Effect of Nano and Bulk Nickel Oxide on Biomass and Antioxidant Enzymes Production of Fennel


Hilda Besharat(1), Ramazan Ali Khavari-Nejad(2), Homa Mahmoodzadeh(3*), Khadijeh Nejad Shahrokh Abadi(4)

(1) Department of Biology, Science and Research Branch, Islamic Azad University, Tehran
(2) Department of Biology, Science and Research Branch, Islamic Azad University, Tehran
(3) Department of Biology, Mashhad Branch, Islamic Azad University, Mashhad
(4) Department of Biology, Mashhad Branch, Islamic Azad University, Mashhad
(*) Corresponding Author


The production, growth, and physiological processes of plants respond differently to the varying concentrations of nanoparticles. Due to the increasing importance and application of nanoparticles, it is essential to determine the impact on plants physiological systems. Therefore, this study investigated the effect of different bulk and nano nickel oxide concentrations on biomass production and the enzymatic system of fennel. The experiment was carried out in a completely randomized design with the applications of 5 replications and 5 concentrations (0, 20, 100, 400, and 800 ppm) in the greenhouse of the Faculty of Science, Mashhad Branch, Islamic Azad University. This study analyzed various plants traits, including shoot and dry root weight and a few antioxidant enzymes. The results showed that root and shoot dry weight were not affected by the applied treatments. Furthermore, all applied levels of treatment significantly increased the activity of fennel leaf polyphenol oxidase compared to the control. The bulk treatment at 800 ppm was exempted, where the application of bulk nickel oxide and nanoparticles decreased dehydrogenase enzyme activity. In addition, the activity of guaiacol peroxidase increased under all levels of treatments except 100 ppm nanoparticles. The highest amount of phenylalanine ammonia-lyase activity was obtained under 20 ppm treatment with a 61.98% increase compared to the control method. Furthermore, nickel oxide treatments also increased MDA. The results showed that nanomaterials' toxicity, caused oxidative stress in this plant, and the differences in MDA content of leaves explained the higher toxicity of NiO nanoparticles than bulk form. Moreover, higher activity of leaf antioxidative enzymes in bulk NiO2 treatments, especially Guaiacol Peroxidase, explained the plant's higher resistance to oxidative stress.


Antioxidant enzymes; bulk nickel; fennel; malondialdehyde; nanoparticles; phenylalanine ammonia-lyase

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Aghdam, M.T.B., Mohammadi, H., & Ghorbanpour, M. (2016). Effects of Nano particulate anatase titanium dioxide on physiological and biochemical performance of (Linum usitatissimum) (Linaceae) under well-watered and drought stress conditions. Brazilian Journal of Botany, 39(1), pp.139-146. https://doi.org/10.1007/s40415-015-0227-x

Ahmad, M.S.A., & Ashraf, M. (2012). Essential roles and hazardous effects of nickel in plants. In Reviews of environmental contamination and toxicology, (pp. 125-167). Springer, New York, NY. https://doi.org/10.1007/978-1-4614-0668-6_6

Ahmed, A.I., Yadav, D.R., & Lee, Y.S. (2016). Applications of nickel nanoparticles for control of Fusarium wilt on lettuce and tomato. Int J Innov Res Sci Eng Technol, 5,zpp.7378-7385. https://www.semanticscholar.org/paper

Asher, C.J. (1991). Beneficial elements, functional nutrients, and possible new essential elements. Micronutrients in agriculture, 4 pp.703-723. https://doi.org/10.2136/sssabookser4.2ed.c18

Azimi, R., Jankju Borzelabad, M., Feizi, H., & Azimi, A. (2014). Interaction of SiO2 nanoparticles with seed prechilling on germination and early seedling growth of tall wheatgrass (Agropyron elongatum L.). Polish Journal of Chemical Technology, 16(3) pp.25-29. https://doi.org/10.2478/pjct-2014-0045

Barros, L., Carvalho, A.M., & Ferreira, I.C. (2010). The nutritional composition of fennel (Foeniculum vulgare): Shoots, leaves, stems and inflorescences. LWT-Food Science and Technology, 43(5), pp.814-818. https://doi.org/10.1016/j.lwt.2010.01.010

Beaudoin-Eagan, L.D., & Thorpe, T.A. (1985). Tyrosine and phenylalanine ammonia lyase activities during shoot initiation in tobacco callus cultures. Plant Physiology, 78(3), pp.438-441. https://doi.org/10.1104/pp.78.3.438

Chutipaijit, S. (2015). Establishment of condition and nano particle factors influencing plant regeneration from aromatic rice (Oryza sativa). International Journal of Agriculture & Biology, 17 pp.1049-1054. https://web.b.ebscohost.com

Cramer, G.R., Urano, K., Delrot, S., Pezzotti, M., & Shinozaki, K. (2011). Effects of abiotic stress on plants: a systems biology perspective. BMC plant biology, 11(1), pp.163. https://doi.org/10.1186/1471-2229-11-163

Curien, G., Ravanel, S., Robert, M., & Dumas, R. (2005). Identification of Six Novel Allosteric Effectors of Arabidopsis thaliana Aspartate Kinase-Homoserine Dehydrogenase Isoforms Physiological Context Sets the Specificity. Journal of Biological Chemistry, 280(50), pp.41178-41183. https://www.jbc.org/content/280/50/41178.short

D’Souza, M.R., & Devaraj, V.R. (2013). Oxidative stress biomarkers and metabolic changes associated with cadmium stress in hyacinth bean (Lablab Purpureus). African Journal of Biotechnology, 12(29). DOI: 10.5897/AJB2013.12385

Diao, W.R., Hu, Q.P., Zhang, H., & Xu, J.G. (2014). Chemical composition, antibacterial activity and mechanism of action of essential oil from seeds of fennel (Foeniculum vulgare Mill.). Food Control, 35(1), pp.109-116. https://doi.org/10.1016/j.foodcont.2013.06.056

Fageria, N.K., Filho, M.B., Moreira, A., & Guimarães, C.M. (2009). Foliar fertilization of crop plants. Journal of plant nutrition, 32(6), pp.1044-1064. https://doi.org/10.1080/01904160902872826

Faisal, M., Saquib, Q., Alatar, A.A., Al-Khedhairy, A.A., Hegazy, A.K., & Musarrat, J. (2013). Phytotoxic hazards of NiO-nanoparticles in tomato: a study on mechanism of cell death. Journal of hazardous materials, 250, pp.318-332. https://doi.org/10.1016/j.jhazmat.2013.01.063

Feizi, H., Kamali, M., Jafari, L., & Moghaddam, P.R. (2013). Phytotoxicity and stimulatory impacts of nanosized and bulk titanium dioxide on fennel (Foeniculum vulgare Mill). Chemosphere, 91(4), pp.506-511. https://doi.org/10.1016/j.chemosphere.2012.12.012

Frazier, T.P., Burklew, C.E., & Zhang, B. (2014). Titanium dioxide nanoparticles affect the growth and microRNA expression of tobacco (Nicotiana tabacum). Functional & integrative genomics, 14(1), pp.75-83. https://doi.org/10.1007/s10142-013-0341-4

Gill, S.S., & Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant physiology and biochemistry, 48(12), pp.909-930. https://doi.org/10.1016/j.plaphy.2010.08.016

Gupta, U.C., Kening, W.U., & Liang, S. (2008). Micronutrients in soils, crops, and livestock. Earth Science Frontiers, 15(5), pp.110-125. https://doi.org/10.1016/S1872-5791(09)60003-8

Hernandez-Viezcas, J.A., Castillo-Michel, H., Servin, A.D., Peralta-Videa, J.R., & Gardea-Torresdey, J.L. (2011). Spectroscopic verification of zinc absorption and distribution in the desert plant Prosopis juliflora-velutina (velvet mesquite) treated with ZnO nanoparticles. Chemical engineering journal, 170(2-3), pp.346-352. https://doi.org/10.1016/j.cej.2010.12.021

Huang, J., Sun, S., Xu, D., Lan, H., Sun, H., Wang, Z., Bao, Y., Wang, J., Tang, H., & Zhang, H. (2012). A TFIIIA-type zinc finger protein confers multiple abiotic stress tolerances in transgenic rice (Oryza sativa L.). Plant molecular biology, 80(3), pp.337-350. https://doi.org/10.1007/s11103-012-9955-5

Khodakovskaya, M.V., De Silva, K., Biris, A.S., Dervishi, E., & Villagarcia, H. (2012). Carbon nanotubes induce growth enhancement of tobacco cells. ACS nano, 6(3), pp.2128-2135. https://doi.org/10.1021/nn204643g

Kim, J.J., & Kim, W.Y. (2013). Purification and characterization of polyphenol oxidase from fresh ginseng. Journal of ginseng research, 37(1), p.117-123. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3659630/pdf/grosbr-37-117.pdf

Kim, M.K., Lee, J.S., Kim, K.Y., & Lee, H.G. (2013). Ascorbyl palmitate-loaded chitosan nanoparticles: characteristic and polyphenol oxidase inhibitory activity. Colloids and Surfaces B: Biointerfaces, 103, pp.391-394. https://doi.org/10.1016/j.colsurfb.2012.09.038

Kozlov, M.V. (2005). Pollution resistance of mountain birch, (Betula pubescens) subsp. czerepanovii, near the copper–nickel smelter: natural selection or phenotypic acclimation?. Chemosphere, 59(2), pp.189-197. https://doi.org/10.1016/j.chemosphere.2004.11.010

Krishnaraj, C., Jagan, E.G., Ramachandran, R., Abirami, S.M., Mohan, N., & Kalaichelvan, P.T. (2012). Effect of biologically synthesized silver nanoparticles on (Bacopa monnieri) (Linn.) Wettst. plant growth metabolism. Process biochemistry, 47(4), pp.651-658. https://doi.org/10.1016/j.procbio.2012.01.006

Kumar, V., Kumari, A., Guleria, P., & Yadav, S.K. (2012). Evaluating the toxicity of selected types of nano-chemicals. In Reviews of environmental contamination and toxicology (pp. 39-121). Springer, New York, NY. https://doi.org/10.1007/978-1-4614-1463-6_2

Lee, W.M., Kwak, J.I., & An, Y.J. (2012). Effect of silver nanoparticles in crop plants Phaseolus radiatus and Sorghum bicolor: media effect on phytotoxicity. Chemosphere, 86(5), pp.491-499. https://doi.org/10.1016/j.chemosphere.2011.10.013

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(3), pp.273-279. https://doi.org/10.1016/j.chemosphere.2009.10.050

MacAdam, J.W., Nelson, C.J., & Sharp, R.E. (1992). Peroxidase activity in the leaf elongation zone of tall fescue: I. Spatial distribution of ionically bound peroxidase activity in genotypes differing in length of the elongation zone. Plant Physiology, 99(3), pp.872-878. https://doi.org/10.1104/pp.99.3.872

Mizobutsi, G.P., Finger, F.L., Ribeiro, R.A., Puschmann, R., Neves, L.L.D.M., & Mota, W.F.D. (2010). Effect of pH and temperature on peroxidase and polyphenol oxidase activities of litchi pericarp. Scientia Agricola, 67(2), pp.213-217. https://doi.org/10.1590/S0103-90162010000200013

Moser, B.R., Zheljazkov, V.D., Bakota, E.L., Evangelista, R.L., Gawde, A., Cantrell, C.L., Winkler-Moser, J.K., Hristov, A.N., Astatkie, T., & Jeliazkova, E. (2014). Method for obtaining three products with different properties from fennel (Foeniculum vulgare) seed. Industrial crops and products, 60, pp.335-342. https://doi.org/10.1016/j.indcrop.2014.06.017

Nair, P.M.G., & Chung, I.M. (2014). A mechanistic study on the toxic effect of copper oxide nanoparticles in soybean (Glycine max L.) root development and lignification of root cells. Biological trace element research, 162(1-3), pp.342-352. https://doi.org/10.1007/s12011-014-0106-5

Nair, R., Varghese, S.H., Nair, B.G., Maekawa, T., Yoshida, Y., & Kumar, D.S. (2010). Nano particulate material delivery to plants. Plant science, 179(3), pp.154-163. https://doi.org/10.1016/j.plantsci.2010.04.012

Nguyen, T., Aparicio, M., & Saleh, M. (2015). Accurate mass GC/LC-quadrupole time of flight mass spectrometry analysis of fatty acids and triacylglycerols of spicy fruits from the Apiaceae family. Molecules, 20(12), pp.21421-21432. https://doi.org/10.3390/molecules201219779

Pollard, A.J., Powell, K.D., Harper, F.A., & Smith, J.A.C. (2002). The genetic basis of metal hyper accumulation in plants. Critical reviews in plant sciences, 21(6), pp.539-566. https://doi.org/10.1080/0735-260291044359

Poonam, T., Tanushree, B., & Sukalyan, C. (2013). Water quality indices-important tools for water quality assessment: a review. International Journal of Advances in chemistry, 1(1), pp.15-28. https://s3.amazonaws.com/academia.edu.documents

Raymond, J., Rakariyatham, N., & Azanza, J.L. (1993). Purification and some properties of polyphenoloxidase from sunflower seeds. Phytochemistry, 34(4), pp. 927-931. https://doi.org/10.1016/S0031-9422(00)90689-7

Rather, M.A., Dar, B.A., Sofi, S.N., Bhat, B.A., & Qurishi, M.A. (2016). (Foeniculum vulgare): A comprehensive review of its traditional use, phytochemistry, pharmacology, and safety. Arabian Journal of Chemistry, 9, pp. S1574-S1583. https://doi.org/10.1016/j.arabjc.2012.04.011

Rico, C.M., Majumdar, S., Duarte-Gardea, M., Peralta-Videa, J.R., & Gardea-Torresdey, J.L. (2011). Interaction of nanoparticles with edible plants and their possible implications in the food chain. Journal of agricultural and food chemistry, 59(8), pp.3485-3498. https://doi.org/10.1021/jf104517j

Rico, C.M., Peralta-Videa, J.R., & Gardea-Torresdey, J.L. (2015). Differential effects of cerium oxide nanoparticles on rice, wheat, and barley roots: A Fourier Transform Infrared (FT-IR) micro spectroscopy study. Applied spectroscopy, 69(2), pp.287-295. https://doi.org/10.1366/14-07495

Saeidian, S., & Ghasemifar, E. (2013). Effect of temperature on guaiacol Peroxidase of (Pyrus communis). International Letters of Natural Sciences, (5), 46-51. https://doi.org/10.18052/www.scipress.com/ILNS.5.46

Saison, C., Perreault, F., Daigle, J.C., Fortin, C., Claverie, J., Morin, M., & Popovic, R. (2010). Effect of core–shell copper oxide nanoparticles on cell culture morphology and photosynthesis (photosystem II energy distribution) in the green alga, (Chlamydomonas reinhardtii). Aquatic toxicology, 96(2), pp.109-114. https://doi.org/10.1016/j.aquatox.2009.10.002

Seregin, I., & Kozhevnikova, A.D. (2006). Physiological role of nickel and its toxic effects on higher plants. Russian Journal of Plant Physiology, 53(2), pp.257-277. https://doi.org/10.1134/S1021443706020178

Siddiqui, M.H., Al-Whaibi, M.H., Firoz, M., & Al-Khaishany, M.Y. (2015). Role of nanoparticles in plants. In Nanotechnology and Plant Sciences (pp. 19-35). Springer, Cham. https://doi.org/10.1007/978-3-319-14502-0_2

Smirnova, G.V., Vysochina, G.I., Muzyka, N.G., Samoylova, Z.Y., Kukushkina, T.A., & Oktyabrsky, O.N. (2010). Evaluation of antioxidant properties of medical plants using microbial test systems. World Journal of Microbiology and Biotechnology, 26(12), pp.2269-2276. https://doi.org/10.1007/s11274-010-0417-4

Soares, C., Branco-Neves, S., de Sousa, A., Pereira, R., & Fidalgo, F. (2016). Eco toxicological relevance of nano-NiO and acetaminophen to (Hordeum vulgare L.): combining standardized procedures and physiological endpoints. Chemosphere, 165, pp.442-452. https://doi.org/10.1016/j.chemosphere.2016.09.053

Sunkar, R. (2010). October. MicroRNAs with macro-effects on plant stress responses. In Seminars in cell & developmental biology (Vol. 21, No. 8, pp. 805-811). Academic Press. https://doi.org/10.1016/j.semcdb.2010.04.001

Suriyaprabha, R., Karunakaran, G., Kavitha, K., Yuvakkumar, R., Rajendran, V., & Kannan, N. (2013). Application of silica nanoparticles in maize to enhance fungal resistance. IET nanobiotechnology, 8(3), pp.133-137. https://doi.org/10.1049/iet-nbt.2013.0004

Syu, Y.Y., Hung, J.H., Chen, J.C., & Chuang, H.W. (2014). Impacts of size and shape of silver nanoparticles on Arabidopsis plant growth and gene expression. Plant physiology and biochemistry, 83, pp.57-64. https://doi.org/10.1016/j.plaphy.2014.07.010

Taiz, L., Zeiger, E., Møller, I.M., & Murphy, A. (2015). Plant physiology and development. https://www.forskningsdatabasen.dk/en/catalog/2524903221

Tarrahi, R., Khataee, A., Movafeghi, A., Rezanejad, F., & Gohari, G. (2017). Toxicological implications of selenium nanoparticles with different coatings along with Se4+ on (Lemna minor). Chemosphere, 181, pp.655-665. https://doi.org/10.1016/j.chemosphere.2017.04.142

Tiwari, P.K., Singh, A.K., Singh, V.P., Prasad, S.M., Ramawat, N., Tripathi, D.K., Chauhan, D.K., & Rai, A.K. (2019). Liquid assisted pulsed laser ablation synthesized copper oxide nanoparticles (CuO-NPs) and their differential impact on rice seedlings. Ecotoxicology and Environmental Safety, 176, pp.321-329. https://doi.org/10.1016/j.ecoenv.2019.01.120

Torbati, S. (2018). Phytotoxicological Effects of Bulk-NiO and NiO Nanoparticles on Lesser and Giant Duckweeds as Model Macrophytes: Changes in the Plants Physiological Responses. Iranian Journal of Toxicology, 12(4), pp.31-39. http://ijt.arakmu.ac.ir/article-1-690-en.pdf

Tripathi, D.K., Singh, S., Singh, S., Pandey, R., Singh, V.P., Sharma, N.C., Prasad, S.M., Dubey, N.K., & Chauhan, D.K. (2017). An overview on manufactured nanoparticles in plants: uptake, translocation, accumulation and phytotoxicity. Plant Physiology and Biochemistry, 110, pp.2-12. https://doi.org/10.1016/j.plaphy.2016.07.030

Tripathi, D.K., Singh, S., Singh, V.P., Prasad, S.M., Chauhan, D.K., & Dubey, N.K. (2016). Silicon nanoparticles more efficiently alleviate arsenate toxicity than silicon in maize cultivar and hybrid differing in arsenate tolerance. Frontiers in Environmental Science, 4, p.46. https://doi.org/10.3389/fenvs.2016.00046

Velikova, M., Bankova, V., Sorkun, K., Houcine, S., Tsvetkova, I., & Kujumgiev, A. (2000). Propolis from the Mediterranean region: chemical composition and antimicrobial activity. Zeitschrift für Naturforschung C, 55(9-10), pp.790-793. https://doi.org/10.1515/znc-2000-9-1019

Wang, X., Han, H., Liu, X., Gu, X., Chen, K., & Lu, D. (2012). Multi-walled carbon nanotubes can enhance root elongation of wheat (Triticum aestivum) plants. Journal of Nanoparticle Research, 14(6), p.841. https://doi.org/10.1007/s11051-012-0841-5

Watanabe, S., Kojima, K., Ide, Y., & Sasaki, S. (2000). Effects of saline and osmotic stress on proline and sugar accumulation in (Populus euphratica) in vitro. Plant Cell, Tissue and Organ Culture, 63(3), p.199. https://doi.org/10.1023/A:1010619503680

Wei, L., Thakkar, M., Chen, Y., Ntim, S.A., Mitra, S., & Zhang, X. (2010). Cytotoxicity effects of water dispersible oxidized multiwalled carbon nanotubes on marine alga, Dunaliella tertiolecta. Aquatic Toxicology, 100(2), pp.194-201. https://doi.org/10.1016/j.aquatox.2010.07.001

Yang, L., & Watts, D.J. (2005). Particle surface characteristics may play an important role in phytotoxicity of alumina nanoparticles. Toxicology Letters, 158(2) pp.122-132. https://doi.org/10.1016/j.toxlet.2005.03.003

Yruela, I. (2005). Copper in plants. Brazilian Journal of Plant Physiology, 17(1), pp.145-156. https://doi.org/10.1590/S1677-04202005000100012

Zafar, H., Ali, A., Ali, J.S., Haq, I.U., & Zia, M. (2016). Effect of ZnO nanoparticles on Brassica nigra seedlings and stem explants: growth dynamics and antioxidative response. Frontiers in plant science, 7, p.535. https://doi.org/10.3389/fpls.2016.00535

Zhang, P., Cui, H.X., Zhang, Z.J., & Zhong, R.G. (2008). Effects of nano-TiO2 photo semiconductor on photosynthesis of cucumber plants. Chinese Agricultural Science Bulletin, 24 pp.230-233. http://en.cnki.com.cn/Article_en/CJFDTotal-ZNTB200808051.htm

DOI: https://doi.org/10.22146/agritech.55643

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