Phytotoxicity, accumulation and transport of silver nanoparticles by Arabidopsis thaliana

Nanotoxicology

Volumn 7, Issue 3, 2012, Pages 323-337

  Geisler Lee, Jane ^a   Wang, Qiang ^b   Yao, Ying ^c   Zhang, Wen ^c   Geisler, Matt ^a   Li, Kungang ^c   Huang, Ying ^c   Chen, Yongsheng ^c   Kolmakov, Andrei ^a   Ma, Xingmao ^b  

^a SOUTHERN ILLINOIS UNIVERSITY   (United States)

^b Southern Illinois University Carbondale   (United States)

^c Georgia Institute of Technology   (United States)

Author keywords

Accumulation and transport; Arabidopsis thaliana; Particle size; Phytotoxicity; Silver ions; Silver nanoparticles

Indexed keywords

CITRIC ACID; SILVER; SILVER NANOPARTICLE;

ARABIDOPSIS; ARTICLE; BIOACCUMULATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISPERSION; INTRACELLULAR TRANSPORT; NONHUMAN; PARTICLE SIZE; PHYTOTOXICITY; PLANT ROOT CAP; PLASMODESMA; PRIORITY JOURNAL; ROOT DEVELOPMENT; TRANSPORT KINETICS;

EID: 84867605571     PISSN: 17435390     EISSN: 17435404     Source Type: Journal    
DOI: 10.3109/17435390.2012.658094     Document Type: Article

References (78)

1. Abedin M, King N. 2010. Diverse evolutionary paths to cell adhesion. Trends Cell Biol 20:734-742.
2. AshaRani P, Low KMG, Hande M, Valiyaveettil S. 2009. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 3:279.
3. AshaRani PV, Lianwu Y, Gong Z, Valiyaveettil S. 2011. Comparison of the toxicity of silver, gold and platinum nanoparticles in developing zebrafish embryos. Nanotoxicology in press.
4. Asli S, Neumann PM. 2009. Colloidal suspensions of clay or titanium dioxide nanoparticles can inhibit leaf growth and transpiration via physical effects on root water transport. Plant Cell Environ 32:577-584.
5. Auffan M, Bottero JY, Chaneac C, Rose J. 2010. Inorganic manufactured nanoparticles: how their physicochemical properties influence their biological effects in aqueous environments. Nanomedicine (Lond) 5:999-1007.
6. Auffan M, Rose J, Bottero JY, Lowry GV, Jolivet JP, Wiesner MR. 2009. Towards a definition of inorganic nanoparticles from an environmental, health and safety perspective. Nat Nanotechnol 4:634-641.
7. Benn T, Westerhoff P. 2008. Nanoparticle silver released into water from commercially available sock fabrics. Environ Sci Technol 42:4133.
8. Benn TM, Cavanagh B, Hristovski K, Posner JD, Westerhoff P. 2010. The release of nanosilver from consumer products used in the home. J Environ Qual 39(6):1875-1882.
9. Bennett MD, Leitch IJ, Price HJ, Johnston JS. 2003. Comparisons with Caenorhabditis (~100 Mb) and Drosophila (~175 Mb) Using Flow Cytometry Show Genome Size in Arabidopsis to be ~157 Mb and thus ~25% Larger than the Arabidopsis Genome Initiative Estimate of ~125 Mb. Ann Bot 91:547-557.
10. Borm P, Klaessig FC, Landry TD, Moudgil B, Pauluhn J, Thomas K, et al. 2006. Research strategies for safety evaluation of nanomaterials. Part V: role of dissolution in biological fate and effects of nanoscale particles. Toxicol Sci 90:23.
11. Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, et al. 2001. Growth stage-based phenotypic analysis of arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13:1499-1510.
12. Bozzola JJ, Russell LD. 1999. Electron microscopy: principles and techniques for biologists. Boston: Jones and Bartlett Publishers.
13. Carpita N, Sabularse D, Montezinos D, Delimer D. 1979. Determination of the pore size of cell walls of living plant cells. Science 205:1144-1147.
14. Cheng Y, Yin L, Lin S, Wiesner M, Bernhardt E, Liu J. 2011. Toxicity reduction of polymer-stabilized silver nanoparticles by sunlight. J Phys Chem C 115:4425-4432.
15. Chesson A, Gardner PT, Wood TJ. 1997. Cell wall porosity and available surface area of wheat straw and wheat grain fractions. J Sci Food Agric 75:289-295.
16. Christian P, Von der Kammer F, Baalousha M, Hofmann T. 2008. Nanoparticles: structure, properties, preparation and behaviour in environmental media. Ecotoxicology 17:326-343.
17. Concenco G, Galon L. 2011. Plasmodesmata: symplastic transport of herbicides within the plant. Source: Herbicides, Theory and Applications. Soloneski S, Larramendy ML. ISBN: 978-953-307-975-2.
18. InTech. Available from: http://www.intechopen.com/articles/ show/title/plasmodesmata-symplastic-transport-of-herbicides-withinthe- plant.
19. Connors K. 1990. Chemical kinetics: the study of reaction rates in solution. Wiley-VCH.ISBN-13: 978-0471720201.
20. Cosgrove DJ. 1997. Assembly and enlargement of the primary cell wall in plants. Annu Rev Cell Dev Biol 13:171-201.
21. Cumberland SA, Lead Jr. 2009. Particle size distributions of silver nanoparticles at environmentally relevant conditions. J Chromatogr A 1216:9099-9105.
22. Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, et al. 1993. Cellular organisation of the Arabidopsis thaliana root. Development 119:71-84.
23. Du J, Huang Y-P, Xi J, Cao M-J, Ni W-S, Chen X, et al. 2008. Functional gene-mining for salt-tolerance genes with the power of Arabidopsis. Plant J 56:653-664.
24. El Badawy A, Silva RG, Morris B, Scheckel KG, Suidan MT, Tolaymat TM. 2011. Surface charge-dependent toxicity of silver nanoparticles. Environ Sci Technol 45:283-287.
25. El Badawy AM, Luxton TP, Silva RG, Scheckel KG, Suidan MT, Tolaymat TM. 2010. Impact of environmental conditions (pH, ionic strength, and electrolyte type) on the surface charge and aggregation of silver nanoparticles suspensions. Environ Sci Technol 44:1260-1266.
26. El-Temsah YS, Joner EJ. 2012. Impact of Fe and Ag nanoparticles on seed germination and differences in bioavailability during exposure in aqueous suspension and soil. Environmental Toxicology 27:42-49.
27. Fan L, Neumann PM. 2004. The spatially variable inhibition by water deficit of maize root growth correlates with altered profiles of proton flux and cell wall pH. Plant Physiol 135:2291-2300.
28. Geisler-Lee CJ, Hong Z, Verma DPS. 2002. Overexpression of the cell plate-associated dynamin-like GTPase, phragmoplastin, results in the accumulation of callose at the cell plate and arrest of plant growth. Plant Sci 163:33-42.
29. Geisler-Lee J, Geisler M, Coutinho PM, Segerman B, Nishikubo N, Takahashi J, et al. 2006. Poplar carbohydrate-active enzymes. gene identification and expression analyses. Plant Physiol 140:946-962.
30. Grant D, Nelson RT, Cannon SB, Shoemaker RC. 2010. SoyBase, the USDA-ARS soybean genetics and genomics database. Nucleic Acids Res 38:D843-D846.
31. Harris A, Bali R. 2008. On the formation and extent of uptake of silver nanoparticles by live plants. J Nanopart Res 10:691-695.
32. Haywood V, Kragler F, Lucas WJ. 2002. Plasmodesmata: pathways for protein and ribonucleoprotein signaling. Plant Cell 14:S303-S325.
33. Heinlein M, Epel BL. 2004. Macromolecular transport and signaling through plasmodesmata. Int Rev Cytol. 235:93-164.
34. Hischemöller A, Nordmann J, Ptacek P, Mummenhoff K, Haase M. 2009. In-vivo imaging of the uptake of upconversion nanoparticles by plant roots. J Biomed Nanotechnol 5:278-284.
35. Hoagland DR, Arnon DI. 1950. The Water Culture Method for Growing Plants Without Soil. Carlifornia Agricultural Experimental Station Circular. 347:1-32.
36. Horst WJ. 1995. The role of the apoplast in aluminium toxicity and resistance of higher plants: a review. Zitschrift für Pflanzenernä hrung und Bodenkunde 158:419-428.
37. Horst WJ, Wang Y, Eticha D. 2010. The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminium resistance of plants: a review. Ann Bot (Lond) 106:185-197.
38. Huala E, Dickerman AW, Garcia-Hernandez M, Weems D, Reiser L, LaFond F, et al. 2001. The Arabidopsis Information Resource (TAIR): a comprehensive database and web-based information retrieval, analysis, and visualization system for a model plant. Nucleic Acids Res 29:102-105.
39. Iijima M, Higuchi T, Barlow P. 2004. Contribution of root cap mucilage and presence of an intact root cap in maize (zea mays) to the reduction of soil mechanical impedance. Ann Bot (Lond) 94:473-477.
40. Initiative TAG. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796-815.
41. Jarvis MC, Briggs SPH, Knox JP. 2003. Intercellular adhesion and cell separation in plants. Plant Cell Environ 26:977-989.
42. Ji JH, Jung JH, Kim SS, Yoon J-U, Park JD, Choi BS, et al. 2007. Twentyeight- day inhalation toxicity study of silver nanoparticles in sprague- dawley rats. Inhal Toxicol 19:857-871.
43. Johnston HJ, Hutchison G, Christensen FM, Peters S, Hankin S, Stone V. 2010. A review of the in vivo and in vitro toxicity of silver and gold particulates: particle attributes and biological mechanisms responsible for the observed toxicity. Crit Rev Toxicol 40:328-346.
44. Jones DL, Nguyen C, Finlay RD. 2009. Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil 321:5-33.
45. Kim E, Kim S-H, Kim H-C, Lee S, Lee S, Jeong S. 2011. Growth inhibition of aquatic plant caused by silver and titanium oxide nanoparticles. Toxicol Environ Health Sci 3:1-6.
46. Kim YS, Kim JS, Cho HS, Rha DS, Kim JM, Park JD, et al. 2008. Twenty- Eight-Day oral toxicity, genotoxicity, and gender-related tissue distribution of silver nanoparticles in sprague-dawley rats. Inhal Toxicol 20:575-583.
47. Kiser MA, Westerhoff P, Benn TM, Wang Y, Pérez-Rivera J, Hristovski K. 2009. Titanium nanomaterial removal and release from wastewater treatment plants. Environ Sci Technol 43:6757-6763.
48. Kjemtrup S, Boyes DC, Christensen C, McCaskill AJ, Hylton M, Davis K. 2003. Growth stage-based phenotypic profiling of plants. Methods Mol Biol 236:427-442.
49. Kollmeier M, Dietrich P, Bauer CS, Horst WJ, Hedrich R. 2001. Aluminum activates a citrate-permeable anion channel in the aluminum-sensitive zone of the maize root apex. a comparison between an aluminum-sensitive and an aluminum-resistant cultivar. Plant Physiol 126:397-410.
50. Koornneef M, Meinke D. 2010. The development of Arabidopsis as a model plant. Plant J 61:909-921.
51. Lee WM, An YJ, Yoon H, Kweon HS. 2008. 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. Environ Toxicol Chem 27:1915-1921.
52. Liepman AH, Wightman R, Geshi N, Turner SR, Scheller HV. 2010. Arabidopsis - a powerful model system for plant cell wall research. Plant J 61:1107-1121.
53. Lin D, Xing B. 2008. Root uptake and phytotoxicity of ZnO nanoparticles. Environ Sci Technol 42:5580-5585.
54. Lucas WJ, Ham B-K, Kim J-Y. 2009. Plasmodesmata - bridging the gap between neighboring plant cells. Trends Cell Biol 19:495-503.
55. Lucas WJ, Lee J-Y. 2004. Plasmodesmata as a supracellular control network in plants. Nat Rev Mol Cell Biol 5:712-726.
56. Ma X, Geisler-Lee J, Yang D, Kolmakov A. 2010. Interactions between engineered nanoparticles (ENPs) and plants: phytotoxicity, uptake and accumulation. Sci Total Environ 408:3053-3061.
57. Ma Y, He X, Zhang P, Zhang Z, Guo Z, Tai R, et al. 2011. Phytotoxicity and biotransformation of La2O3 nanoparticles in a terrestrial plant cucumber (Cucumis sativus). Nanotoxicology in press.
58. McCourt P, Benning C. 2010. Arabidopsis: a rich harvest 10 years after completion of the genome sequence. Plant J 61:905-908.
59. Meyer DE, Curran MA, Gonzalez MA. 2009. An examination of existing data for the industrial manufacture and use of nanocomponents and their role in the life cycle impact of nanoproducts. Environ Sci Technol 43:1256-1263.
60. Reynolds ES. 1963. The use of lead citrate at high ph as an electronopaque stain in electron microscopy. J Cell Biol 17:208-212.
61. Rhee SY, Beavis W, Berardini TZ, Chen G, Dixon D, Doyle A, et al. 2003. The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nucleic Acids Res 31:224-228.
62. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, et al. 2009. The B73 Maize genome: complexity, diversity, and dynamics. Science 326:1112-1115.
63. Schranz ME, Song B-H, Windsor AJ, Mitchell-Olds T. 2007. Comparative genomics in the Brassicaceae: a family-wide perspective. Curr Opin Plant Biol 10:168-175.
64. Shultz JL, Kurunam D, Shopinski K, Iqbal MJ, Kazi S, Zobrist K, et al. 2006. The Soybean Genome Database (SoyGD): a browser for display of duplicated, polyploid, regions and sequence tagged sites on the integrated physical and genetic maps of Glycine max. Nucleic Acids Res 34:D758-D765.
65. Sopjani M, Foller M, Haendeler J, Gotz F, Lang F. 2009. Silver ioninduced suicidal erythrocyte death. J Appl Toxicol 29:531.
66. Sørensen SPL. 1901. Enzymstudien. II: Mitteilung. Über die Messung und die bedeutung der wasserstoffionenkoncentration bei enzymatischen prozessen. Biochemische Zeitschrift (in German) 21:131-304.
67. Stampoulis D, Sinha SK, White JC. 2009. Assay-dependent phytotoxicity of nanoparticles to plants. Environ Sci Technol 43:9473-9479.
68. Tolaymat TM, El Badawy AM, Genaidy A, Scheckel KG, Luxton TP, Suidan M. 2010. An evidence-based environmental perspective of manufactured silver nanoparticle in syntheses and applications: a systematic review and critical appraisal of peer-reviewed scientific papers. Sci Total Environ 408:999-1006.
69. Wen F, VanEtten HD, Tsaprailis G, Hawes MC. 2007. Extracellular proteins in pea root tip and border cell exudates. Plant Physiol 143:773-783.
70. Wiechers JW, Musee N. 2010. Engineered inorganic nanoparticles and cosmetics: facts, issues, knowledge gaps and challenges. J Biomed Nanotechnol 6:408-431.
71. Wienkoop S, Baginsky S, Weckwerth W. 2010. Arabidopsis thaliana as a model organism for plant proteome research. J Proteomics 73:2239- 2248.
72. Wijnhoven SWP, Peijnenburg WJGM, Herberts CA, Hagens WI, Oomen AG, Heugens EHW, et al. 2009. Nano-silver - a review of available data and knowledge gaps in human and environmental risk assessment. Nanotoxicology 3:109-138.
73. YangJ,ZhangL, Li Y,YOUJ, Jiang F,WuP, et al. 2006. Citrate transporters play a critical role in aluminium-stimulated citrate efflux in rice bean (Vigna umbellata) roots. Ann Bot (Lond) 97:579-584.
74. Yin L, Cheng Y, Espinasse B, Colman BP, Auffan M, Wiesner M, et al. 2011. More than the Ions: the effects of silver nanoparticles on lolium multiflorum. Environ Sci Technol 45:2360-2367.
75. Yuan JS, Galbraith DW, Dai SY, Griffin P, Stewart CN Jr. 2008. Plant systems biology comes of age. Trends Plant Sci 13:165-171.
76. Zachariadis GA, Sahanidou E. 2009. Multi-element method for determination of trace elements in sunscreens by ICP-AES. J Pharm Biomed Anal 50:342-348.
77. Zhang W, Yao Y, Sullivan N, Chen Y. 2011. Modeling the primary size effects of citrate-coated silver nanoparticles on their ion release kinetics. Environ Sci Technol.45:4422-8.
78. Zhu H, Han J, Xiao JQ, Jin Y. 2008. Uptake, translocation, and accumulation of manufactured iron oxide nanoparticles by pumpkin plants. J Environ Monit 10:713-717.