and root surface. Similarly, Barrios et al52 found that the citric acid modified nCeO2 with negative charge had no concentration dependent effects in tomato roots in soil culture. Trujillo-Reyes et al. also reported the similar result of citric acid coated nCeO2 to radish plant.53 Interestingly, although PAA-nCeO2 had lower accumulation in the roots, the contents of Ce in the shoots in this group were about twice as high as those of the positively charged group, which was consistent with the previous results.27,

28

To

compare the translocation capability of the different charged nCeO2 from roots to shoots, translocation factors (TFs) were calculated by dividing the Ce contents in the shoots by those in the roots. Clearly, the TF values of PAA-nCeO2 group were



significantly higher than those of Cs-nCeO2 group at all tested concentrations (Figure 3B). The relatively low root accumulation and high shoot internalization for PAA-nCeO2 indicated that negatively charged NPs could still overcome the electrostatic and/or potential repulsion, and were more advantageous to transport from the roots to the shoots.

Figure 3. Root/shoot contents of Ce (A) and TFs (B) in cucumber plants exposed to different concentrations of Cs-nCeO2 and PAA-nCeO2. Significant differences are expressed as lowercase or uppercase letters (p < 0.05).

3.3.2 TEM observation of the root tips After exposure to 1000 mg/L Cs-nCeO2 and PAA-nCeO2 for 14 d, the root sections of cucumber were observed by TEM. As shown in Figure 4, a large number of Cs-nCeO2 and their aggregations were attached to the root surface (Figure 4A), while the PAA-nCeO2 was hardly adsorbed on the epidermis (Figure 4E). Moreover, no ceria NP was found inside the roots under the two treatments. Because the diameter of pores in cell walls of plants is about 3-8 nm,54 only single particle/very small agglomerates can enter the roots. So it is difficult to distinguish between the background and small particles by TEM. In addition, some needlelike or urchin-like clusters in the intercellular regions and a large number of flocculent in vacuoles were observed under the two treatments (Figure 4B-D and F-H). The EDX spectra confirmed the presence of P and Ce in the dense deposits inside the roots (Figure S9).


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Accordingly, it was deduced that the original NPs were adsorbed on the root surface, whereas their transformed product CePO4 was deposited inside the roots. It was worth noting that the amount of clusters in the intercellular space of root cells in PAA-nCeO2 group was larger than that in Cs-nCeO2 group, and the structure of clusters was more tightly in the former than the latter group (Figure 4B, C, G and H). Combing the above ICP-MS results that more Ce was transported to the shoots in PAA-nCeO2 group, we speculated that the amount of Ce3+ ions released from PAA-nCeO2 at the nano-bio interface was more than that from Cs-nCeO2.

Figure 4. TEM images of root sections of cucumbers treated with 1000 mg/L Cs-nCeO2 (A-D) and PAA-nCeO2 (E-H) at root epidermis (A, E), cell gaps (B, H), and vacuoles (D, F). Panels B, D, E and H were the magnifications of the highlighted rectangle areas in panels C, E and G, respectively.

3.4 Distribution and transformation of Ce in cucumber plants 3.4.1 Ce distribution in cucumber tissues The -XRF images in Figure 5 and Figure S10 show the distribution of Ce in



cucumber roots and leaves after exposure to 1000 mg/L of Cs-nCeO2 and PAA-nCeO2 for 14 days. Ce signals were detected mainly in the root tips (Figure S10) and the main roots (Figure 5) under the two treatments. Moreover, the intensity of Ce in Cs-nCeO2 group was significantly higher than that in PAA-nCeO2 group, which was consistent with the result of ICP-MS. And interestingly, Ce signals were stronger in the junctions between the lateral root and main root than in other areas under both of the treatments, demonstrating the possible transport routes of Ce through these regions. It is well known that Casparian strip is a barrier in the endodermis of plant roots, preventing the transfer of substances from the cortex to the xylem. The molecules that reach the endodermis either through apoplastic or symplastic pathways must enter the symplast before they reach the vascular cylinder. However, the Casparian strip at lateral roots, developed from the cell layers in the stele, is disconnected and thus a bypass into the vascular bundle is provided without entering the symplast.9 The compounds bypassing the barrier of Casparian strip to enter the root has been reported in several studies.55-57 Besides the lateral roots, another possible route for NPs to traverse this barrier is through the root apical meristem, where the Casparian strip is poorly developed because of rapid cell division. From this region, NPs can easily enter the vascular bundle and be transported upward by water flow.29 In this study, the different forms of Ce-containing compounds might enter the vascular bundles and transport upwards through the gaps of Casparian strip at the root tips and lateral roots.


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Figure 5. -XRF images of Ce in cucumber roots and leaves after exposed to 1000 mg/L Cs-nCeO2 and PAA-nCeO2. The red area of each map corresponds to the maximum concentration of the Ce element. The lateral roots are denoted by rectangles in the LM images. The scale bars in roots and leaves represent 100 m 500 m, respectively.

For leaves, Ce signals were concentrated not only in the veins but also at the edge of leaves of both treatments (Figure 5). We previously investigated the distribution of CeO2 NPs and Ce3+ ions in cucumber plants using radioisotope labeling and found that Ce in the NPs group was predominately distributed at the edge of the leaves, while Ce in the ions group was mainly accumulated along the veins.29 Recently, Li et al. studied the subcellular distribution of Ce in tomato on exposure to different charged CeO2 NPs using -XRF and -XANES spectroscopy. They found that the untransformed Ce(IV)O2 was primarily accumulated in the mesophyll, whereas Ce(III) was accumulated in the veins.28 In this study, the distribution pattern of Ce was similar to that in the above two reports, so we speculated that Ce was transported simultaneously in the forms of Ce(III) and Ce(IV). 3.4.2 Ce transformation in cucumber tissues XANES spectroscopy has been proved to be very useful for distinguishing between Ce(III) and Ce(IV), with the former producing one absorption peak and the latter producing two peaks. Figure 6A shows the normalized Ce XANES spectra of samples and standard compounds. The solid vertical line represents the characteristic peak of Ce(III), and the dotted lines represent the two peaks of Ce(IV). It could be found that the spectra of all cucumber tissue samples exhibited the features of mixture of Ce(III) and Ce(IV), especially in the shoots. This indicated that the intact CeO2 NPs together with their transformation products were translocated in plants. LCF results showed that Ce was presented as Ce(IV) in as-synthesized Cs-nCeO2 and PAA-nCeO2 (data not shown). However, 11% of Cs-nCeO2 and 21.6% of PAA-nCeO2 were transformed from Ce(IV) to Ce(III) in the roots, and the proportion of Ce(III) in the shoots was 35.5% for Cs-nCeO2 group and 32% for PAA-nCeO2 group, respectively. To further



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explore the different transport behaviors of different charged nCeO2, the absolute contents of Ce(IV)/Ce(III) in the roots and shoots were calculated by multiplying each proportion of Ce(III) and Ce(IV) by the total Ce contents (Figure 6B). In the roots, the amount of Ce(IV) in Cs-nCeO2 group were much higher than that in PAA-nCeO2 group, because a large amount of NPs was attached to the root surface in the former group. However, Ce in the shoots can only be obtained by transport from the roots. The amounts of Ce (IV) and Ce(III) in the shoots in the PAA-nCeO2 group were both higher than those in Cs-nCeO2 group, which explained the observed poor translocation efficiency of the Cs-nCeO2 treatment (Figure 3B). The different transport behavior of Ce(IV) between Cs-nCeO2 and PAA-nCeO2 groups might also be attributed to their different surface charge. Since there are many negatively charged groups on the walls of xylem, the translocation of positively charged Cs-nCeO2 as particles was usually more difficult than the negative PAA-nCeO2 in xylem. We previously demonstrated that CeO2 NPs adsorbed on the root surface can be partially dissolved by root exudates.24 Some of the released Ce3+ ions were precipitated by phosphate around the rhizosphere and in the cell gaps and others were complexed with carboxyl ligands to transport upwards along the xylem.32 In this study, similar transformation and translocation of coated nCeO2 were observed although the NPs were modified by different surface charges. In addition, Cs-nCeO2 and PAA-nCeO2 were better dispersed in the nutrient solution than nCeO2 due to the surface modification, so they had more opportunities to enter vascular bundle through the gap of the Casparian strip at the root tip or lateral roots. After entering the roots of cucumber, Ce(III) was combined with the negative carboxyl groups on the walls of xylem and concentrated in the veins, while Ce(IV) was transported with the water flow driven by transpiration and finally accumulated at the edge of leaves.29,

37

Therefore, Ce signals were observed not only in the veins but also the margins of leaves of the two treatments (Figure 5B).


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Figure 6. Analyses of Ce XANES spectra (A) and the total contents of Ce(III) and Ce(IV) in the roots (g/kg) and shoots (mg/kg) (B) of cucumber exposed to 1000 mg/L Cs-nCeO2 and PAA-nCeO2.

4. CONCLUSION In the present study, Cs-nCeO2 and PAA-nCeO2 with different surface charges were synthesized and were stable in the nutrient solution for a long time. Then the phytotoxicity, translocation, and transformation of these NPs in cucumber plants were investigated. Cs-nCeO2 could decrease ROS level in the roots and promote the root growth at high concentrations. The surface charge of NPs played important roles in determining their uptake and translocation in plants, and PAA-nCeO2 was more likely to facilitate long-distance transport in vascular bundles, which suggested that surface charge functionalization can be applied to design smart delivery nanomaterials for targeted delivery systems in agriculture. Supporting Information The Supporting Information is available free of charge on the ACS Publications website. XRD, FT-IR, and TGA results of uncoated and coated nCeO2 (Figure S1-3). Images of nCeO2, Cs-nCeO2, and PAA-nCeO2 incubated in the exposure medium at



1000 mg/L for 0 and 14 d (Figure S4). Root and shoot biomass of cucumber exposed to PAA, Cs, and different concentrations of Cs-nCeO2 and PAA-nCeO2 (Figure S5). Images and quantitation of H2O2 contents in cucumber root and leaves after DAB staining (Figure S6-8). The representative EDX spectrum of dense deposits inside the roots from TEM scans (Figure S9). -XRF images of Ce in cucumber root tips after exposed to Cs-nCeO2 and PAA-nCeO2 (Figure S10). Conflict of Interest The authors declare no competing financial interest. Acknowledgments This work was financially supported by National Natural Science Foundation of China (Grant No. 11575208, 11675190, and 11875267) and the Ministry of Science and Technology of China (Grant No. 2016YFA0201604).

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