Interactions between nanoparticles and plants: Phytotoxicity and defense mechanisms

Journal of Plant Interactions

Volumn 12, Issue 1, 2017, Pages 158-169

  Yanga, Jie ^a   Cao, Weidong ^b   Rui, Yukui ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Antioxidant defense system; NPs; Phytotoxicity; Plant; Risks

Indexed keywords

EID: 85026396900     PISSN: 17429145     EISSN: 17429153     Source Type: Journal    
DOI: 10.1080/17429145.2017.1310944     Document Type: Review

References (127)

1. 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.
2. Batley GE, Kirby JK, McLaughlin MJ. 2013. Fate and risks of nanomaterials in aquatic and terrestrial environments. Acc Chem Res. 46:854-862.
3. Bleecker AB, Kende H. 2000. Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol. 16:1-18.
4. 3 toxicity in pumpkin: a physiological and molecular response. Nanotoxicology. 10:1243-1253.
5. Cheng Y, Song C. 2006. Hydrogen peroxide homeostasis and signaling in plant cells. Sci China. Ser C Life Sci/Chinese Acad Sci. 49:1-11.
6. Cui D, Zhang P, Ma Y, He X, Li Y, Zhang J, Zhao Y, Zhang Z. 2014. Effect of cerium oxide nanoparticles on asparagus lettuce cultured in an agar medium. Environ Sci Nano. 1:459-465.
7. Demir E, Kaya N, Kaya B. 2014. Genotoxic effects of zinc oxide and titanium dioxide nanoparticles on root meristem cells of Allium cepa by comet assay. Turk J Biol. 38:31-39.
8. Dimkpa CO, McLean JE, Latta DE, Manangón E, Britt DW, Johnson WP, Boyanov MI, Anderson AJ. 2012. Cuo and ZnO nanoparticles: phytotoxicity, metal speciation, and induction of oxidative stress in sand-grown wheat. J Nanopart Res. 14:1-15.
9. Dimkpa CO, McLean JE, Martineau N, Britt DW, Haverkamp R, Anderson AJ. 2013. Silver nanoparticles disrupt wheat (Triticum aestivum L.) growth in a sand matrix. Environ Sci Technol. 47:1082-1090.
10. Diplock AT, Machlin L, Packer L, Pryor W. 1989. Vitamin E: biochemistry and health implications. New York: The New York Academy of Sciences.
11. 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. Environ Toxicol. 27:42-49.
12. Faisal M, Saquib Q, Alatar AA, Al-Khedhairy AA, Hegazy AK, Musarrat J. 2013. Phytotoxic hazards of NiO-nanoparticles in tomato: a study on mechanism of cell death. J Hazard Mater. 250-251:318-332.
13. Feizi H, Kamali M, Jafari L, Moghaddam PR. 2013. Phytotoxicity and stimulatory impacts of nanosized and bulk titanium dioxide on fennel (Foeniculum vulgare Mill). Chemosphere. 91:506-511.
14. Foyer CH, Halliwell B. 1976. The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta. 133:21-25.
15. Foyer CH, Lopez-Delgado H, Dat JF, Scott IM. 1997. Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol Plant. 100:241-254.
16. Foyer CH, Noctor G. 2003. Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant. 119:355-364.
17. Freinbichler W, Colivicchi MA, Stefanini C, Bianchi L, Ballini C, Misini B, Weinberger P, Linert W, Varešlija D, Tipton KF, Corte LD. 2011. Highly reactive oxygen species: detection, formation, and possible functions. Cell Mol Life Sci. 68:2067-2079.
18. Fridovich I. 1989. Superoxide dismutases. An adaptation to a paramagnetic gas. J Biol Chem. 264:7761-7764.
19. Garg N, Manchanda G. 2009. ROS generation in plants: boon or bane? Plant Biosyst. 143:81-96.
20. Ghisla S, Massey V. 1989. Mechanisms of flavoprotein-catalyzed reactions. Eur J Biochem. 181:1-17.
21. 2) nanoparticles at two trophic levels: plant and human lymphocytes. Chemosphere. 81:1253-1262.
22. Ghosh M, Bhadra S, Adegoke A, Bandyopadhyay M, Mukherjee A. 2015. MWCNT uptake in Allium cepa root cells induces cytotoxic and genotoxic responses and results in DNA hyper-methylation. Mutat Res/ Fundam Mol Mech Mutagen. 774:49-58.
23. Gill SS, Tuteja N. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem. 48:909-930.
24. Gottschalk F, Lassen C, Kjoelholt J, Christensen F, Nowack B. 2015. Modeling flows and concentrations of nine engineered nanomaterials in the Danish environment. Int J Environ Res Public Health. 12:5581-5602.
25. 2, ZnO, Ag, CNT, fullerenes) for different regions. Environ Sci Technol. 43:9216-9222.
26. Griffitt RJ, Weil R, Hyndman KA, Denslow ND, Powers K, Taylor D, Barber DS. 2007. Exposure to copper nanoparticles causes gill injury and acute lethality in zebrafish (Danio rerio). Environ Sci Technol. 41:8178-8186.
27. 3). Environ Sci Pollut Res. 22:17716-17723.
28. 2 nanoparticles on lettuce cultured in the potting soil environment. PloS one. 10:e0134261.
29. Halliwell B, Gutteridge JM. 2015. Free radicals in biology and medicine. USA: Oxford University Press.
30. Hancock J, Desikan R, Harrison J, Bright J, Hooley R, Neill S. 2006. Doing the unexpected: proteins involved in hydrogen peroxide perception. J Exp Bot. 57:1711-1718.
31. Hao Y, Yu F, Lv R, Ma C, Zhang Z, Rui Y, Liu L, Cao W, Xing B, Choi J. 2016. Carbon nanotubes filled with different ferromagnetic alloys affect the growth and development of rice seedlings by changing the C:N ratio and plant hormones concentrations. PloS One. 11: e0157264.
32. Hawthorne J, Musante C, Sinha SK, White JC. 2012. Accumulation and phytotoxicity of engineered nanoparticles to Cucurbita pepo. Int J Phytoremediation. 14:429-442.
33. 2 nanoparticles on cucumber (Cucumis sativus) plants. Environ Sci Technol. 48:4376-4385.
34. 2 and CuO alter cucumber (Cucumis sativus) fruit quality. Sci Total Environ. 563-564:904-911.
35. 2 on photochemical reaction of chloroplasts of spinach. Biol Trace Elem Res. 105:269-280.
36. 3, ZnO, and Ag nanoparticles stress. J Hazard Mater. 304:291-305.
37. Imlay JA, Linn S. 1988. DNA damage and oxygen radical toxicity. Sci (Washington). 240:1302-1309.
38. Ivanov B, Khorobrykh S. 2003. Participation of photosynthetic electron transport in production and scavenging of reactive oxygen species. Antioxid Redox Signal. 5:43-53.
39. Joo JH, Bae YS, Lee JS. 2001. Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol. 126:1055-1060.
40. Khodakovskaya MV, Kim BS, Kim JN, Alimohammadi M, Dervishi E, Mustafa T, Cernigla CE. 2013. Carbon nanotubes as plant growth regulators: effects on tomato growth, reproductive system, and soil microbial community. Small. 9:115-123.
41. Khodakovskaya MV, de Silva K, Biris AS, Dervishi E, Villagarcia H. 2012. Carbon nanotubes induce growth enhancement of tobacco cells. ACS Nano. 6:2128-2135.
42. Kirchner C, Liedl T, Kudera S, Pellegrino T, Muñoz Javier A, Gaub HE, Stölzle S, Fertig N, Parak WJ. 2005. Cytotoxicity of colloidal CdSe and CdSe/ZnS nanoparticles. Nano Lett. 5:331-338.
43. 2. Ecotoxicol Environ Saf. 74:85-92.
44. Kumari M, Khan SS, Pakrashi S, Mukherjee A, Chandrasekaran N. 2011. Cytogenetic and genotoxic effects of zinc oxide nanoparticles on root cells of Allium cepa. J Hazard Mater. 190:613-621.
45. Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI. 2003. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 22:2623-2633.
46. Le Van N, Ma C, Rui Y, Liu S, Li X, Xing B, Liu L. 2015. Phytotoxic mechanism of nanoparticles: destruction of chloroplasts and vascular bundles and alteration of nutrient absorption. Sci Rep. 5:116-118.
47. Le Van N, Rui Y, Cao W, Shang J, Liu S, Nguyen Quang T, Liu L. 2016. Toxicity and bio-effects of CuO nanoparticles on transgenic Ipt-cotton. J Plant Interact. 11:108-116.
48. 2 nanoparticles in Bt-transgenic cotton. J Nanobiotechnol. 12:50.
49. 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.
50. Lee CW, Mahendra S, Zodrow K, Li D, Tsai YC, Braam J, Alvarez PJ. 2010. Developmental phytotoxicity of metal oxide nanoparticles to Arabidopsis thaliana. Environ Toxicol Chem. 29:669-675.
51. Li W, Zheng Y, Zhang H, Liu Z, Su W, Chen S, Liu Y, Zhuang J, Lei B. 2016. Phytotoxicity, uptake, and translocation of fluorescent carbon dots in mung bean plants. ACS Appl Mater Interfaces. 8:19939-19945.
52. Liman R. 2013. Genotoxic effects of bismuth (III) oxide nanoparticles by allium and comet assay. Chemosphere. 93:269-273.
53. Lin S, Reppert J, Hu Q, Hudson JS, Reid ML, Ratnikova TA, Rao AM, Luo H, Ke PC. 2009. Uptake, translocation, and transmission of carbon nanomaterials in rice plants. Small. 5:1128-1132.
54. Lin D, Xing B. 2008. Root uptake and phytotoxicity of ZnO nanoparticles. Environ Technol. 42:5580-5585.
55. 2 nanoparticles on soybean (Glycine max) plants. Environ Sci Technol. 44:7315-7320.
56. 2 nanoparticles and assessment of their differential toxicity in four edible plant species. J Agric Food Chem. 58:3689-3693.
57. Lu C, Zhang C, Wen J, Wu G, Tao M. 2001. Research of the effect of nanometer materials on germination and growth enhancement of Glycine max and its mechanism. Soybean Sci. 21:168-171.
58. Ma C, Chhikara S, Xing B, Musante C, White JC, Dhankher OP. 2013. Physiological and molecular response of Arabidopsis thaliana (L.) to nanoparticle cerium and indium oxide exposure. ACS Sustain Chem Eng. 1:768-778.
59. Ma Y, Kuang L, He X, Bai W, Ding Y, Zhang Z, Zhao Y, Chai Z. 2010. Effects of rare earth oxide nanoparticles on root elongation of plants. Chemosphere. 78:273-279.
60. 3 nanoparticles. Environ Sci Nano. 3:1369-1379.
61. Ma X, Wang Q, Rossi L, Zhang W. 2015. Cerium oxide nanoparticles and bulk cerium oxide leading to different physiological and biochemical responses in Brassica rapa. Environ Sci Technol. 50:6793-6802.
62. Ma C, White JC, Dhankher OP, Xing B. 2015. Metal-based nanotoxicity and detoxification pathways in higher plants. Environ Sci Technol. 49:7109-7122.
63. Ma H, Williams PL, Diamond SA. 2013. Ecotoxicity of manufactured ZnO nanoparticles - a review. Environ Pollut. 172:76-85.
64. Ma Y, Zhang P, Zhang Z, He X, Li Y, Zhang J, Zheng L, Chu S, Yang K, Zhao Y, Chai Z. 2015. Origin of the different phytotoxicity and biotransformation of cerium and lanthanum oxide nanoparticles in cucumber. Nanotoxicology. 9:262-270.
65. Ma Y, Zhang P, Zhang Z, He X, Zhang J, Ding Y, Zhang J, Zheng L, Guo Z, Zhang L, et al. 2015. Where does the transformation of precipitated ceria nanoparticles in hydroponic plants take place? Environ Sci Technol. 49:10667-10674.
66. Majumdar S, Peralta-Videa JR, Bandyopadhyay S, Castillo-Michel H, Hernandez-Viezcas JA, Sahi S, Gardea-Torresdey JL. 2014. Exposure of cerium oxide nanoparticles to kidney bean shows disturbance in the plant defense mechanisms. J Hazard Mater. 278:279-287.
67. Majumdar S, Peralta-Videa JR, Trujillo-Reyes J, Sun Y, Barrios AC, Niu G, Flores-Margez JP, Gardea-Torresdey JL. 2016. Soil organic matter influences cerium translocation and physiological processes in kidney bean plants exposed to cerium oxide nanoparticles. Sci Total Environ. 569-570:201-211.
68. McKee MS, Filser J. 2016. Impacts of metal-based engineered nanomaterials on soil communities. Environ Sci Nano. 3:506-533.
69. Meriga B, Reddy BK, Rao KR, Reddy LA, Kishor PBK. 2004. Aluminium-induced production of oxygen radicals, lipid peroxidation and DNA damage in seedlings of rice (Oryza sativa). J Plant Physiol. 161:63-68.
70. Mirzajani F, Askari H, Hamzelou S, Schober Y, Römpp A, Ghassempour A, Spengler B. 2014. Proteomics study of silver nanoparticles toxicity on Oryza sativa L. Ecotoxicol Environ Saf. 108:335-339.
71. Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7:405-410.
72. Møller IM, Kristensen BK. 2004. Protein oxidation in plant mitochondria as a stress indicator. Photochem Photobiol Sci. 3:730-735.
73. 2 in the execution of hypersensitive cell death in tobacco leaves. Plant Physiol. 138:1516-1526.
74. Nel A, Xia T, Mädler L, Li N. 2006. Toxic potential of materials at the nanolevel. Science. 311:622-627.
75. Noctor G, Foyer CH. 1998. Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Biol. 49:249-279.
76. Oberdürster G. 2000. Toxicology of ultrafine particles: in vivo studies. Philos Trans Roy Soc London A Math Phys Eng Sci. 358:2719-2740.
77. Oukarroum A, Barhoumi L, Pirastru L, Dewez D. 2013. Silver nanoparticle toxicity effect on growth and cellular viability of the aquatic plant Lemna gibba. Environ Toxicol Chem. 32:902-907.
78. Pakrashi S, Jain N, Dalai S, Jayakumar J, Chandrasekaran PT, Raichur AM, Chandrasekaran N, Mukherjee A, Bansal V. 2014. In vivo genotoxicity assessment of titanium dioxide nanoparticles by Allium cepa root tip assay at high exposure concentrations. PLoS One. 9:e87789.
79. Priester JH, Ge Y, Mielke RE, Horst AM, Moritz SC, Espinosa K, Gelb J, Walker SL, Nisbet RM, An YJ, et al. 2012. Soybean susceptibility to manufactured nanomaterials with evidence for food quality and soil fertility interruption. Proceed Nat Acad Sci. 109:E2451-E2456.
80. Qian H, Peng X, Han X, Ren J, Sun L, Fu Z. 2013. Comparison of the toxicity of silver nanoparticles and silver ions on the growth of terrestrial plant model Arabidopsis thaliana. J Environ Sci. 25:1947-1956.
81. Rajeshwari A, Kavitha S, Alex SA, Kumar D, Mukherjee A, Chandrasekaran N, Mukherjee A. 2015. Cytotoxicity of aluminum oxide nanoparticles on Allium cepa root tip - effects of oxidative stress generation and biouptake. Environ Sci Pollut Res. 22:11057-11066.
82. Rani PU, Yasur J, Loke KS, Dutta D. 2016. Effect of synthetic and bio-synthesized silver nanoparticles on growth, physiology and oxidative stress of water hyacinth: Eichhornia crassipes (Mart) Solms. Acta Physiol Plant. 38:1-9.
83. Rao K, Raghavendra A, Reddy K. 2006. Physiology and molecular biology of stress tolerance in plants. Netherlands: Springer.
84. Riahi-Madvar A, Rezaee F, Jalali V. 2012. Effects of alumina nanoparticles on morphological properties and antioxidant system of Triticum aestivum. Iran J Plant Physiol. 3:595-603.
85. Rico CM, Hong J, Morales MI, Zhao L, Barrios AC, Zhang JY, Peralta-Videa JR, Gardea-Torresdey JL. 2013. Effect of cerium oxide nanoparticles on rice: a study involving the antioxidant defense system and in vivo fluorescence imaging. Environ Sci Technol. 47:5635-5642.
86. Rico CM, Lee SC, Rubenecia R, Mukherjee A, Hong J, Peralta-Videa JR, Gardea-Torresdey JL. 2014. Cerium oxide nanoparticles impact yield and modify nutritional parameters in wheat (Triticum aestivum L.). J Agric Food Chem. 62:9669-9675.
87. Rico CM, Majumdar S, Duarte-Gardea M, Peralta-Videa JR, Gardea-Torresdey JL. 2011. Interaction of nanoparticles with edible plants and their possible implications in the food chain. J Agric Food Chem. 59:3485-3498.
88. Rico CM, Morales MI, Barrios AC, McCreary R, Hong J, Lee WY, Nunez J, Peralta-Videa JR, Gardea-Torresdey JL. 2013. Effect of cerium oxide nanoparticles on the quality of rice (Oryza sativa L.) grains. J Agric Food Chem. 61:11278-11285.
89. Rico C, Peralta-Videa J, Gardea-Torresdey J. 2015. Nanotechnology and Plant Sciences. In: Manzer H. Siddiqui, Mohamed H. Al-Whaibi, Firoz Mohammad, editors. Chemistry, biochemistry of nanoparticles, and their role in antioxidant defense system in plants, Nanotechnology and Plant Sciences. Springer; p. 1-17.
90. Rui M, Ma C, Hao Y, Guo J, Rui Y, Tang X, Zhao Q, Fan X, Zhang Z, Hou T. 2016. Iron oxide nanoparticles as a potential iron fertilizer for peanut (Arachis hypogaea). Front Plant Sci. 7:815.
91. Rui Y, Zhang P, Zhang Y, Ma Y, He X, Gui X, Li Y, Zhang J, Zheng L, Chu S, et al. 2015. Transformation of ceria nanoparticles in cucumber plants is influenced by phosphate. Environ Pollut. 198:8-14.
92. Salah SM, Yajing G, Dongdong C, Jie L, Aamir N, Qijuan H, Weimin H, Mingyu N, Jin H. 2015. Seed priming with polyethylene glycol regulating the physiological and molecular mechanism in rice (Oryza sativa L.) under nano-ZnO stress. Sci Rep. 5:14278.
93. Santner A, Calderon-Villalobos LIA, Estelle M. 2009. Plant hormones are versatile chemical regulators of plant growth. Nat Chem Biol. 5:301-307.
94. Scandalios JG. 1993. Oxygen stress and superoxide dismutases. Plant Physiol. 101:7-12.
95. Schlich K, Hund-Rinke K. 2015. Influence of soil properties on the effect of silver nanomaterials on microbial activity in five soils. Environ Pollut. 196:321-330.
96. 2 nanoparticle transfer from soil into the food chain. Environ Sci Technol. 47:11592-11598.
97. Sharma P, Jha AB, Dubey RS, Pessarakli M. 2012. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot. 2012:1-26.
98. Shaw AK, Hossain Z. 2013. Impact of nano-CuO stress on rice (Oryza sativa L.) seedlings. Chemosphere. 93:906-915.
99. Shaymurat T, Gu J, Xu C, Yang Z, Zhao Q, Liu Y, Liu Y. 2012. Phytotoxic and genotoxic effects of ZnO nanoparticles on garlic (Allium sativum L.): A morphological study. Nanotoxicology. 6:241-248.
100. Shen CX, Zhang QF, Li J, Bi FC, Yao N. 2010. Induction of programmed cell death in Arabidopsis and rice by single-wall carbon nanotubes. Am J Bot. 97:1602-1609.
101. Singh VP, Singh S, Kumar J, Prasad SM. 2015. Investigating the roles of ascorbate-glutathione cycle and thiol metabolism in arsenate tolerance in ridged luffa seedlings. Protoplasma. 252:1217-1229.
102. 2 and Ag on tomatoes (Lycopersicon esculentum). Ecotoxicol Environ Saf. 93:60-67.
103. Stampoulis D, Sinha SK, White JC. 2009. Assay-dependent phytotoxicity of nanoparticles to plants. Environ Sci Technol. 43:9473-9479.
104. Syu Y, Hung JH, Chen JC, Chuang H. 2014. Impacts of size and shape of silver nanoparticles on Arabidopsis plant growth and gene expression. Plant Physiol Biochem. 83:57-64.
105. Tang Y, He R, Zhao J, Nie G, Xu L, Xing B. 2016. Oxidative stress-induced toxicity of CuO nanoparticles and related toxicogenomic responses in Arabidopsis thaliana. Environ Pollut. 212:605-614.
106. Tanou G, Molassiotis A, Diamantidis G. 2009. Induction of reactive oxygen species and necrotic death-like destruction in strawberry leaves by salinity. Environ Exp Bot. 65:270-281.
107. Tarasenko V, Garnik EY, Shmakov V, Konstantinov YM. 2012. Modified alternative oxidase expression results in different reactive oxygen species contents in Arabidopsis cell culture but not in whole plants. Biol Plant. 56:635-640.
108. Thannickal VJ, Fanburg BL. 2000. Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol. 279:L1005-L1028.
109. Tolaymat T, El Badawy A, Sequeira R, Genaidy A. 2015. A system-of-systems approach as a broad and integrated paradigm for sustainable engineered nanomaterials. Sci Total Environ. 511:595-607.
110. Vannini C, Domingo G, Onelli E, De Mattia F, Bruni I, Marsoni M, Bracale M. 2014. Phytotoxic and genotoxic effects of silver nanoparticles exposure on germinating wheat seedlings. J Plant Physiol. 171:1142-1148.
111. Wang Z, Xie X, Zhao J, Liu X, Feng W, White JC, Xing B. 2012. Xylem- and phloem-based transport of CuO nanoparticles in maize (Zea mays L.). Environ Sci Technol. 46:4434-4441.
112. Wei H, Wang E. 2013. Nanomaterials with enzyme-like characteristics (nanozymes): next-generation artificial enzymes. Chem Soc Rev. 42:6060-6093.
113. Xia T, Kovochich M, Liong M, Mädler L, Gilbert B, Shi H, Yeh JI, Zink JI, Nel AE. 2008. Comparison of the mechanism of toxicity of zinc oxide and cerium oxide nanoparticles based on dissolution and oxidative stress properties. ACS Nano. 2:2121-2134.
114. Yan S, Zhao L, Li H, Zhang Q, Tan J, Huang M, He S, Li L. 2013. Single-walled carbon nanotubes selectively influence maize root tissue development accompanied by the change in the related gene expression. J Hazard Mater. 246-247:110-118.
115. 2 on the nitrogen metabolism of growing spinach. Biol Trace Elem Res. 110:179-190.
116. Yasur J, Rani PU. 2013. Environmental effects of nanosilver: impact on castor seed germination, seedling growth, and plant physiology. Environ Sci Pollut Res. 20:8636-8648.
117. Yin L, Colman BP, McGill BM, Wright JP, Bernhardt ES. 2012. Effects of silver nanoparticle exposure on germination and early growth of eleven wetland plants. PLoS One. 7:e47674.
118. Young AJ. 1991. The photoprotective role of carotenoids in higher plants. Physiol Plant. 83:702-708.
119. 2 in sand cultured romaine lettuce. Environ Pollut. 220:1400-1408.
120. Zhang P, Ma Y, Zhang Z, He X, Li Y, Zhang J, Zheng L, Zhao Y. 2015. Species-specific toxicity of ceria nanoparticles to Lactuca plants. Nanotoxicology. 9:1-8.
121. Zhang P, Ma Y, Zhang Z, He X, Zhang J, Guo Z, Tai R, Zhao Y, Chai Z. 2012. Biotransformation of ceria nanoparticles in cucumber plants. ACS Nano. 6:9943-9950.
122. Zhang W, Musante C, White JC, Schwab P, Wang Q, Ebbs SD, Ma X. 2015. Bioavailability of cerium oxide nanoparticles to Raphanus sativus L. in two soils. Plant Physiol Biochem. 110:185-193.
123. Zhang R, Zhang H, Tu C, Hu X, Li L, Luo Y, Christie P. 2015. Phytotoxicity of ZnO nanoparticles and the released Zn (II) ion to corn (Zea mays L.) and cucumber (Cucumis sativus L.) during germination. Environ Sci Pollut Res. 22:11109-11117.
124. 2, heat shock protein, and lipid peroxidation. ACS Nano. 6:9615-9622.
125. 2 and ZnO nanoparticles on cucumber physiological markers and bioaccumulation of Ce and Zn: a life cycle study. J Agric Food Chem. 61:11945-11951.
126. 2. Biol Trace Elem Res. 104:83-91.
127. Zhu H, Han J, Xiao JQ, Jin Y. 2008. Uptake, translocation, and accumulation of manufactured iron oxide nanoparticles by pumpkin plants. J Environ Monitor. 10:713-717.