Nanoceria and bulk cerium oxide effects on the germination of asplenium adiantum-nigrum spores

Aranzazu Gomez-Garay, Beatriz Pintos, José Antonio Manzanera, Carmen Prada, Luisa Martin, José María Gabriel y Galan

Abstract


Aim of study: The effect of cerium oxide engineered nanoparticles on the spore germination of the fern. Asplenium adiantum-nigrum.

Area of study: France, Britanny Region, Finistére Department, Plougonvelin, in rocks near the sea.

Material and methods: Asplenium spores were cultured in vitro on agar medium with Nano-CeO2 (less than 25 nm particle size) and bulk-CeO2. The addition of each nano- and bulk particles ranged from 0 to 3000 mg L-1. Observations on rhizoidal and prothallial cells during first stages of gametophyte development were made. The No-Observed-Adverse-Effect concentration (NOAEC) and Lowest-Observed-Adverse-Effect-Concentration (LOEC) values for spore germination rate data were analyzed.

 Main results: Germination was speeded up by 100 to 2000 mg L-1 nanoceria, while bulk cerium oxide had the same effect for 500 to 200 mg L-1 concentrations. Present results showed cellular damage in the protonema while rhizoid cells seemed not to be affected, as growth and membrane integrity remained.

Research highlights: Both nanosized and bulk cerium oxide are toxic for the fern Asplenium adiantum-nigrum, although diverse toxicity patterns were shown for both materials. Diverse toxic effects have been observed: chloroplast membrane damage and lysis, cell wall and membrane disruption which leads to cell lysis; and alterations in morphology and development.

Keywords: Nanoparticles; rhizoid; prothallus; chloroplast; fern.


Keywords


Nanoparticles; rhizoid; prothallus; chloroplast; fern.

Full Text:

PDF HTML XML

References


References

Andersen CP, King G, Plocher M, Storm M, Pokhrel LR, Johnson MG, Rygiewicz PT, 2016. Germination and early plant development of ten plant species exposed to TiO2 and CeO2 nanoparticles. Environ Toxicol Chem 35(9): 2223-2229. http://dx.doi.org/10.1002/etc.3374

Banks JA, 1999. Gametophyte development in ferns. Ann Rev Plant Physiol Plant Mol Biol 50: 163-186. http://dx.doi.org/10.1146/annurev.arplant.50.1.163

Chang J-S, Yoon I-H, Kim K-W, 2009. Heavy metal and arsenic accumulating fern species as potential ecological indicators in As-contaminated abandoned mines. Ecol Indic 9: 1275-1279. http://dx.doi.org/10.1016/j.ecolind.2009.03.011

Darlington TK, Neigh AM, Spencer MT, Nguyen OT, Oldenburg SJ, 2009. Nanoparticle characteristics affecting environmental fate and transport through soil. Environ Toxicol Chem 28: 1191-1199. http://dx.doi.org/10.1897/08-341.1

Diatloff E, Smith FW, Asher CJ, 2008. Effects of lanthanum and cerium on the growth and mineral nutrition of corn and mungbean. Ann Bot-London 101: 971-982. http://dx.doi.org/10.1093/aob/mcn021

Donaldson K, Brown D, Clouter A, Duffin R, MacNee W, Renwick L, Tran L, Stone V, 2002. The pulmonary toxicology of ultrafine particles. J Aerosol Med 15: 213-220. http://dx.doi.org/10.1089/089426802320282338

Dyer A, 1979. The culture of fern gametophytes for experimental investigation. In: Dyer A (ed.) The experimental biology of ferns, London: Academic Press.

Gabriel y Galán JM, Prada C, 2010. Pteridophyte spores viability. In: Fernández H, Kumar A, Revilla MA (eds.). Working with ferns: issues and applications, New York: Springer.

Karakoti AS, Hench LL, Seal S, 2006. The potential toxicity of nanomaterials - The role of surfaces. Jom 58: 77-82. http://dx.doi.org/10.1007/s11837-006-0147-0

Lee W-M, An Y-J, Yoon H, 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. http://dx.doi.org/10.1897/07-481.1

Lloyd R, Klekowski EJ, 1970. Spore germination and viability in pteridophyta: evolutionary significance of chlorophyllous spores. Biotropica 2: 129-137. http://dx.doi.org/10.2307/2989770

Lopez-Moreno ML, de la Rosa G, Hernandez-Viezcas JA, Castillo-Michel H, Botez CE, Peralta-Videa JR, Gardea-Torresdey JL, 2010a. Evidence of the Differential Biotransformation and Genotoxicity of ZnO and CeO2 Nanoparticles on Soybean (Glycine max) Plants. Environ Sci Technol 44: 7315-7320. http://dx.doi.org/10.1021/es903891g

Lopez-Moreno ML, de la Rosa G, Hernandez-Viezcas JA, Peralta-Videa JR, Gardea-Torresdey JL, 2010b. X-ray Absorption Spectroscopy (XAS) Corroboration of the Uptake and Storage of CeO2 Nanoparticles and Assessment of Their Differential Toxicity in Four Edible Plant Species. J Agr Food Chem 58: 3689-3693. http://dx.doi.org/10.1021/jf904472e

Ma Y, Kuang L, He X, Bai W, Ding Y, Zhang Z, Zhao Z, Chai Z, 2010. Effects of rare earth oxide nanoparticles on root elongation of plants. Chemosphere, 78(3), 273-279. http://dx.doi.org/10.1016/j.chemosphere.2009.10.050

Monteiller C, Tran L, MacNee W, Faux S, Jones A, Miller B, Donaldson K, 2007. The pro-inflammatory effects of low-toxicity low-solubility particles, nanoparticles and fine particles, on epithelial cells in vitro: the role of surface area. Occup Environ Med 64: 609-615. http://dx.doi.org/10.1136/oem.2005.024802

OECD, 2014. Series on Testing and Assessment Guidance Document 116 on the Conduct and Design of Chronic Toxicity and Carcinogenicity Studies, Supporting Test Guidelines 451, 452 and 453 Second edition. 156 pp. Paris, France.

Ozaki T, Enomoto S, Minai Y, Ambe S, Makide Y, 2000. A survey of trace elements in pteridophytes. Biol Trace Elem Res 74: 259-273. http://dx.doi.org/10.1385/BTER:74:3:259

Park E-J, Choi J, Park Y-K, Park K, 2008. Oxidative stress induced by cerium oxide nanoparticles in cultured BEAS-2B cells. Toxicology 245: 90-100. http://dx.doi.org/10.1016/j.tox.2007.12.022

Prada C, Pangua E, Pajaron S, Herrero A, Escudero A, Rubio A, 1995. A comparative-study of gametophyte morphology, gametangial ontogeny and sex expression in the Asplenium adiantum-nigrum complex (Aspleniaceae, Pteridophyta). Ann Bot Fenn 32: 107-115.

Prada C, 2004. Helechos. In: Izco J (ed.) Botánica, McGraw Hill, Madrid, Spain.

Prasad MNV, Freitas HMD, 2003. Metal hyperaccumulation in plants - Biodiversity prospecting for phytoremediation technology. Electron J Biotechn 6: 285-321. http://dx.doi.org/10.2225/vol6-issue3-fulltext-6

Pulido-Reyes G, Rodea-Palomares I, Das S, Sakthivel TS, Leganes F, Rosal R, Fernández-Piñas, F, 2015. Untangling the biological effects of cerium oxide nanoparticles: the role of surface valence states. Scientific Reports, 5: 15613. PMC. Web. http://dx.doi.org/10.1038/srep15613

Raghavan V, 1989. Developmental biology of fern gametophytes. Cambridge: University Press. New York, USA. http://dx.doi.org/10.1017/CBO9780511529757

Remedios C, Rosario F, Bastos V, 2012. Environmental Nanoparticles Interactions with Plants: Morphological, Physiological, and Genotoxic Aspects. Journal of Botany 2012: 8. http://dx.doi.org/10.1155/2012/751686

Rico CM, Peralta-Videa JR, Gardea-Torresdey JL, 2015. Chemistry, biochemistry of nanoparticles, and their role in antioxidant defense system in plants. In Nanotechnology and Plant Sciences (pp. 1-17). Springer International Publishing. http://dx.doi.org/10.1007/978-3-319-14502-0_1

Rodà F, Retana J, Gracia CA, Bellot J, 1999. Ecology of Mediterranean evergreen oak forest. Springer-Verlag Berlin Heidelberg. 377 pp. New York, USA. http://dx.doi.org/10.1007/978-3-642-58618-7

Rodea-Palomares I, Boltes K, Fernandez-Pinas F, Leganes F, Garcia-Calvo E, Santiago J, Rosal R, 2011. Physicochemical Characterization and Ecotoxicological Assessment of CeO2 Nanoparticles Using Two Aquatic Microorganisms. Toxicological Sciences 119: 135-145. http://dx.doi.org/10.1093/toxsci/kfq311

Rodea-Palomares I, Gonzalo S, Santiago-Morales J, Leganes F, Garcia-Calvo E, Rosal R, Fernandez-Pinas F, 2012. An insight into the mechanisms of nanoceria toxicity in aquatic photosynthetic organisms. Aquat Toxicol 122: 133-143. http://dx.doi.org/10.1016/j.aquatox.2012.06.005

Rogers NJ, Franklin NM, Apte SC, Batley GE, Angel BM, Lead JR, Baalousha M, 2010. Physico-chemical behaviour and algal toxicity of nanoparticulate CeO2 in freshwater. Environ Chem 7: 50-60. http://dx.doi.org/10.1071/EN09123

Sager TM, Castranova V, 2009. Surface area of particle administered versus mass in determining the pulmonary toxicity of ultrafine and fine carbon black: comparison to ultrafine titanium dioxide. Particle and Fibre Toxicology 6. http://dx.doi.org/10.1186/1743-8977-6-15

Shan XQ, Wang HI, Zhang SZ, Zhou HF, Zheng Y, Yu H, Wen B, 2003. Accumulation and uptake of light rare earth elements in a hyperaccumulator Dicropteris dichotoma. Plant Sci 165: 1343-1353. http://dx.doi.org/10.1016/S0168-9452(03)00361-3

Sheffield E, 1996. From pteridophyte spore to sporophyte in the natural environment. In: J. M. Camus MG, R. Johns (ed.) Pteridology in Perspective, Kew: Royal Botanic Gardens. Richmond, Surrey, England, Great Britain.

StatSoft, 2009. Statistica 9.0.

Thill A, Zeyons O, Spalla O, Chauvat F, Rose J, Auffan M, Flank AM, 2006. Cytotoxicity of CeO2 nanoparticles for Escherichia coli. Physico-chemical insight of the cytotoxicity mechanism. Environ Sci Technol 40: 6151-6156. http://dx.doi.org/10.1021/es060999b

Warheit DB, Webb Tr Fau - Sayes CM, Sayes Cm Fau - Colvin VL, Colvin Vl Fau - Reed KL, Reed KL, 2006. Pulmonary instillation studies with nanoscale TiO2 rods and dots in rats: toxicity is not dependent upon particle size and surface area. Toxicol Sci 91: 227-236. http://dx.doi.org/10.1093/toxsci/kfj140

Warheit DB, Webb TR, Reed KL, Frerichs S, Sayes CM, 2007. Pulmonary toxicity study in rats with three forms of ultrafine-TiO2 particles: Differential responses related to surface properties. Toxicology 230: 90-104. http://dx.doi.org/10.1016/j.tox.2006.11.002

Weinberg ES, Voeller BR, 1969. Induction of fern spore germination. P Natl Acad Sci USA 64: 835-842. http://dx.doi.org/10.1073/pnas.64.3.835

Zeyons O, Thill A, Chauvat F, Menguy N, Cassier-Chauvat C, Orear C, Daraspe J, Auffan M, Rose J, Spalla O, 2009. Direct and indirect CeO2 nanoparticles toxicity for Escherichia coli and Synechocystis. Nanotoxicology 3: 284-295. http://dx.doi.org/10.3109/17435390903305260

Zhang P, Ma Y, Zhang Z, He X, Guo Z, Tai R, Ding Y, Zhao Y, Chai Z, 2012. Comparative toxicity of nanoparticulate/bulk Yb2O3 and YbCl3 to cucumber (Cucumis sativus). Environ Sci Technol 46: 1834-1841. http://dx.doi.org/10.1021/es2027295




DOI: 10.5424/fs/2016253-09294

Webpage: www.inia.es/Forestsystems