Xylem and Phloem Based Transport of CeO2 Nanoparticles in

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Xylem and Phloem Based Transport of CeO2 Nanoparticles in Hydroponic Cucumber Plants Yuhui Ma, Xiao He, Peng Zhang, Zhiyong Zhang, Yayun Ding, Junzhe Zhang, Guohua Wang, Changjian Xie, Wenhe Luo, Jing Zhang, Lirong Zheng, Zhifang Chai, and Ke Yang Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.6b05998 • Publication Date (Web): 06 Apr 2017 Downloaded from http://pubs.acs.org on April 10, 2017

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Environmental Science & Technology

Xylem and Phloem Based Transport of CeO2 Nanoparticles in Hydroponic Cucumber Plants 85x45mm (300 x 300 DPI)

ACS Paragon Plus Environment


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Xylem and Phloem Based Transport of CeO2 Nanoparticles in

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Hydroponic Cucumber Plants

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Yuhui Ma,a,1 Xiao He,a,1 Peng Zhang,a Zhiyong Zhang,a, b, * Yayun Ding,a Junzhe Zhang,a Guohua Wang,a Changjian Xie,a Wenhe Luo,a Jing Zhang,c Lirong Zheng,c Zhifang Chai,a Ke Yangd

3 4 5 6

7

8

a

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

Key Laboratory for Biomedical Effects of Nanomaterials and Nanosafety, Institute

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b

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Beijing 100049, China.

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c

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Academy of Sciences, Beijing 100049, China.

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d

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Chinese Academy of Sciences, Shanghai 201204, China.

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

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

Shanghai Synchrotron Radiation Facility, Shanghai Institute of Applied Physics,

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* Corresponding author.

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E-mail address: [email protected]

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Tel: +86-10-88233215; Fax: +86-10-88235294

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1

The two authors contributed equally to this article.

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Abstract

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Uptake and translocation of manufactured nanoparticles (NPs) in plants have

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drawn much attention due to their potential toxicity to the environment, including

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food webs. In this paper, the xylem and phloem based transport of CeO2 NPs in

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hydroponic cucumber plants was investigated using a split-root system. One half of

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the root system was treated with 200 or 2000 mg/L of CeO2 NPs for three days,

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whereas the other half remained untreated, with both halves sharing the same aerial

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part. The quantitative distribution and speciation of Ce in different plant tissues and

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xylem sap were analyzed by inductively coupled plasma-mass spectrometry,

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transmission electron microscope, X-ray absorption near edge structure, and X-ray

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fluorescence. Results show that about 15% of Ce was reduced from Ce(IV) to Ce(III)

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in the roots of the treated-side (TS), while almost all of Ce remained Ce(IV) in the

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blank-side (BS). The detection of CeO2 or its transformation products in the xylem

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sap, shoots and BS roots indicates that Ce was transported as a mixture of Ce(IV) and

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Ce(III) from roots to shoots through xylem, while was transported almost only in the

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form of CeO2 from shoots back to roots through phloem. To our knowledge, this is the

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first report of root-to-shoot-to-root redistribution after transformation of CeO2 NPs in

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plants, which has significant implications for food safety and human health.

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Introduction

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CeO2 NPs (nano-ceria), produced in large quantities1, are widely used in

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catalysts2, UV-blockers, gas sensors3, solid-state fuel cells4, polishing agents, and so

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on. With the manufacture and applications, this nanomaterial will be inevitably

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released into the environment, potentially posing environmental risks5. Plants are the

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basic components of the ecological system and may serve as a potential pathway for

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NP transport and a route for bioaccumulation into the food chain6, 7. Research on the

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impact of CeO2 NPs after their release in the environment is ongoing, but their

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transport process in plants is still largely unknown. 2



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Besides the phytotoxicity of CeO2 NPs8, the accumulation and translocation of

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CeO2 NPs in many plant species have also been investigated in various culture

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media9-15. According to the previous studies, two exposure pathways were widely

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adopted: through roots or leaves. In the former mode, the accumulation of Ce in the

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plant tissues was usually dose-dependent and most of Ce was retained in the roots,

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with very low transfer factors (TFs) from roots to shoots (smaller than 0.01)16-18. It

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was difficult to distinguish whether the CeO2 NPs were from inside or outside the root,

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since a large number of them were adsorbed on the root surface of hydroponic plants.

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Under roots exposure conditions, Ce in the aerial parts of plants was only translocated

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from the roots, so it was convincible to clarify the transport behavior by analyzing the

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Ce in the shoots. But unfortunately, the involved low content of metal and small

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spatial

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Synchrotron-based techniques, such as X-ray absorption spectroscopy (XAS) and

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micro X-ray fluorescence (μ-XRF), with advanced speciation or spatial resolution

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(μm or nm scale), can play an important role in the studies of the uptake and transport

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of nanomaterials in the plant system27, 28. Another advantage of these methods is that

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they do not need excessive pretreatment of samples (e.g. prior chemical extraction or

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staining), therefore providing a better way to show the actual situation of NPs in the

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biological tissues. By using these techniques, we documented the distribution and

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biotransformation of some REO NPs in cucumber plants, such as La2O319 and Yb2O320

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NPs, as well as CeO2 NPs21, which were previously regarded as stable in the

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environment22. The biotransformation of CeO2 NPs has been proposed to relate to

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natural reducing substances21 and phosphates23, which are ubiquitous in plants24, 25.

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These techniques were also used to study other metal-based NPs in plants26,

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rapid development of synchrotron-based techniques allows us to have new insights

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into the interaction between NPs and organisms.

scale

made

the

(in

situ)

detection

and

analysis

very

difficult.

27

. The

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Considering that CeO2 NPs can be partially transformed in the biological system,

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the mobility of this material in plants should be reevaluated. Meanwhile, the

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mechanisms by which CeO2 NPs are accumulated and transported in plants also need

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further investigation. The objective of present work is to illustrate the accumulation

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and transport of CeO2 NPs in hydroponic cucumber plants as a function of

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transformation through a split-root experiment. The distribution and speciation of Ce

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in plant tissues and cells are analyzed using transmission electron microscope (TEM), 3


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X-ray absorption near edge structure (XANES), and XRF. The possible transport

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process of CeO2 NP in seedlings is also discussed. The results of this study will

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provide an insightful understanding of the fate of CeO2 NPs in the plants.

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Materials and Methods

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CeO2 Nanoparticles

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All chemicals were analytical grade and obtained from the Beijing Chemical

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Plant. CeO2 NPs were synthesized using a precipitation method8. Briefly, The

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solutions of Ce(NO3)3·6H2O (0.0375 M) and hexamethylenetetramine (HMT) (0.05

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M) were mixed and stirred at 75 oC for 3 h. The precipitation was washed with

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deionized water thoroughly and separated by centrifugation. The morphology of the

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as-synthesized NPs was investigated by TEM (Tecnai G2 20 S-Twin, FEI, Japan).

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After sonication for 30 min, the hydrodynamic diameter and zeta-potential of CeO2

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NPs in ultrapure water (20 mg/L) were determined by dynamic light scattering (DLS,

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ZetaSizer, Malvern Instruments, UK). The characterization showed that CeO2 NPs

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were octahedral shape with a primary size of 25.2 ± 2.3 nm (Figure S1). The

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hydrodynamic size of the agglomerates and zeta-potential were 122.6 ± 20.9 nm and

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34.3 ±5.1 mV, respectively.

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Plant Growth and CeO2 NP Application

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Cucumber seedlings were cultured in glass beakers with 1/5 strength Hoagland

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solution and grown under controlled-environment conditions with a 16/8 h, 26/17 oC

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day/night scheme and light intensity of 50 W m2 (PRX-450C, Saifu, China). For more

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details of the growth conditions, please refer to our previous publication21. The

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seedlings at the 3rd leaf stage were treated with CeO2 NPs by the split-root exposure

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mode (Figure 1). The root system of a single plant was manually separated into two

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parts and carefully placed in the two separate containers, which allows the differential

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treatments of separate root systems, while sharing the same aerial part28. If the

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untreated part of the root system shows a response when a stimulus is applied to the

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treated part, a systemic regulation and long-distance transport are suggested to be 4



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involved29, 30. One container was filled with 200 or 2000 mg/L CeO2 NPs suspended

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in ultrapure water (named treated-side, TS), and the other container was filled with

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ultrapure water (named blank-side, BS). The two sides of roots both cultured in

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ultrapure water were taken as the control group. The experiments were performed

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with five plants at each treatment. The seedlings were harvested after three day

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exposure.

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Figure 1. The photograph of the split-root exposure system. TS and BS indicate the treated and

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blank side of roots, respectively.

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Ce Content Determination

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At the end of the experiment, the BS/TS roots and the shoots were separated,

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thoroughly washed with deionized water and lyophilized in a freeze dryer (Alpha 1-2

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LD plus, Christ, Germany). The dry samples were ground into fine powders and

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digested with a mixture of HNO3 and H2O2 (4:1 by volume) on a heating plate (80 oC

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for 1 h, 120 oC for 3 h, and 160 oC for 1 h). Total Ce contents in the tissues were

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determined using inductively coupled plasma-mass spectrometry (ICP-MS, Thermo,

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USA). Indium, as an internal standard, was added in the solution to compensate for

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matrix suppression and signal drifting. Analytical runs included calibration

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verification samples, spike recovery samples, and duplicate dilutions. Mean recovery 5


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of Ce from standard reference material (bush branches and leaves, GBW 07602) was

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101%. Spike recovery averaged 103%, and the mean relative percent difference

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between replicate samples was 3%. The Ce content in the BS solution after exposure

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was also measured to make sure there was no contamination in it.

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Bulk XANES analysis

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XANES spectra were collected on 1W1B beamline of Beijing Synchrotron

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Radiation Facility (BSRF Beijing, China). CeO2 and CePO4/CeAc3 were used as

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reference compounds. Ce LIII-edge absorption spectra of reference compounds and

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samples were collected using transmission and fluorescence mode, respectively. The

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background was removed by spline fitting. The spectra were normalized using linear

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pre-edge and post-edge. The XANES spectra were analyzed by linear combination

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fitting (LCF) using Athena software31. For each sample, the combination of standards

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with the lowest residual parameter was chosen as the most likely set of components.

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In situ distribution and speciation of Ce by TEM and μ-XRF

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After washing thoroughly, the roots apexes were cut and fixed in 2.5%

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glutaraldehyde solution. Then they were dehydrated and embedded in Spurr's resin,

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cut in ultrathin sections (about 90 nm), and mounted on copper grids. Xylem sap

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samples were collected from the cut of seedling stems about 3 cm above the surface

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of the solution. After washing, the stem surface on the root side thoroughly with ultra

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pure water, the tissues were blotted dry and the exuding fluid was collected on a grid

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and drying. Root sections and xylem sap samples were observed by TEM (JEM-1230,

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JEOL, Japan) operating at 80 kV. The compositional analysis of the specific area was

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performed using energy dispersive X-ray spectroscopy (EDS) (Oxford Instruments,

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Oxfordshire, UK). EDS spectra were collected over 100 s with a beam diameter of

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approximately 25 nm.

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XRF analyses were performed on the beamline BL15U at the Shanghai

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Synchrotron Radiation Facility (SSRF Shanghai, China). CeO2 and CePO4 were 6



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chosen as the Ce(IV) and Ce(III) reference materials, respectively. The sample

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preparation and experimental conditions were both consistent with our previous

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reports16. The X-ray fluorescence data were processed using the Igor software

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(Wavemetrics, Lake Oswego, OR) software. For μ-XANES data acquisition, the

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energy level was selected using a Si (111) monochromator and scanned from 5.60 to

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5.80 keV. The analysis of μ-XANES data was carried out using Athena software.

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Results and Discussion

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Xylem based transport of CeO2 NPs in plants

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Figure 2. Contents of Ce in TS/BS roots and shoots under the different treatments. The values

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were given as mean ± SD (n =5). BS and TS indicate the blank and treated side of roots,

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respectively.

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The split-root system is an advanced tool to study the local (root origin) and

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systemic (shoot origin) regulation mechanisms in plants induced by environmental

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factors, such as NPs32. After 3 days of exposure, Ce contents in each side of roots, 7


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shoots, and BS solutions under the different treatments were separately measured by

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ICP-MS. As shown in Figure 2, Ce could be detected in all of the plant tissues, though

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the contents of Ce in the BS roots were much lower than those in the BS roots under

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the exposure of CeO2 NPs. Although the concentration of 2000 mg/L solution was

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one order higher than 200 mg/L solution, Ce contents in TS roots and shoots of 2000

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mg/L group were only about 3 times higher than those of 200 mg/L group. The lower

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bioavailability of 2000 mg/L CeO2 NPs might be due to the agglomeration and

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sedimentation of NPs. It is also possible that the root reached its capacity of

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adsorption or absorption at the higher concentration. After exposure, Ce could hardly

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be found in the BS solutions of the two groups (less than 10 ppb). Considering that

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the lateral transport of substance was limited in plant roots33, almost all of the Ce in

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the BS roots was from the shoots by the transport inside the plants rather than from

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the TS roots or solutions. To verify whether CeO2 NPs can move from the roots to

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shoots, the xylem sap of the cucumber plant exposed to 2000 mg/L CeO2 NPs was

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analyzed by TEM and particles with high electron density were observed (Figure 3A).

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The EDS spectra confirm the presence of Ce as well as P, showing that CeO2 and/or

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its transformed product could be transported from the roots to shoots through xylem

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(Figure 3B). Therefore, the detection of Ce in the shoots, BS roots and xylem sap

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suggests that Ce-containing species could be transported throughout the whole plant

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by vascular system.

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Figure 3. TEM image (A) and EDS spectra (B) of the dark particles in the xylem sap.

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Observation of CeO2 NPs in the roots using TEM

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Figure 4. TEM images of cucumber root sections at the TS root surface (A), inside the TS root

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(B), and BS root surfaces (C, D) under the treatment of 2000 mg/L CeO2 NPs. The insets are

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higher magnification of the rectangular areas.

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TEM images in Figure 4 show the distribution of Ce in the TS and BS root

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sections of cucumbers treated by 2000 mg/L CeO2 NPs for three days. It can be seen

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that a large number of NPs or aggregates were adsorbed on the TS root surface

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(Figure 4A). NPs could be adhered to root surfaces by exudates, which contain large

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amounts of mucilage34, and these NPs could not be wiped off just by rinsing13, 18. In

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addition, some needle-like clusters with high electron density, the shapes of which

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were different from that of the original CeO2 NPs (Figure S1), were also found inside

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the TS root, such as in the cytoplasm, vacuoles, and middle lamellas (Figure 4B). 9


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Inside the BS roots, however, almost no high electron density substance was found

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(Figure S2), which might be attributed that the absence of Ce in the selected area or

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the concentration of Ce was too low to be detected by TEM35. But interestingly, some

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high electron density substance was observed in sporadic distributions in the

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epidermis of BS roots (Figure 4C), and even some like exosomes coated with NPs

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were observed on the surface of the BS root (Figure 4D). Meanwhile, the morphology

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of these deposits was generally similar to that of pristine CeO2 NPs, but with some

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weathering. It has been reported that plant tips (for example, trichomes on leaves)

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were involved in the protection of the plant against diverse environmental

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challenges36. Trichomes were also suggested as possible excretory system for

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different kinds of NPs, such as TiO226 or CeO216 NPs. In the present study, the

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distribution of Ce in BS roots suggests that CeO2 NPs was transported from shoots to

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roots and might be excreted to the environment through the cucumber root tips.

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Speciation of Ce in plant tissues

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To examine the biotransformation of CeO2 NPs in plants after treated with 200

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and 2000 mg/L CeO2 NPs for 3 days, the speciation of Ce in different tissues was

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analyzed using XANES. Based on the distinction of Ce(IV) and Ce(III) compounds,

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the spectra of Ce in the shoots and TS roots exhibit a mixture of Ce(III) and (IV)

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oxidation states, with the appearance of shoulders at the feature of Ce(III) (Figure 5A).

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Calculated by LCF, about 15% of Ce(IV) was reduced to Ce(III) in the TS roots of the

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two groups, while 18% and 8.1% of Ce was present as Ce(III) in the shoots at

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concentrations of 200 and 2000 mg/L respectively (Figure 5B), confirming the

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biotransformation of CeO2 NPs. In contrast, the spectra of Ce in the BS roots were

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almost the same as that of the initial CeO2 NPs (Figure 5A). The quantitative results

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of LCF revealed that the proportions of Ce(IV) at 200 and 2000 mg/L treatment were

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100% and 98.3%, respectively (Figure 4B), indicating that the CeO2 NPs were hardly

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reduced in the BS roots, which was consistent with our previous results that the

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transformation of CeO2 NPs only take place at the root surface of hydroponic 10



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cucumber plants37. Moreover, no Ce(IV)-containing species was found in the plant

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tissues when treated with Ce3+ ions16, which eliminated the possibility of reoxidation

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from Ce(III) to Ce(IV) in the BS roots. Therefore, the different speciation of Ce in the

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two sides suggests that the biotransformation of CeO2 NPs almost exclusively

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occurred in the TS roots. The very small amount of Ce(III) (< 2%) in the BS roots of

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2000 mg/L treatment might be due to the transformation of CeO2 NPs after they

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returned to the root surface. These results imply that the transport way of Ce(IV) and

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Ce(III) compounds was completely different: the former one could be translocated

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from the shoots back to roots while the latter one could not. In a similar treatment

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with CuO NPs, Wang et al. reported that Cu could be translocated from roots to shoots

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and from shoots back to roots in maize, but they found some of the CuO NPs were

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reduced from Cu (II) to Cu (I) during the downward transport32. Considering that the

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reactivity of CuO is much higher than that of CeO2, this result was not difficult to

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understand.

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Figure 5. Ce XANES spectra (A) and percent contributions of Ce(III)/Ce(IV) to the fit of LCF

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analysis (B) of the corresponding tissues under the treatment of 200 and 2000 mg/L CeO2 NPs. BS

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and TS indicate the blank and treated side of roots, respectively.

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Phloem based transport of CeO2 NPs in plants

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The bulk XANES results were acquired from homogeneous samples of the whole

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root tissue, which could not distinguish whether the Ce was localized on the root 11


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surface or inside the root. Therefore, we further investigated the in situ distribution

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and speciation of Ce in cucumber root sections by the combined use of -SRXRF and

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-XANES. The normalized X-ray fluorescence intensities are scaled by color-coded

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map from minimum (blue) to maximum (red). As shown in Figure 6A, the distribution

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of Ce in the TS roots was similar at the two different concentrations of CeO2 NPs,

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with the highest concentration of Ce in the root epidermis and a little Ce being

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scattered in the cortex, which was consistent with the TEM observations (Figure 4).

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Conversely, in the BS roots, Ce concentrations were much lower than those in the TS

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roots and they were irregularly scattered throughout the whole root section (Figure

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6B). These results agreed well with the Ce contents in the roots obtained from the

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ICP-MS (Figure 2). Moreover, the scattered appearance of Ce inside the BS roots

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corroborated that Ce-containing species were translocated from the shoots back to

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roots rather than contaminated by the other side. Figure 6C shows the Ce -XANES

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spectra of the high intensity spots which were selected from the color-coded μ-XRF

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map. As can be seen, the absorption spectra of Spot 1 and 2 both resembled that of

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Ce(IV) reference compound, which further confirmed that Ce was translocated from

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shoots back to roots as CeO2. It is generally accepted that NPs are upward transferred

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from the roots to shoots through the apoplastic pathway by the xylem vascular system

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as mineral elements38, 39. However, there is little research on the downward transport

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of NPs from the shoots back to roots. The current study proved for the first time that

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CeO2 NPs could be transported from shoots to roots through phloem. It is well known

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that the phloem transport system is responsible for the movement of photosynthates

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and certain minerals40. The direction of phloem transport can be either up or down,

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depending on where the source and sink are relative to each other. Consequently,

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during reproductive development CeO2 NPs might be transported to seeds and fruits

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of the cucumber plants and be introduced into the food chain.

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Figur 6. -SRXRF images of Ce in root sections of TS (A) and BS (B) under the treatments of

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200 and 2000 mg/L CeO2 NPs. The images were normalized by the Compton scattering radiation

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and showed by the color-coded maps (the bottom line). A quarter of the root section was examined

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as denoted by white rectangles in LM images (the top line). The scale bars represent 100 m.

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Spots 1 and 2 denoted by black arrows in panel B indicated where μ-XANES were acquired. (C)

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The normalized Ce LIII μ-XANES spectra of Ce(III)/Ce(IV) reference, as well as spots 1 and 2

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selected from the BS sections.

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In summary, we demonstrated the transport of CeO2 NPs from the roots to shoots

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and back to the roots within cucumber plants by using multiple advanced techniques.

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Different distribution and speciation of Ce in the two sides of roots highlighted that

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the biotransformation of CeO2 NPs occurred almost exclusively in the TS roots and

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they were translocated from shoots back to roots as the form of CeO2 through phloem

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transport. The accumulated NPs might be subsequently released by terrestrial plants

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via root exudation to the environment or deposited in the edible parts, which could 13


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affect the final fate and environmental impact of NPs in the ecosystem.

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Conflict of Interest The authors declare no competing financial interest.

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Supporting Information

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The Supporting Information is available free of charge on the ACS Publications

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website. TEM image of CeO2 NPs dispersed in ultrapure water (Figure S1). TEM

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observation inside the BS roots of cucumbers under the treatment of 2000 mg/L CeO2

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NPs (Figure S2).

305

Acknowledgments

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This work was financially supported by National Natural Science Foundation of

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China (Grant No. 11375009, 11575208, 11405183, 11675190, 11275215, and

308

11275218) and the Ministry of Science and Technology of China (Grant No.

309

2013CB932703).

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311

References

312 313 314 315 316 317 318 319 320 321 322 323 324 325

1.

Hendren, C. O.; Mesnard, X.; Droge, J.; Wiesner, M. R., Estimating production data for five

engineered nanomaterials as a basis for exposure assessment. Environ. Sci. Technol. 2011, 45, (7), 2562-2569. 2.

Garcia, T.; Solsona, B.; Taylor, S. H., Nano-crystalline ceria catalysts for the abatement of

polycyclic aromatic hydrocarbons. Catal. Lett. 2005, 105, (3-4), 183-189. 3.

Liao, L.; Mai, H.; Yuan, Q.; Lu, H.; Li, J.; Liu, C.; Yan, C.; Shen, Z.; Yu, T., Single CeO2

nanowire gas sensor supported with Pt nanocrystals: Gas sensitivity, surface bond states, and chemical mechanism. J. Phys. Chem. C 2008, 112, (24), 9061-9065. 4.

Cassee, F. R.; Van Balen, E. C.; Singh, C.; Green, D.; Muijser, H.; Weinstein, J.; Dreher, K.,

Exposure, health and ecological effects review of engineered nanoscale cerium and cerium oxide associated with its use as a fuel additive. Crit. Rev. Toxicol. 2011, 41, (3), 213-229. 5.

Johnson, A. C.; Park, B., Predicting contamination by the fuel additive cerium oxide engineered

nanoparticles within the United Kingdom and the associated risks. Environ. Toxicol. Chem. 2012, 31, (11), 2582-2587. 14



326 327 328 329 330 331 332 333 334 335 336 337 338 339 340 341 342 343 344 345 346 347 348 349 350 351 352 353 354 355 356 357 358 359 360 361 362 363 364 365 366 367 368 369

6.

Page 16 of 18

Hawthorne, J.; De La Torre Roche, R.; Xing, B.; Newman, L. A.; Ma, X.; Majumdar, S.;

Gardea-Torresdey, J.; White, J. C., Particle-Size Dependent Accumulation and Trophic Transfer of Cerium Oxide through a Terrestrial Food Chain. Environ. Sci. Technol. 2014, 48, (22), 13102-13109. 7.

Majumdar, S.; Trujillo-Reyes, J.; Hernandez-Viezcas, J. A.; White, J. C.; Peralta-Videa, J. R.;

Gardea-Torresdey, J. L., Cerium biomagnification in a terrestrial food chain: Influence of particle size and growth stage. Environ. Sci. Technol. 2015, 50, 6782-6792. 8.

Ma, Y.; Kuang, L.; He, X.; Bai, W.; Ding, Y.; Zhang, Z.; Zhao, Y.; Chai, Z., Effects of rare earth

oxide nanoparticles on root elongation of plants. Chemosphere 2010, 78, (3), 273-279. 9.

Wang, Q.; Ma, X.; Zhang, W.; Pei, H.; Chen, Y., The impact of cerium oxide nanoparticles to

tomato (Solanum lycopersicum L.) and its implications on food safety. Metallomics 2012, 4, 1105-1112. 10. Gui, X.; Zhang, Z.; Liu, S.; Ma, Y.; Zhang, P.; He, X.; Li, Y.; Zhang, J.; Li, H.; Rui, Y., Fate and Phytotoxicity of CeO 2 Nanoparticles on Lettuce Cultured in the Potting Soil Environment. PloS one 2015, 10, (8), e0134261. 11. Ebbs, S. D.; Bradfield, S. J.; Kumar, P.; White, J. C.; Musante, C.; Ma, X., Accumulation of zinc, copper, or cerium in carrot (Daucus carota) exposed to metal oxide nanoparticles and metal ions. Environ. Sci. Nano 2016, 3, (1), 114-126. 12. Hernandez-Viezcas, J. A.; Castillo-Michel, H.; Andrews, J. C.; Cotte, M.; Rico, C.; Peralta-Videa, J. R.; Ge, Y.; Priester, J. H.; Holden, P. A.; Gardea-Torresdey, J. L., In situ synchrotron X-ray fluorescence mapping and speciation of CeO2 and ZnO nanoparticles in soil cultivated soybean (Glycine max). ACS nano 2013, 7, (2), 1415-1423. 13. Zhang, Z.; He, X.; Zhang, H.; Ma, Y.; Zhang, P.; Ding, Y.; Zhao, Y., Uptake and distribution of ceria nanoparticles in cucumber plants. Metallomics 2011, 3, (8), 816-822. 14. Servin, A. D.; De La Torre-Roche, R.; Castillo-Michel, H.; Pagano, L.; Hawthorne, J.; Musante, C.; Pignatello, J.; Uchimiya, M.; White, J. C., Exposure of agricultural crops to nanoparticle CeO 2 in biochar-amended soil. Plant Physiol. Biochem. 2017, 110, 147-157. 15. Cui, D.; Zhang, P.; Ma, Y.; He, X.; Li, Y.; Zhang, J.; Zhao, Y.; Zhang, Z., Effect of cerium oxide nanoparticles on asparagus lettuce cultured in an agar medium. Environ. Sci. Nano 2014, 1, 459-465. 16. Ma, Y.; Zhang, P.; Zhang, Z.; He, X.; Li, Y.; Zhang, J.; Zheng, L.; Chu, S.; Yang, K.; Zhao, Y., Origin of the different phytotoxicity and biotransformation of cerium and lanthanum oxide nanoparticles in cucumber. Nanotoxicology 2015, 9, (2), 262-270. 17. Majumdar, S.; Peralta-Videa, J. R.; Bandyopadhyay, S.; Castillo-Michel, H.; Hernandez-Viezcas, J. A.; Sahi, S.; Gardea-Torresdey, J. L., Exposure of cerium oxide nanoparticles to kidney bean shows disturbance in the plant defense mechanisms. J. Hazard. Mater. 2014, 278, 279-287. 18. Schwabe, F.; Schulin, R.; Limbach, L. K.; Stark, W.; Bürge, D.; Nowack, B., Influence of two types of organic matter on interaction of CeO2 nanoparticles with plants in hydroponic culture. Chemosphere 2013, 91, (4), 512-520. 19. Ma, Y.; He, X.; Zhang, P.; Zhang, Z.; Guo, Z.; Tai, R.; Xu, Z.; Zhang, L.; Ding, Y.; Zhao, Y., Phytotoxicity and biotransformation of La2O3 nanoparticles in a terrestrial plant cucumber (Cucumis sativus). Nanotoxicology 2011, 5, 743-753. 20. Zhang, P.; Ma, Y.; Zhang, Z.; He, X.; Guo, Z.; Tai, R.; Ding, Y.; Zhao, Y.; Chai, Z., Comparative toxicity of nanoparticulate/bulk Yb2O3 and YbCl3 to cucumber (Cucumis sativus). Environ. Sci. Technol. 2012, 46, 1834-1841. 21. Zhang, P.; Ma, Y.; Zhang, Z.; He, X.; Zhang, J.; Guo, Z.; Tai, R.; Zhao, Y.; Chai, Z., Biotransformation of Ceria Nanoparticles in Cucumber Plants. ACS nano 2012, 6, (11), 9943-9950. 15


Page 17 of 18

370 371 372 373 374 375 376 377 378 379 380 381 382 383 384 385 386 387 388 389 390 391 392 393 394 395 396 397 398 399 400 401 402 403 404 405 406 407 408 409 410 411 412 413


22. Cornelis, G.; Ryan, B.; Mclaughlin, M. J.; Kirby, J. K.; Beak, D.; Chittleborough, D., Solubility and batch retention of CeO2 nanoparticles in soils. Environ. Sci. Technol. 2011, 45, (7), 2777-2782. 23. Rui, Y.; Zhang, P.; Zhang, Y.; Ma, Y.; He, X.; Gui, X.; Li, Y.; Zhang, J.; Zheng, L.; Chu, S., Transformation of ceria nanoparticles in cucumber plants is influenced by phosphate. Environ. Pollut. 2015, 198, 8-14.24. 24. Haverkamp, R. G., Silver and gold nanoparticles in plants: sites for the reduction to metal. Metallomics 2012, 3, (6), 628-632. 25. Slewinski, T. L.; Braun, D. M., Current perspectives on the regulation of whole-plant carbohydrate partitioning. Plant Sci. 2010, 178, (4), 341-349. 26. Yin, L.; Cheng, Y.; Espinasse, B.; Colman, B. P.; Auffan, M.; Wiesner, M.; Rose, J.; Liu, J.; Bernhardt, E. S., More than the ions: the effects of silver nanoparticles on Lolium multiflorum. Environ. Sci. Technol. 2011, 45, 2360-2367. 27. Servin, A. D.; Castillo-Michel, H.; Hernandez-Viezcas, J. A.; Corral, B.; Peralta-Videa, J. R.; Gardea-Torresdey, J. L., Synchrotron micro-XRF and micro-XANES confirmation of the uptake and translocation of TiO2 nanoparticles in cucumber (Cucumis sativus) plants. Environ. Sci. Technol. 2012, 46, 7637-7643. 28. Tabata, R.; Sumida, K.; Yoshii, T.; Ohyama, K.; Shinohara, H.; Matsubayashi, Y., Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science 2014, 346, (6207), 343-346. 29. Larrainzar, E.; Gil‐Quintana, E.; Arrese‐Igor, C.; González, E. M.; Marino, D., Split-root systems applied to the study of the legume-rhizobial symbiosis: What have we learned? J Integr. Plant Biol. 2014, 56, (12), 1118-1124. 30. Kassaw, T. K.; Frugoli, J. A., Simple and efficient methods to generate split roots and grafted plants useful for long-distance signaling studies in Medicago truncatula and other small plants. Plant methods 2012, 8, (1), 1. 31. Datta, S.; Rule, A. M.; Mihalic, J. N.; Chillrud, S. N.; Bostick, B. C.; Ramos-Bonilla, J. P.; Han, I.; Polyak, L. M.; Geyh, A.; Breysse, P., Use of X-Ray Absorption Spectroscopy (XAS) to Speciate Manganese in Airborne Particulate Matter from 5 Counties Across the US. Environ. Sci. Technol. 2012, 46, 3101-3109. 32. Wang, Z.; Xie, X.; Zhao, J.; White, J. C.; Xing, B.; Liu, X.; Feng, W., Xylem-and Phloem-based Transport of CuO Nanoparticles in Maize (Zea mays L.). Environ. Sci. Technol. 2012, 46, (8), 4434-4441. 33. Epstein, E.; Bloom, A., Mineral nutrition of plants: principles and perspectives, 2nd edn. Sinauer Assoc. Inc., Sunderland, UK 2005. 34. Jones, D., Organic acids in the rhizosphere–a critical review. Plant Soil 1998, 205, (1), 25-44. 35. Dan, Y.; Ma, X.; Zhang, W.; Liu, K.; Stephan, C.; Shi, H., Single particle ICP-MS method development for the determination of plant uptake and accumulation of CeO2 nanoparticles. Anal. Bioanal. Chem. 2016, 408, (19), 5157-5167. 36. Gutiérrez-Alcalá, G.; Gotor, C.; Meyer, A. J.; Fricker, M.; Vega, J. M.; Romero, L. C., Glutathione biosynthesis in Arabidopsis trichome cells. Proc. Natl. Acad. Sci. USA 2000, 97, (20), 11108-11113. 37. Ma, Y.; Zhang, P.; Zhang, Z.; He, X.; Zhang, J.; Ding, Y.; Zhang, J.; Zheng, L.; Guo, Z.; Zhang, L., Where Does the Transformation of Precipitated Ceria Nanoparticles in Hydroponic Plants Take Place? Environ. Sci. Technol. 2015, 49, (17), 10667-10674. 38. Yin, W.; Zhou, L.; Ma, Y.; Tian, G.; Zhao, J.; Yan, L.; Zheng, X.; Zhang, P.; Yu, J.; Gu, Z., 16



414 415 416 417 418 419 420

Page 18 of 18

Phytotoxicity, Translocation, and Biotransformation of NaYF4 Upconversion Nanoparticles in a Soybean Plant. Small 2015, 11, (36), 4774-4784. 39. Li, W.; Zheng, Y.; Zhang, H.; Liu, Z.; Su, W.; Chen, S.; Liu, Y.; Zhuang, J.; Lei, B., Phytotoxicity, Uptake, and Translocation of Fluorescent Carbon Dots in Mung Bean Plants. ACS Appl. Mater. Inter. 2016, 8, (31), 19939-19945. 40. Grusak, M. A., Enhancing mineral content in plant food products. J. Am. Coll. Nutr. 2002, 21, (sup3), 178S-183S.

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