Engineered silver nanoparticles are sensed at the plasma membrane and dramatically modify the physiology of Arabidopsis thaliana plants

Plant Journal

Volumn 85, Issue 2, 2016, Pages 245-257

  Sosan, Arifa ^a   Svistunenko, Dimitri ^a   Straltsova, Darya ^b   Tsiurkina, Katsiaryna ^b   Smolich, Igor ^b   Lawson, Tracy ^a   Subramaniam, Sunitha ^a   Golovko, Vladimir ^c   Anderson, David ^c   Sokolik, Anatoliy ^b   Colbeck, Ian ^a   Demidchik, Vadim ^b,d  

^a UNIVERSITY OF ESSEX   (United Kingdom)

^b BELARUSIAN STATE UNIVERSITY   (Belarus)

^c UNIVERSITY OF CANTERBURY   (New Zealand)

^d KOMAROV BOTANICAL INSTITUTE   (Russian Federation)

Author keywords

Arabidopsis thaliana; ascorbic acid; cell calcium; ion channels; reactive oxygen species; silver nanoparticles; stress signalling

Indexed keywords

ANTIFUNGAL AGENTS; ANTIMICROBIAL AGENTS; ASCORBIC ACID; CALCIUM; CELL MEMBRANES; CELL SIGNALING; CELLS; CYTOLOGY; ELECTRON SPECTROSCOPY; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTROPHYSIOLOGY; MAGNETIC RESONANCE; MEMBRANES; METAL NANOPARTICLES; NANOPARTICLES; ORGANIC ACIDS; OXYGEN; PARAMAGNETIC RESONANCE; PHYSIOLOGY; PLANT CELL CULTURE; PLASMA DIAGNOSTICS;

ARABIDOPSIS THALIANA; ELECTRON PARAMAGNETIC RESONANCE SPECTROSCOPY; HYDROXYL RADICAL GENERATION; ION CHANNEL; PHOTOSYNTHETIC EFFICIENCY; REACTIVE OXYGEN SPECIES; SILVER NANOPARTICLES; SILVER NANOPARTICLES (AGNPS);

SILVER;

ASCORBIC ACID; CALCIUM; ION CHANNEL; METAL NANOPARTICLE; REACTIVE OXYGEN METABOLITE; SILVER;

ARABIDOPSIS; CELL MEMBRANE; CHEMISTRY; METABOLISM;

ARABIDOPSIS; ASCORBIC ACID; CALCIUM; CELL MEMBRANE; ION CHANNELS; METAL NANOPARTICLES; REACTIVE OXYGEN SPECIES; SILVER;

EID: 84955571788     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.13105     Document Type: Article

References (74)

1. AshaRani, P.V., Hande, M.P., and, Valiyaveettil, S., (2009) Anti-proliferative activity of silver nanoparticles. BMC Cell Biol. 10, 65.
2. Baker, N.R., (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu. Rev. Plant Biol. 59, 89-113.
3. Barbagallo, R.P., Oxborough, K., Pallett, K.E., and, Baker, N.R., (2003) Rapid, noninvasive screening for perturbations of metabolism and plant growth using chlorophyll fluorescence imaging. Plant Physiol. 132, 485-493.
4. Benn, T.M., and, Westerhoff, P., (2008) Nanoparticle silver released into water from commercially available sock fabrics. Environ. Sci. Technol. 42, 4133-4139.
5. Benn, T., Cavanagh, B., Hristovski, K., Posner, J.D., and, Westerhoff, P., (2010) The release of nanosilver from consumer products used in the home. J. Environ. Qual. 39, 1875-1882.
6. Blaser, S.A., Scheringer, M., MacLeod, M., and, Hungerbuehler, K., (2008) Estimation of cumulative aquatic exposure and risk due to silver: contribution of nano-functionalized plastics and textiles. Sci. Tot. Environ. 390, 396-409.
7. Braydich-Stolle, L., Hussain, S., Schlager, J.J., and, Hofmann, M., (2005) In vitro cytotoxicity of nanoparticles in mammalian germline stem cells. Toxicol. Sci. 88, 412-419.
8. Buettner, G.R., and, Jurkiewicz, B.A., (1993) Ascorbate free radical as a marker of oxidative stress: an EPR study. Free Rad. Biol. Med. 14, 49-55.
9. Choi, O., and, Hu, Z., (2008) Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. Environ. Sci. Technol. 42, 4583-4588.
10. De Planque, M.R.R., Aghdaei, S., Roose, T., and, Morgan, H., (2011) Electrophysiological characterization of membrane disruption by nanoparticles. ACS Nano, 5, 3599-3606.
11. Demidchik, V., (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biologyReactive oxygen species and oxidative stress in plants. Environ. Exp. Bot. 109, 212-228.
12. Demidchik, V., and, Maathuis, F.J.M., (2007) Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytol., 175, 387-405.
13. Demidchik, V., and, Maathuis, F.J.M., (2010) Ion channels and plant stress responses. Berlin, Heidelberg, New York: Springer-Verlag.
14. Demidchik, V., and, Tester, M.A., (2002) Sodium fluxes through nonselective cation channels in the plant plasma membrane of protoplasts from Arabidopsis roots. Plant Physiol. 128, 379-387.
15. Demidchik, V., Davenport, R.J., and, Tester, M.A., (2002a) Nonselective cation channels in plants. Annu. Rev. Plant Biol. 53, 67-107.
16. Demidchik, V., Bowen, H.C., Maathuis, F.J.M., Shabala, S.N., Tester, M.A., White, P.J., and, Davies, J.M., (2002b) Arabidopsis thaliana root nonselective cation channels mediate calcium uptake and are involved in growth. Plant J. 32, 799-808.
17. +-permeable channels in plant root cells. J. Cell Sci. 116, 81-88.
18. 2+ channels. Plant J. 49, 377-386.
19. + efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. J. Cell Sci. 123, 1468-1479.
20. Diatloff, E., Roberts, M., Sanders, D., and, Roberts, S.K., (2004) Characterization of anion channels in the plasma membrane of Arabidopsis epidermal root cells and the identification of a citrate-permeable channel induced by phosphate starvation. Plant Physiol. 136, 4136-4149.
21. Fabrega, J., Luoma, S.N., Tyler, C.R., Galloway, T.S., and, Lead, J.R., (2011) Silver nanoparticles: behaviour and effects in the aquatic environment. Environ. Int. 37, 517-531.
22. Foreman, J., Demidchik, V., Bothwell, J.H.F., Mylona, P., Miedema, H., Torres, M.A., Linstead, P., Costa, S., Brownlee, C., and, Jones, J.D.G., (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature, 422, 442-446.
23. Fujishige, N., Nishimura, N., Iuchi, S., Kunii, T., Shinozaki, K., and, Hirayama, T., (2004) A novel arabidopsis gene required for ethanol tolerance is conserved among plants and archaea. Plant Cell Physiol. 45, 659-666.
24. Gaul, L.E., and, Staud, A.H., (1935) Seventy cases of generalized argyria following organic and colloidal silver medication, including biospectrometric analysis of ten cases. J. Amer. Med. Assoc. 104, 1387-1390.
25. Geisler-Lee, J., Wang, Q., Yao, Y., Zhang, W., Geisler, M., Li, K., Huang, Y., Chen, Y., Kolmakov, A., and, Ma, X., (2013) Phytotoxicity, accumulation and transport of silver nanoparticles by Arabidopsis thaliana. Nanotoxicology, 7, 323-337.
26. Geranio, L., Heuberger, M., and, Nowack, B., (2009) The behavior of silver nanotextiles during washing. Environ. Sci. Technol. 43, 8113-8118.
27. Gottschalk, F., and, Nowack, B., (2011) The release of engineered nanomaterials to the environment. J. Environ. Monitor. 13, 1145-1155.
28. 2, ZnO, Ag, CNT, fullerenes) for different regions. Environ. Sci. Technol. 43, 9216-9222.
29. Gottschalk, F., Sonderer, T., Scholz, R.W., and, Nowack, B., (2010) Possibilities and limitations of modeling environmental exposure to engineered nanomaterials by probabilistic material flow analysis. Environ. Toxicol. Chem. 29, 1036-1048.
30. Gubbins, E.J., Batty, L.C., and, Lead, J.R., (2011) Phytotoxicity of silver nanoparticles to Lemna minor L. Environ. Pollut. 159, 1551-1559.
31. Halliwell, B., and, Gutteridge, J.M.C., (1999) Free Radicals in Biology and Medicine. New York: Oxford University Press Inc.
32. Haswell, E.S., Peyronnet, R., Barbier-Brygoo, H., Meyerowitz, E.M., and, Frachisse, J.M., (2008) Two MscS homologs provide mechanosensitive channel activities in the Arabidopsis root. Curr. Biol. 18, 730-734.
33. He, D., Jones, A.M., Garg, S., Pham, A.N., and, Waite, T.D., (2011) Silver nanoparticle-reactive oxygen species interactions: application of a charging-discharging model. J. Phys. Chem. C, 115, 5461-5468.
34. Hughes, S., El Haj, A.J., and, Dobson, J., (2005) Magnetic micro- and nanoparticle mediated activation of mechanosensitive ion channels. Med. Eng. Phys. 27, 754-762.
35. Hussain, S.M., Hess, K.L., Gearhart, J.M., Geiss, K.T., and, Schlager, J.J., (2005) In vitro toxicity of nanoparticles in BRL 3A rat liver cells. Toxicol. In Vitro, 19, 975-983.
36. Ikeda, Y., Jimbo, H., Shimazu, M., and, Satoh, K., (2002) Sumatriptan scavenges superoxide, hydroxyl, and nitric oxide radicals: in vitro electron spin resonance study. Headache, 42, 888-892.
37. Ji, J.H., Jung, J.H., Kim, S.S., Yoon, J.U., Park, J.D., Choi, B.S., Chung, Y.H., Kwon, I.H., Jeong, J., and, Han, B.S., (2007) Twenty-eight-day inhalation toxicity study of silver nanoparticles in Sprague-Dawley rats. Inhal. Toxicol. 19, 857-871.
38. Jones, A.M., Garg, S., He, D., Pham, A.N., and, Waite, T.D., (2011) Superoxide-mediated formation and charging of silver nanoparticles. Environ. Sci. Technol. 45, 1428-1434.
39. Kaegi, R., Sinnet, B., Zuleeg, S., Hagendorfer, H., Mueller, E., Vonbank, R., Boller, M., and, Burkhardt, M., (2010) Release of silver nanoparticles from outdoor facades. Environ. Pollut. 158, 2900-2905.
40. Kim, S., Choi, J.E., Choi, J., Chung, K.H., Park, K., Yi, J., and, Ryu, D.Y., (2009) Oxidative stress-dependent toxicity of silver nanoparticles in human hepatoma cells. Toxicol. In Vitro, 23, 1076-1084.
41. Kim, B., Park, C.S., Murayama, M., and, Hochella, M.F., (2010) Discovery and characterization of silver sulfide nanoparticles in final sewage sludge products. Environ. Sci. Technol. 44, 7509-7514.
42. Kiss, T., and, Osipenko, O.N., (1994) Toxic effects of heavy metals on ionic channels. Pharmacol. Rev. 46, 245-267.
43. Klein, S.A., Wilk, S.J., Thornton, T.J., and, Posner, J.D., (2008) Formation of nanopores in suspended lipid bilayers using quantum dots. J. Phys: Conf. Ser. 109, 012022.
44. Knight, H., Trewavas, A.J., and, Knight, M.R., (1996) Cold calcium signalling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell, 8, 489-501.
45. Knight, H., Trewavas, A.J., and, Knight, M.R., (1997) Calcium signalling in Arabidopsis thaliana responding to drought and salinity. Plant J. 12, 1067-1078.
46. 2+-permeable conductance and have peroxidase activity. Plant Cell, 21, 479-493.
47. 2 and humidity. Plant Physiol. 128, 1-11.
48. Lee, W.M., An, Y.J., Yoon, H., and, Kweon, H.S., (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.
49. Lee, C.W., Mahendra, S., Zodrow, K., Li, D., Tsai, Y.C., Braam, J., and, Alvarez, P.J.J., (2010) Developmental phytotoxicity of metal oxide nanoparticles to Arabidopsis thaliana. Environ. Toxicol. Chem. 29, 669-675.
50. Lee, W.M., Kwak, J.I., and, An, Y.J., (2012) Effect of silver nanoparticles in crop plants Phaseolus radiatus and Sorghum bicolor: media effect on phytotoxicity. Chemosphere, 86, 491-499.
51. •OH) by maize roots and their role in wall loosening and elongation growth. Plant Physiol. 136, 3114-3123.
52. Liu, J., and, Hurt, R.H., (2010) Ion release kinetics and particle persistence in aqueous nano-silver colloids. Environ. Sci. Technol., 44, 2169-2175.
53. Luther, G.W., and, Rickard, D.T., (2005) Metal sulfide cluster complexes and their biogeochemical importance in the environment. J. Nanopart. Res. 7, 389-407.
54. Maksaev, G., and, Haswell, E.S., (2012) MscS-Like10 is a stretch-activated ion channel from Arabidopsis thaliana with a preference for anions. Proc. Natl Acad. Sci. USA, 109, 19015-19020.
55. Monica, R.C., and, Cremonini, R., (2009) Nanoparticles and higher plants. Caryologia, 62, 161-165.
56. Montes, M.O., Hanna, S.K., Lenihan, H.S., and, Keller, A.A., (2012) Uptake, accumulation, and biotransformation of metal oxide nanoparticles by a marine suspension-feeder. J. Hazard. Mater. 225, 139-145.
57. Morones, J.R., Elechiguerra, J.L., Camacho, A., Holt, K., Kouri, J.B., Ramírez, J.T., and, Yacaman, M.J., (2005) The bactericidal effect of silver nanoparticles. Nanotechnology, 10, 2346-2353.
58. Murashige, T., and, Skoog, F., (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
59. Nair, P.M., and, Chung, I.M., (2014a) Assessment of silver nanoparticle-induced physiological and molecular changes in Arabidopsis thaliana. Environ. Sci. Pollut. Res. Int. 21, 8858-8869.
60. Nair, P.M., and, Chung, I.M., (2014b) Physiological and molecular level effects of silver nanoparticles exposure in rice (Oryza sativa L.) seedlings. Chemosphere, 112, 105-113.
61. Navarro, E., Piccapietra, F., Wagner, B., Marconi, F., Kaegi, R., Odzak, N., Sigg, L., and, Behra, R., (2008) Toxicity of silver nanoparticles to Chlamydomonas reinhardtii. Environ. Sci. Technol. 42, 8959-8964.
62. Nowack, B., Krug, H.F., and, Height, M., (2011) 120 Years of nanosilver history: implications for policy makers. Environ. Sci. Technol. 45, 1177-1183.
63. Polisensky, D.H., and, Braam, J., (1996) Cold-shock regulation of the Arabidopsis TCH genes and the effects of modulating intracellular calcium levels. Plant Physiol. 111, 1271-1279.
64. Qian, H., Peng, X., Han, X., Ren, J., Sun, L., and, 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. (China), 1, 1947-1955.
65. Radojevic, M., and, Bashkin, V.N., (1999) Plant Analysis. Practical Environmental Analysis. Cambridge: Royal Society of Chemistry.
66. Rahman, M.F., Wang, J., Patterson, T.A., Saini, U.T., Robinson, B.L., Newport, G.D., Murdock, R.C., Schlager, J.J., Hussain, S.M., and, Ali, S.F., (2009) Expression of genes related to oxidative stress in the mouse brain after exposure to silver-25 nanoparticles. Toxicol. Lett. 187, 15-21.
67. Rai, M., Yadav, A., and, Gade, A., (2009) Silver nanoparticles as a new generation of antimicrobials. Biotechnol. Adv. 27, 76-83.
68. Ratte, H., (1999) Bioaccumulation and toxicity of silver compounds: a review. Environ. Toxicol. Chem., 18, 89-108.
69. Schröder, P., and, Collins, C.D., (2011) Organic xenobiotics and plants. From mode of action to ecophysiology. In Plant Ecophysiology, Volume VIII. Dordrecht: Springer Science+Business Media B.V.
70. Scown, T.M., van Aerle, R., and, Tyler, C.R., (2010) Do engineered nanoparticles pose a significant threat to the aquatic environment? Crit. Rev. Toxicol. 40, 653-670.
71. Stampoulis, D., Sinha, S.K., and, White, J.C., (2009) Assay-dependent phytotoxicity of nanoparticles to plants. Environ. Sci. Technol. 43, 9473-9479.
72. Wang, Z., Xie, X., Zhao, J., Liu, X., Feng, W., White, J.C., and, Xing, B., (2012) Xylem- and phloem-based transport of CuO nanoparticles in maize (Zea mays L.). Environ. Sci. Technol. 46, 4434-4441.
73. Yamazaki, I., Piette, L.H., and, Grover, T.A., (1990) Kinetic studies on spin trapping of superoxide and hydroxyl radicals generated in NADPH-cytochrome P-450 reductase-paraquat systems: effect of iron chelates. J. Biol. Chem. 265, 652-659.
74. Yin, L., Cheng, Y., Espinasse, B., Colman, B.P., Auffan, M., Wiesner, M., Rose, J., Liu, J., and, Bernhardt, E.S., (2011) More than the ions: the effects of silver nanoparticles on Lolium multiflorum. Environ. Sci. Technol. 45, 2360-2367.