Effect of CeO2 nanomaterial surface functional groups on tissue and subcellular distribution of Ce in tomato (Solanum lycopersicum)

Li, Jieran; Tappero, Ryan V.; Acerbo, Alvin S.; Yan, Hanfei; Chu, Yong; Lowry, Gregory V.; Unrine, Jason M.

doi:10.1039/C8EN01287C

Title: Effect of CeO₂ nanomaterial surface functional groups on tissue and subcellular distribution of Ce in tomato (Solanum lycopersicum)

Journal Article · Mon Dec 10 00:00:00 EST 2018 · Environmental Science: Nano

DOI:https://doi.org/10.1039/C8EN01287C· OSTI ID:1506633

Li, Jieran ^[1]; Tappero, Ryan V. ^[2]; Acerbo, Alvin S. ^[3]; Yan, Hanfei ^[2]; Chu, Yong ^[2];

^[4];

^[1]

Univ. of Kentucky, Lexington, KY (United States)
Brookhaven National Lab. (BNL), Upton, NY (United States)
Univ. of Chicago, IL (United States)
Carnegie Mellon Univ., Pittsburgh, PA (United States)

Using recent advances in X-ray microscopy, this study aimed to elucidate mechanisms of uptake, subcellular distribution, and translocation of functionalized CeO₂ MNM (manufactured nanomaterials), having different charges, by tomato plants (Solanum lycopersicum cv Micro-Tom). As a result, we found that plant growth and Ce concentration in tissues were functions of surface charge and exposure concentration with root to shoot translocation being much greater for negatively charged CeO₂ than positive or neutral CeO₂. Mechanisms of entry into roots and translocation within plants were examined using X-ray nano- and microprobes. There were dramatic differences in the tissue and subcellular distributions of Ce in plant roots exposed to dextran-coated CeO₂ nanoparticles conjugated with positive, neutral and negative functional groups. Positively charged CeO₂ remained mainly bound to the epidermis of the root with little present in the apoplast or cytoplasm. Negatively charged CeO₂ was found in the cytoplasm throughout the root cross section, and negatively charged CeO₂ was found within the apoplast in the cortex and both the apoplast and the cytoplasm in the vasculature. Neutral CeO₂ likely entered through the gaps between epidermal cells being sloughed off during root growth and penetrated deeper into the interior of the roots (vasculature) via a combination of apoplastic and symplastic transport. Evidence of symplastic Ce transport was observed with the neutrally and negatively charged particles. We observed evidence of endocytosis as the mechanism for entry into the symplast allowing for entry into the xylem. Finally, this study provides critical information on how particle surface chemistry influences the biodistribution and cellular localization of nanomaterials in plants and is to date the highest resolution X-ray imaging of nanomaterials in plant cells.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0012704; FG02-92ER14244; AC02-06CH11357

OSTI ID:: 1506633

Alternate ID(s):: OSTI ID: 1485187

Report Number(s):: BNL-211517-2019-JAAM; ESNNA4

Journal Information:: Environmental Science: Nano, Vol. 6, Issue 1; ISSN 2051-8153

Publisher:: Royal Society of ChemistryCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 31 works

Citation information provided by
Web of Science

References (49)

ATHENA , ARTEMIS , HEPHAESTUS : data analysis for X-ray absorption spectroscopy using IFEFFIT Ravel, B.; Newville, M. Journal of Synchrotron Radiation, Vol. 12, Issue 4 https://doi.org/10.1107/S0909049505012719	journal	June 2005
Synthesis of Biocompatible Dextran-Coated Nanoceria with pH-Dependent Antioxidant Properties Perez, J. Manuel; Asati, Atul; Nath, Sudip Small, Vol. 4, Issue 5 https://doi.org/10.1002/smll.200700824	journal	May 2008
Toxicity, Uptake, and Translocation of Engineered Nanomaterials in Vascular plants Miralles, Pola; Church, Tamara L.; Harris, Andrew T. Environmental Science & Technology, Vol. 46, Issue 17 https://doi.org/10.1021/es202995d	journal	August 2012
Effects of Particle Size on Chemical Speciation and Bioavailability of Copper to Earthworms () Exposed to Copper Nanoparticles Unrine, Jason M.; Tsyusko, Olga V.; Hunyadi, Simona E. Journal of Environment Quality, Vol. 39, Issue 6 https://doi.org/10.2134/jeq2009.0387	journal	January 2010
Phytotoxicity, accumulation and transport of silver nanoparticles by Arabidopsis thaliana Geisler-Lee, Jane; Wang, Qiang; Yao, Ying Nanotoxicology, Vol. 7, Issue 3 https://doi.org/10.3109/17435390.2012.658094	journal	January 2012
The utilization of ceria in industrial catalysis Trovarelli, Alessandro; de Leitenburg, Carla; Boaro, Marta Catalysis Today, Vol. 50, Issue 2 https://doi.org/10.1016/S0920-5861(98)00515-X	journal	April 1999
Speciation Matters: Bioavailability of Silver and Silver Sulfide Nanoparticles to Alfalfa ( Medicago sativa ) Stegemeier, John P.; Schwab, Fabienne; Colman, Benjamin P. Environmental Science & Technology, Vol. 49, Issue 14 https://doi.org/10.1021/acs.est.5b01147	journal	July 2015
Uptake and cellular distribution, in four plant species, of fluorescently labeled mesoporous silica nanoparticles Sun, Dequan; Hussain, Hashmath I.; Yi, Zhifeng Plant Cell Reports, Vol. 33, Issue 8 https://doi.org/10.1007/s00299-014-1624-5	journal	May 2014
Uptake, Translocation, and Transformation of Quantum Dots with Cationic versus Anionic Coatings by Populus deltoides × nigra Cuttings Wang, Jing; Yang, Yu; Zhu, Huiguang Environmental Science & Technology, Vol. 48, Issue 12 https://doi.org/10.1021/es501425r	journal	May 2014
Toxicity and Bioavailability of Copper Nanoparticles to the Terrestrial Plants mung bean (Phaseolus Radiatus) and Wheat (Triticum Aestivum): Plant agar test for Water-Insoluble Nanoparticles Lee, Woo-Mi; An, Youn-Joo; Yoon, Hyeon Environmental Toxicology and Chemistry, Vol. 27, Issue 9 https://doi.org/10.1897/07-481.1	journal	January 2008
Toxicity of Gold Nanoparticles Functionalized with Cationic and Anionic Side Chains Goodman, Catherine M.; McCusker, Catherine D.; Yilmaz, Tuna Bioconjugate Chemistry, Vol. 15, Issue 4 https://doi.org/10.1021/bc049951i	journal	July 2004
Phytotoxicity and biotransformation of La ₂ O ₃ nanoparticles in a terrestrial plant cucumber ( Cucumis sativus ) Ma, Yuhui; He, Xiao; Zhang, Peng Nanotoxicology, Vol. 5, Issue 4 https://doi.org/10.3109/17435390.2010.545487	journal	September 2010
Novel Method for the Direct Visualization of in Vivo Nanomaterials and Chemical Interactions in Plants Wild, Edward; Jones, Kevin C. Environmental Science & Technology, Vol. 43, Issue 14 https://doi.org/10.1021/es900065h	journal	July 2009
Plant nanotoxicology Dietz, Karl-Josef; Herth, Simone Trends in Plant Science, Vol. 16, Issue 11 https://doi.org/10.1016/j.tplants.2011.08.003	journal	November 2011
Phytotoxicity of nanoparticles: Inhibition of seed germination and root growth Lin, Daohui; Xing, Baoshan Environmental Pollution, Vol. 150, Issue 2 https://doi.org/10.1016/j.envpol.2007.01.016	journal	November 2007
Large-Scale Synthesis of Water Dispersible Ceria Nanocrystals by a Simple Sol–Gel Process and Their Use as a Chemical Mechanical Planarization Slurry Yu, Taekyung; Park, Yong Il; Kang, Min-Cheol European Journal of Inorganic Chemistry, Vol. 2008, Issue 6 https://doi.org/10.1002/ejic.200700979	journal	February 2008
Nanoparticulate material delivery to plants Nair, Remya; Varghese, Saino Hanna; Nair, Baiju G. Plant Science, Vol. 179, Issue 3 https://doi.org/10.1016/j.plantsci.2010.04.012	journal	September 2010
Investigation of gold nanoparticles uptake and their tissue level distribution in rice plants by laser ablation-inductively coupled-mass spectrometry Koelmel, Jeremy; Leland, Thomas; Wang, Huanhua Environmental Pollution, Vol. 174 https://doi.org/10.1016/j.envpol.2012.11.026	journal	March 2013
Nanoparticle penetration and transport in living pumpkin plants: in situ subcellular identification Corredor, Eduardo; Testillano, Pilar S.; Coronado, María-José BMC Plant Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2229-9-45	journal	January 2009
Fate and Effects of CeO ₂ Nanoparticles in Aquatic Ecotoxicity Tests Hoecke, Karen Van; Quik, Joris T. K.; Mankiewicz-Boczek, Joanna Environmental Science & Technology, Vol. 43, Issue 12 https://doi.org/10.1021/es9002444	journal	June 2009
Pharmacological potential of cerium oxide nanoparticles Celardo, Ivana; Pedersen, Jens Z.; Traversa, Enrico Nanoscale, Vol. 3, Issue 4 https://doi.org/10.1039/c0nr00875c	journal	January 2011
Transformation of ceria nanoparticles in cucumber plants is influenced by phosphate Rui, Yukui; Zhang, Peng; Zhang, Yanbei Environmental Pollution, Vol. 198 https://doi.org/10.1016/j.envpol.2014.12.017	journal	March 2015
The Evolution of the Protein Corona around Nanoparticles: A Test Study Lundqvist, Martin; Stigler, Johannes; Cedervall, Tommy ACS Nano, Vol. 5, Issue 9 https://doi.org/10.1021/nn202458g	journal	August 2011
Surface-Charge-Dependent Cell Localization and Cytotoxicity of Cerium Oxide Nanoparticles Asati, Atul; Santra, Santimukul; Kaittanis, Charalambos ACS Nano, Vol. 4, Issue 9 https://doi.org/10.1021/nn100816s	journal	August 2010
Protein Corona Fingerprinting Predicts the Cellular Interaction of Gold and Silver Nanoparticles Walkey, Carl D.; Olsen, Jonathan B.; Song, Fayi ACS Nano, Vol. 8, Issue 3 https://doi.org/10.1021/nn406018q	journal	February 2014
Nanotechnology: A New Opportunity in Plant Sciences Wang, Peng; Lombi, Enzo; Zhao, Fang-Jie Trends in Plant Science, Vol. 21, Issue 8 https://doi.org/10.1016/j.tplants.2016.04.005	journal	August 2016
Root uptake and phytotoxicity of nanosized molybdenum octahedral clusters Aubert, Tangi; Burel, Agnès; Esnault, Marie-Andrée Journal of Hazardous Materials, Vol. 219-220 https://doi.org/10.1016/j.jhazmat.2012.03.058	journal	June 2012
Nanomaterials in the Environment: Behavior, Fate, Bioavailability, and Effects Klaine, Stephen J.; Alvarez, Pedro J. J.; Batley, Graeme E. Environmental Toxicology and Chemistry, Vol. 27, Issue 9 https://doi.org/10.1897/08-090.1	journal	January 2008
Evidence for Biomagnification of Gold Nanoparticles within a Terrestrial Food Chain Judy, Jonathan D.; Unrine, Jason M.; Bertsch, Paul M. Environmental Science & Technology, Vol. 45, Issue 2 https://doi.org/10.1021/es103031a	journal	January 2011
Root Uptake and Phytotoxicity of ZnO Nanoparticles Lin, Daohui; Xing, Baoshan Environmental Science & Technology, Vol. 42, Issue 15 https://doi.org/10.1021/es800422x	journal	August 2008
Impact of Surface Charge on Cerium Oxide Nanoparticle Uptake and Translocation by Wheat ( Triticum aestivum ) Spielman-Sun, Eleanor; Lombi, Enzo; Donner, Erica Environmental Science & Technology, Vol. 51, Issue 13 https://doi.org/10.1021/acs.est.7b00813	journal	June 2017
Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis Rejman, Joanna; Oberle, Volker; Zuhorn, Inge S. Biochemical Journal, Vol. 377, Issue 1 https://doi.org/10.1042/bj20031253	journal	January 2004
Cytotoxicity of CeO ₂ Nanoparticles for Escherichia coli. Physico-Chemical Insight of the Cytotoxicity Mechanism Thill, Antoine; Zeyons, Ophélie; Spalla, Olivier Environmental Science & Technology, Vol. 40, Issue 19 https://doi.org/10.1021/es060999b	journal	October 2006
Nano-CeO ₂ Exhibits Adverse Effects at Environmental Relevant Concentrations Zhang, Haifeng; He, Xiao; Zhang, Zhiyong Environmental Science & Technology, Vol. 45, Issue 8 https://doi.org/10.1021/es103309n	journal	April 2011
Application of rare-earth elements in the agriculture of China and its environmental behavior in soil Pang, Xin; Li, Decheng; Peng, An Environmental Science and Pollution Research, Vol. 9, Issue 2 https://doi.org/10.1007/BF02987462	journal	March 2002
No Evidence for Cerium Dioxide Nanoparticle Translocation in Maize Plants Birbaum, Karin; Brogioli, Robert; Schellenberg, Maya Environmental Science & Technology, Vol. 44, Issue 22 https://doi.org/10.1021/es101685f	journal	November 2010
Preparation and characterization challenges to understanding environmental and biological impacts of ceria nanoparticles: Environmental and biological impacts of nanoparticles Karakoti, A. S.; Munusamy, P.; Hostetler, K. Surface and Interface Analysis, Vol. 44, Issue 8 https://doi.org/10.1002/sia.5006	journal	April 2012
Effect of Cerium Oxide Nanoparticles on Rice: A Study Involving the Antioxidant Defense System and In Vivo Fluorescence Imaging Rico, Cyren M.; Hong, Jie; Morales, Maria Isabel Environmental Science & Technology, Vol. 47, Issue 11 https://doi.org/10.1021/es401032m	journal	May 2013
Influence of Natural Organic Matter and Surface Charge on the Toxicity and Bioaccumulation of Functionalized Ceria Nanoparticles in Caenorhabditis elegans Collin, Blanche; Oostveen, Emily; Tsyusko, Olga V. Environmental Science & Technology, Vol. 48, Issue 2 https://doi.org/10.1021/es404503c	journal	January 2014
Design and performance of an X-ray scanning microscope at the Hard X-ray Nanoprobe beamline of NSLS-II Nazaretski, E.; Yan, H.; Lauer, K. Journal of Synchrotron Radiation, Vol. 24, Issue 6 https://doi.org/10.1107/S1600577517011183	journal	October 2017
In Vivo Processing of Ceria Nanoparticles inside Liver: Impact on Free-Radical Scavenging Activity and Oxidative Stress Graham, Uschi M.; Tseng, Michael T.; Jasinski, Jacek B. ChemPlusChem, Vol. 79, Issue 8 https://doi.org/10.1002/cplu.201402080	journal	June 2014
Biotransformation of Ceria Nanoparticles in Cucumber Plants Zhang, Peng; Ma, Yuhui; Zhang, Zhiyong ACS Nano, Vol. 6, Issue 11 https://doi.org/10.1021/nn303543n	journal	October 2012
Untangling the biological effects of cerium oxide nanoparticles: the role of surface valence states Pulido-Reyes, Gerardo; Rodea-Palomares, Ismael; Das, Soumen Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep15613	journal	October 2015
11 nm hard X-ray focus from a large-aperture multilayer Laue lens Huang, Xiaojing; Yan, Hanfei; Nazaretski, Evgeny Scientific Reports, Vol. 3, Issue 1 https://doi.org/10.1038/srep03562	journal	December 2013
Mesoporous silica nanoparticles deliver DNA and chemicals into plants Torney, François; Trewyn, Brian G.; Lin, Victor S. -Y. Nature Nanotechnology, Vol. 2, Issue 5 https://doi.org/10.1038/nnano.2007.108	journal	April 2007
Effects of rare earth oxide nanoparticles on root elongation of plants Ma, Yuhui; Kuang, Linglin; He, Xiao Chemosphere, Vol. 78, Issue 3 https://doi.org/10.1016/j.chemosphere.2009.10.050	journal	January 2010
Effects of surface ligands on the uptake and transport of gold nanoparticles in rice and tomato Li, Hongying; Ye, Xinxin; Guo, Xisheng Journal of Hazardous Materials, Vol. 314 https://doi.org/10.1016/j.jhazmat.2016.04.043	journal	August 2016
No evidence for cerium dioxide nanoparticle translocation in maize plants K., Birbaum,; R., Brogioli,; M., Schellenberg, American Chemical Society https://doi.org/10.5167/uzh-39948	text	January 2010
Application of rare-earth elements in the agriculture of china and its environmental behavior in soil Pang, Xin; Li, Decheng; Peng, An Journal of Soils and Sediments, Vol. 1, Issue 2 https://doi.org/10.1007/bf02987718	journal	June 2001

Cited By (2)

Impact of nanoparticle surface charge and phosphate on the uptake of coexisting cerium oxide nanoparticles and cadmium by soybean ( Glycine max. (L.) merr .) Sharifan, Hamidreza; Wang, Xiaoxuan; Ma, Xingmao International Journal of Phytoremediation, Vol. 22, Issue 3 https://doi.org/10.1080/15226514.2019.1658713	journal	August 2019
Impact of nanoparticle surface charge and phosphate on the uptake of coexisting cerium oxide nanoparticles and cadmium by soybean (Glycine max. (L.) merr.) Sharifan, Hamidreza; Wang, Xiaoxuan; Ma, Xingmao Taylor & Francis https://doi.org/10.6084/m9.figshare.9752360	text	January 2019

Similar Records

Effect of CeO₂ nanomaterial surface functional groups on tissue and subcellular distribution of Ce in tomato (Solanum lycopersicum)

Journal Article · Tue Jan 01 00:00:00 EST 2019 · Environmental Science: Nano · OSTI ID:1506633

Li, Jieran; Tappero, Ryan V.; Acerbo, Alvin S.; +4 more

Nanoparticle surface charge influences translocation and leaf distribution in vascular plants with contrasting anatomy

Journal Article · Mon Jul 08 00:00:00 EDT 2019 · Environmental Science: Nano · OSTI ID:1506633

Spielman-Sun, Eleanor; Avellan, Astrid; Bland, Garret D.; +5 more

Speciation Matters: Bioavailability of Silver and Silver Sulfide Nanoparticles to Alfalfa (Medicago sativa)

Journal Article · Wed Jun 24 00:00:00 EDT 2015 · Environmental Science and Technology · OSTI ID:1506633

Stegemeier, John P.; Schwab, Fabienne; Colman, Benjamin P.; +6 more

Related Subjects

54 ENVIRONMENTAL SCIENCES
36 MATERIALS SCIENCE

Title: Effect of CeO2 nanomaterial surface functional groups on tissue and subcellular distribution of Ce in tomato (Solanum lycopersicum)

Citation Formats

References (49)

Cited By (2)

Similar Records

Related Subjects

Title: Effect of CeO₂ nanomaterial surface functional groups on tissue and subcellular distribution of Ce in tomato (Solanum lycopersicum)