Abstract
Titanium dioxide (TiO2) nanoparticles (NPs) are the most widely released nanomaterials in the environment and are considered an emerging contaminant. Although the phytotoxicity mechanism of TiO2 NPs on plants involves the elevated generation of reactive oxygen species (ROS), it is still not well established in soybean. Herein, we evaluated the effects of 250–1000 mg L−1 TiO2 NPs on seed germination, growth, content of ROS, lipid peroxidation, and activity of antioxidant enzymes in roots of soybean plants. Our data revealed that up to 1000 mg L−1 TiO2 NPs did not affect soybean seed germination. Transmission electron microscopy images and determinations of zeta potential and hydrodynamic diameter of a suspension of TiO2 NPs demonstrated that they form aggregates, favoring their adsorption to the root surface with consequent physical damage. The main deleterious effects noted on roots were reduced cell viability, reduced root hair number, striated aspect of root apexes, and reduced fresh and dry weights of roots. In disagreement with other studies, plant exposure to TiO2 NPs reduced the level of total ROS and lipid peroxidation, probably due to increased superoxide dismutase (SOD) activity. Altogether, our data suggest that the toxicity mechanism of TiO2 NPs on soybean roots involves physical damage resulting from their adsorption to the root surface, but not the generation of ROS.
Similar content being viewed by others
Data Availability
Not applicable.
References
Andersen, C. P., King, G., Plocher, M., Storm, M., Pokhrel, L. R., Johnson, M. G., & Rygiewicz, P. T. (2016). Germination and early plant development of ten plant species exposed to titanium dioxide and cerium oxide nanoparticles. Environmental Toxicology and Chemistry, 35(9), 2223–2229. https://doi.org/10.1002/etc.3374.
Avellan, A., Schwab, F., Masion, A., Chaurand, P., Borschneck, D., Vidal, V., & Santaella, C. (2017). Nanoparticle uptake in plants: Gold nanomaterial localized in roots of Arabidopsis thaliana by X-ray computed nanotomography and hyperspectral imaging. Environmental Science and Technology, 51(15), 8682–8691. https://doi.org/10.1021/acs.est.7b01133.
Azevedo, R. A., Alas, R. M., Smith, R. J., & Lea, P. J. (1998). Response of antioxidante enzymes to transfer from elevated carbon dioxide to air and ozone fumigation, in the leaves and roots of wild-type and catalase-deficient mutant of barley. Physiologia Plantarum, 104, 280–292. https://doi.org/10.1034/j.1399-3054.1998.1040217.x.
Bradford, M. M. (1976). Rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254. https://doi.org/10.1006/abio.1976.9999.
Boveris, A., Cadenas, E., Chance, B. (1980). Low level chemiluminescence of the lipoxygenase reaction. Photobiochemistry and Photobiophysics, 1, 175–182.
Castiglione, M. R., Giorgetti, L., Geri, C., & Cremonini, R. (2011). The effects of nano-TiO2 on seed germination, development and mitosis of root tip cells of Vicia narbonensis L. and Zea mays L. Journal of Nanoparticle Research, 13(6), 2443–2449. https://doi.org/10.1007/s11051-010-0135-8.
Coman, V., Oprea, I., Leopold, L. F., Vodnar, D. C., & Coman, C. (2019). Soybean interaction with engineered nanomaterials: A literature review of recent data. Nanomaterials, 9(9), 1–25. https://doi.org/10.3390/nano9091248.
Cox, A., Venkatachalam, P., Sahi, S., & Sharma, N. (2016). Silver and titanium dioxide nanoparticle toxicity in plants : A review of current research. Plant Physiology et Biochemistry, 107, 147–163. https://doi.org/10.1016/j.plaphy.2016.05.022.
Cunha Lopes, T. L., de Cássia Siqueira-Soares, R., Gonçalves de Almeida, G. H., Romano de Melo, G. S., Barreto, G. E., de Oliveira, D. M., et al. (2018). Lignin-induced growth inhibition in soybean exposed to iron oxide nanoparticles. Chemosphere, 211, 226–234. https://doi.org/10.1016/j.chemosphere.2018.07.143.
Das, K., & Roychoudhury, A. (2014). Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Frontiers in Environmental Science, 2, 1–13. https://doi.org/10.3389/fenvs.2014.00053.
Dayem, A. A., Hossain, M. K., Lee, S. B., Kim, K., Saha, S. K., Yang, G., et al. (2017). The role of reactive oxygen species (ros) in the biological activities of metallic nanoparticles. International Journal of Molecular Science, 18(1), 120. https://doi.org/10.3390/ijms18010120.
Devi, R. S., & Prasad, M. N. V. (1996). Ferulic acid mediated changes in oxidative enzymes of maize seedlings: Implications in growth. Biologia Plantarum, 38(3), 387–395. https://doi.org/10.1007/BF02896668.
Dimkpa, C. O., McLean, J. E., Latta, D. E., Manangón, E., Britt, D. W., Johnson, W. P., et al. (2012). CuO and ZnO nanoparticles: Phytotoxicity, metal speciation, and induction of oxidative stress in sand-grown wheat. Journal of Nanoparticle Research, 14(9). https://doi.org/10.1007/s11051-012-1125-9.
Dixon, R. A., & Paiva, N. L. (1995). Stress-Induced Phenylpropanoid Metabolism. The Plant Cell, 7(7), 1085. https://doi.org/10.2307/3870059.
Dos Santos, W. D., Ferrarese, M. L. L., Nakamura, C. V., Mourão, K. S. M., Mangolin, C. A., & Ferrarese-Filho, O. (2008). Soybean (Glycine max) root lignification induced by ferulic acid. The possible mode of action. Journal of Chemical Ecology, 34(9), 1230–1241. https://doi.org/10.1007/s10886-008-9522-3.
Facundo, H. T. F., Brandt, C. T., Owen, J. S., & Lima, V. L. M. (2004). Elevated levels of erythrocyte-conjugated dienes indicate increased lipid peroxidation in schistosomiasis mansoni patients. Brazilian Journal of Medical and Biological Research, 37(7), 957–962. https://doi.org/10.1590/S0100-879X2004000700003.
Feizi, H., Kamali, M., Jafari, L., & Rezvani Moghaddam, P. (2013). Phytotoxicity and stimulatory impacts of nanosized and bulk titanium dioxide on fennel (Foeniculum vulgare Mill). Chemosphere, 91(4), 506–511. https://doi.org/10.1016/j.chemosphere.2012.12.012.
Félix, R., Valentão, P., Andrade, P. B., Félix, C., Novais, S. C., & Lemos, M. F. L. (2020). Evaluating the in vitro potential of natural extracts to protect lipids from oxidative damage. Antioxidants, 9(3), 1–29. https://doi.org/10.3390/antiox9030231.
Ferreira, A. G., Borguetti, F. (2004). Germinação: do básico ao aplicado. Porto Alegre, Artmed.
Foltête, A. S., Masfaraud, J. F., Bigorgne, E., Nahmani, J., Chaurand, P., Botta, C., et al. (2011). Environmental impact of sunscreen nanomaterials: Ecotoxicity and genotoxicity of altered TiO2 nanocomposites on Vicia faba. Environmental Pollution, 159(10), 2515–2522. https://doi.org/10.1016/j.envpol.2011.06.020.
Frazier, T. P., Burklew, C. E., & Zhang, B. (2014). Titanium dioxide nanoparticles affect the growth and microRNA expression of tobacco (Nicotiana tabacum). Functional and Integrative Genomics, 14(1), 75–83. https://doi.org/10.1007/s10142-013-0341-4.
Fu, P. P., Xia, Q., Hwang, H. M., Ray, P. C., & Yu, H. (2014). Mechanisms of nanotoxicity: Generation of reactive oxygen species. Journal of Food and Drug Analysis, 22(1), 64–75. https://doi.org/10.1016/j.jfda.2014.01.005.
Giannopolitis, C. N., & Ries, S. K. (1977). Superoxide dismutases occurrence in higher plants. Plant Physiology, 59, 309–314. https://doi.org/10.1104/pp.59.2.309.
Gutteridge, J. M. C. (1995). Lipid and antioxidants as biomarkers of tissue damage. Clinical Chemistry, 41(12), 1819–1828.
Heath, R. L., & Packer, L. (1968). Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acids peroxidation. Archives of Biochemistry and Biophysics, 125, 189–198.
Heringa, M. B., Geraets, L., van Eijkeren, J. C. H., Vandebriel, R. J., de Jong, W. H., & Oomen, A. G. (2016). Risk assessment of titanium dioxide nanoparticles via oral exposure, including toxicokinetic considerations. Nanotoxicology, 10(10), 1515–1525. https://doi.org/10.1080/17435390.2016.1238113.
IARC. (2010). Carbon black, titanium dioxide, and talc. Lyon.
Jambunathan, N. (2010). Determination and detection of reactive oxygen species (ROS), lipid peroxidation, and electrolyte leakage in plants. In R. Sunkar (Ed.), Plant stress tolerance: Methods in molecular biology (pp. 291–297). Springer. https://doi.org/10.1007/978-1-60761-702-0.
Katiyar, P., Yadu, B., Korram, J., Satnami, M. L., Kumar, M., & Keshaykant, S. (2020). Titanium nanoparticles attenuates arsenic toxicity by up-regulating expressions of defensive genes in Vigna radiata L. Journal of Environmental Sciences, 92, 18–27. https://doi.org/10.1016/j.jes.2020.02.013.
Keller, A. A., McFerran, S., Lazareva, A., & Suh, S. (2013). Global life cycle releases of engineered nanomaterials. Journal of Nanoparticle Research, 15(6). https://doi.org/10.1007/s11051-013-1692-4.
Kořenková, L., Šebesta, M., Urík, M., Kolenčík, M., Kratošová, G., Bujdoš, M., et al. (2017). Physiological response of culture media-grown barley (Hordeum vulgare L.) to titanium oxide nanoparticles. Acta Agriculturae Scandinavica, 67(4), 285–291. https://doi.org/10.1080/09064710.2016.1267255.
Larue, C., Laurette, J., Herlin-Boime, N., Khodja, H., Fayard, B., Flank, A. M., et al. (2012). Accumulation, translocation and impact of TiO2 nanoparticles in wheat (Triticum aestivum spp.): Influence of diameter and crystal phase. Science of the Total Environment, 431, 197–208. https://doi.org/10.1016/j.scitotenv.2012.04.073.
Laware, S. L., & Raskar, S. (2014). Effect of titanium dioxide nanoparticles on hydrolytic and antioxidant enzymes during seed germination in onion. International Journal of Current Microbiology and Applied Sciences, 3, 749–760.
Li, J., Hu, J., Ma, C., Wang, Y., Wu, C., Huang, J., & Xing, B. (2016). Uptake, translocation and physiological effects of magnetic iron oxide (γ-Fe2O3) nanoparticles in corn (Zea mays L.). Chemosphere, 159, 326–334. https://doi.org/10.1016/j.chemosphere.2016.05.083.
Lu, C. M., Zhang, C. Y., Wu, J. Q., & Tao, M. X. (2002). Research of the effect of nanometer on germination and growth enhancement of Glycine max and its mechanism. Soybean Science, 21, 168–172.
Marslin, G., Sheeba, C. J., & Franklin, G. (2017). Nanoparticles alter secondary metabolism in plants via ros burst. Frontiers in Plant Science, 8, 1–8. https://doi.org/10.3389/fpls.2017.00832.
Martínez-Fernández, D., Barroso, D., & Komárek, M. (2016). Root water transport of Helianthus annuus L. under iron oxide nanoparticle exposure. Environmental Science and Pollution Research, 23(2), 1732–1741. https://doi.org/10.1007/s11356-015-5423-5.
Mattiello, A., Lizzi, D., & Marchiol, L. (2018). Influence of titanium dioxide nanoparticles (nTiO2) on crop plants: A systematic overview. In D. K. Tripathi, P. Ahmad, S. Sharma, D. K. Chauhan, & N. K. Dubey (Eds.), Nanomaterials in Plants, Algae, and Microorganisms (pp. 277–296). Elsevier. https://doi.org/10.1016/B978-0-12-811487-2.00012-8.
Mhamdi, A., & Van Breusegem, F. (2018). Reactive oxygen species in plant development. Development, 145(15), dev164376. https://doi.org/10.1242/dev.164376.
Miralles, P., Church, T. L., & Harris, A. T. (2012). Toxicity, uptake, and translocation of engineered nanomaterials in vascular plants. Environmental Science and Technology, 46(17), 9224–9239. https://doi.org/10.1021/es202995d.
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. Ecotoxicology and Environmental Safety, 108, 335–339. https://doi.org/10.1016/j.ecoenv.2014.07.013.
Noctor, G., Veljovic-Jovanovic, S., Foyer, C. H., & Grace, S. (2000). Peroxide processing in photosynthesis: Antioxidant coupling and redox signalling. In Philosophical Transactions of the Royal Society B: Biological Sciences. https://doi.org/10.1098/rstb.2000.0707.
Nowack, B., & Bucheli, T. D. (2007). Occurrence, behavior and effects of nanoparticles in the environment. Environmental Pollution, 150(1), 5–22. https://doi.org/10.1016/j.envpol.2007.06.006.
Pacheco, I., & Buzea, C. (2018). Nanoparticle uptake by plants: Beneficial or detrimental. In M. Faisal, Q. Saquib, A. Alatar, & A. Al-Khedhairy (Eds.), Phytotoxicity of nanoparticles (pp. 1–61). Cham: Springer. https://doi.org/10.1007/978-3-319-76708-6_1.
Pakrashi, S., Jain, N., Dalai, S., Jayakumar, J., Chandrasekaran, P. T., Raichur, A. M., et al. (2014). In vivo genotoxicity assessment of titanium dioxide nanoparticles by Allium cepa root tip assay at high exposure concentrations. PLoS One, 9(2). https://doi.org/10.1371/journal.pone.0087789.
Pandey, V. P., Awasthi, M., Singh, S., Tiwari, S., & Dwivedi, U. N. (2017). A comprehensive review on function and application of plant peroxidases. Biochemistry & Analytical Biochemistry, 6(1), 1000308. https://doi.org/10.4172/2161-1009.1000308.
Pergo, E. M., & Ishii-Iwamoto, E. L. (2011). Changes in energy metabolism and antioxidant defense systems during seed germination of the weed species Ipomoea triloba L. and the responses to allelochemicals. Journal of Chemical Ecology, 37(5), 500–513. https://doi.org/10.1007/s10886-011-9945-0.
Raliya, R., Franke, C., Chavalmane, S., Nair, R., & Reed, N. (2016). Quantitative understanding of nanoparticle uptake in watermelon plants, 7, 1–10. https://doi.org/10.3389/fpls.2016.01288.
Ramesh, M., Palanisamy, K., & Kumar Sharma, N. (2014). Effects of bulk & nano-titanium dioxide and zinc oxide on physio-morphological changes in Triticum aestivum Linn. Journal of Global Biosciences ISSN, 3(2), 2320–1355.
Sergiev, V., Alexieva, E., & Karanov, E. (1997). Effect of spermine, atrazine and combination between them on some endogenous protective systems and stress markers in plants. Comptes Rendus De l’Academie Bulgare Des Sciences, 51, 121–124.
Servin, A. D., Castillo-Michel, H., Hernandez-Viezcas, J. A., Diaz, B. C., Peralta-Videa, J. R., & Gardea-Torresdey, J. L. (2012). Synchrotron micro-XRF and micro-XANES confirmation of the uptake and translocation of TiO2 nanoparticles in cucumber (Cucumis sativus) plants. Environmental Science and Technology, 46(14), 7637–7643. https://doi.org/10.1021/es300955b.
Servin, A. D., Morales, M. I., Castillo-Michel, H., Hernandez-Viezcas, J. A., Munoz, B., Zhao, L., et al. (2013). Synchrotron verification of TiO2 accumulation in cucumber fruit: A possible pathway of TiO2 nanoparticle transfer from soil into the food chain. Environmental Science and Technology, 47(20), 11592–11598. https://doi.org/10.1021/es403368j.
Soares, A. R., Ferrarese, M. D. L. L., Siqueira, R. D. C., Böhm, F. M. L. Z., & Ferrarese-Filho, O. (2007). L-DOPA increases lignification associated with Glycine max root growth-inhibition. Journal of Chemical Ecology, 33(2), 265–275. https://doi.org/10.1007/s10886-006-9227-4.
Soares, A. R., de Ferrarese, M. L. L., de Siqueira-Soares, R. C., Marchiosi, R., Finger-Teixeira, A., & Ferrarese-Filho, O. (2011). The allelochemical L-dopa increases melanin production and reduces reactive oxygen species in soybean roots. Journal of Chemical Ecology, 37(8), 891–898. https://doi.org/10.1007/s10886-011-9988-2.
Song, G., Gao, Y., Wu, H., Hou, W., Zhang, C., & Ma, H. (2012). Physiological effect of anatase TiO2 nanoparticles on Lemna minor. Environmental Toxicology and Chemistry, 31(9), 2147–2152. https://doi.org/10.1002/etc.1933.
Song, U., Jun, H., Waldman, B., Roh, J., Kim, Y., Yi, J., & Lee, E. J. (2013a). Functional analyses of nanoparticle toxicity: A comparative study of the effects of TiO2 and Ag on tomatoes (Lycopersicon esculentum). Ecotoxicology and Environmental Safety, 93, 60–67. https://doi.org/10.1016/j.ecoenv.2013.03.033.
Song, U., Shin, M., Lee, G., Roh, J., Kim, Y., & Lee, E. J. (2013b). Functional analysis of TiO2 nanoparticle toxicity in three plant species. Biological Trace Element Research, 155(1), 93–103. https://doi.org/10.1007/s12011-013-9765-x.
Tománková, K., Luhová, L., Petřivalský, M., Peč, P., & Lebeda, A. (2006). Biochemical aspects of reactive oxygen species formation in the interaction between Lycopersicon spp. and Oidium neolycopersici. Physiological and Molecular Plant Pathology, 68(1–3), 22–32. https://doi.org/10.1016/j.pmpp.2006.05.005.
Tripathi, D. K., Singh, S., Singh, S., Srivastava, P. K., Singh, V. P., Singh, S., et al. (2017). Nitric oxide alleviates silver nanoparticles (AgNps)-induced phytotoxicity in Pisum sativum seedlings. Plant Physiology and Biochemistry, 110, 167–177. https://doi.org/10.1016/j.plaphy.2016.06.015.
Wang, Y., Zhu, X., Lao, Y., Lv, X., Tao, Y., Huang, B., et al. (2016). TiO2 nanoparticles in the marine environment: Physical effects responsible for the toxicity on algae Phaeodactylum tricornutum. Science of the Total Environment, 565, 818–826. https://doi.org/10.1016/j.scitotenv.2016.03.164.
Yang, F., Hong, F., You, W., Liu, C., Gao, F., Wu, C., & Yang, P. (2006). Influences of nano-anatase TiO2 on the nitrogen metabolism of growing spinach. Biological Trace Element Research, 110(2), 179–190. https://doi.org/10.1385/BTER:110:2:179.
Zhao, L., Peng, B., Hernandez-Viezcas, J. A., Rico, C., Sun, Y., Peralta-Videa, J. R., et al. (2012). Stress response and tolerance of Zea mays to CeO2 nanoparticles: Cross talk among H2O2, heat shock protein, and lipid peroxidation. ACS Nano, 6(11), 9615–9622. https://doi.org/10.1021/nn302975u.
Zheng, L., Hong, F., Lu, S., & Liu, C. (2005). Effect of nano-TiO2 on strength of naturally aged seeds and growth of spinach. Biological Trace Element Research, 104(1), 83–91. https://doi.org/10.1385/bter:104:1:083.
Zhu, H., Han, J., Xiao, J. Q., & Jin, Y. (2008). Uptake, translocation, and accumulation of manufactured iron oxide nanoparticles by pumpkin plants. Journal of Environmental Monitoring, 10(6), 713–717. https://doi.org/10.1039/b805998e.
Ziental, D., Czarczynska-Golinska, B., Mlynarczyk, D. T., Glowacka-Sobotta, A., Stanisz, B., Golinski, T., & Sobotta, L. (2020). Titanium dioxide nanoparticles: prospects and applications in medicine. Nanomaterials, 10, 387. https://doi.org/10.3390/nano10020387.
Acknowledgments
Rogério Marchiosi and Osvaldo Ferrarese-Filho are research fellows of National Council for Scientific and Technological Development (CNPq). Gabriele Sauthier Romano de Melo was the recipient of a CNPq fellowship. The authors thank César Armando Contreras Lancheros by the aid provided in the microscopy analyzes.
Funding
This work was funded by grants from the National Council for Scientific and Technological Development – CNPq (no. 407791/2018-3).
Author information
Authors and Affiliations
Contributions
Rogério Marchiosi and Osvaldo Ferrarese-Filho designed the study, analyzed data, and wrote the manuscript text. Gabriele Sauthier Romano de Melo performed most experiments. Marcela de Paiva Foletto-Felipe helped in microscopy analysis. Renato Polimeni Constantin and Josielle Abrahão helped in the determination of enzyme activity and quantification of ROS. Wanderley Dantas dos Santos and Rodrigo Polimeni Constantin helped design the study and analyzed the data. All authors revised and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Ethics Approval
Not applicable.
Consent to Participate
Not applicable.
Consent for Publication
Not applicable.
Code Availability
Not applicable.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
de Melo, G.S.R., Constantin, R.P., Abrahão, J. et al. Titanium Dioxide Nanoparticles Induce Root Growth Inhibition in Soybean Due to Physical Damages. Water Air Soil Pollut 232, 25 (2021). https://doi.org/10.1007/s11270-020-04955-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11270-020-04955-7