Growth and antioxidant system responses of maize (Zea mays L.) seedling to different concentration of pyrene in a controlled environment

Authors

  • Mahdieh HOUSHANI Department of Plant Sciences, Faculty of Natural Sciences, University of Tabriz, Tabriz, Iran
  • Seyed Yahya SALEHI-LISAR Department of Plant Sciences, Faculty of Natural Sciences, University of Tabriz, Tabriz, Iran
  • Ali MOVAFEGHI Department of Plant Sciences, Faculty of Natural Sciences, University of Tabriz, Tabriz, Iran
  • Ruhollah MOTAFAKKERAZAD Department of Plant Sciences, Faculty of Natural Sciences, University of Tabriz, Tabriz, Iran

DOI:

https://doi.org/10.14720/aas.2019.113.1.03

Keywords:

PAHs, physiological responses, pollution, toxicity

Abstract

Polycyclic aromatic hydrocarbons (PAHs) are a class of organic pollutants effecting different aspects of plants physiology. To assess the physiological responses of plants to PAHs, maize (Zea mays) was treated with 25, 50, 75, and 100 ppm of pyrene and after 21 days, the activity of some antioxidant enzymes, malondialdehyde (MDA), total flavonoid, total anthocyanin, and soluble sugar contents were measured in shoots and roots of plants. Pyrene led to increase MDA content as well as CAT, POD, and SOD activities. Increase in pyrene concentration reduced all studied growth variables and significantly increased photosynthetic pigments contents of plants. Soluble sugar content was significantly higher in the shoot, while that was reduced in the roots through increasing of pyrene concentration (p < 0.05). Also, the increase of pyrene concentration decreased total flavonoid content compared to anthocyanin content. In conclusion, these findings supported the hypothesis that pyrene toxicity induces oxidative stress in the maize plant and it also increases the antioxidant systems in order to moderating stress condition. However, the antioxidant system of maize was not strong enough to eliminate all produced ROS at high concentrations, thus this caused oxidative damage to the plant and decreased its growth variables.

References

Alberet, R.S., & Thornber, J.P. (1977). Water stress effects on content and organization of chlorophyll in mesophyll and bundle sheath chloroplast of maize. Plant Physiology, 59, 351-353. https://doi.org/10.1104/pp.59.3.351

Alkio, M., Tabuchi, T.M., Wang, X. (2005). Stress responses to polycyclic aromatic hydrocarbons in Arabidopsis include growth inhibition and hypersensitive response-like symptoms. Journal Experimental Botany, 56, 2983-2994. https://doi.org/10.1093/jxb/eri295

Alscher, R.G., Donahue, J.L., Cramer, C.L. (1997). Reactive oxygen species and antioxidant: Relationships in green cells. Plant Physiology, 100, 224-233. https://doi.org/10.1111/j.1399-3054.1997.tb04778.x

Boominathan, R., & Doran, P.M. (2002). Ni induced oxidative stress in root of the Ni hyper accumulator Alyssum bertoloni. New Phytologist, 156, 202-205. https://doi.org/10.1046/j.1469-8137.2002.00506.x

Binet, P., Portal, J.M., Leyval, C. (2000). Fate of polycyclic aromatic hydrocarbons (PAHs) in the rhizosphere and mycorrhizosphere of ryegrass. Plant and Soil, 227, 207-213. https://doi.org/10.1023/A:1026587418611

Bradford, M.M. (1976). A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1), 248-254. https://doi.org/10.1016/0003-2697(76)90527-3

Branquinho, C., Brown, D.H., Catarino, F. (1997). The cellular location of Cu in lichens and its effects on membrane integrity and chlorophyll fluorescence. Environmental and Experimental Botany, 38, 165-179. https://doi.org/10.1016/S0098-8472(97)00015-4

Chance, B., & Mealy, A.C. (1955). Assay of catalases and peroxidases. Methods Enzymology, 11, 764-755. https://doi.org/10.1016/S0076-6879(55)02300-8

Chang, C., Yang, M., Wen, H., Chern, J. (2002). Estimation of total flavonoid content in propolis by two complementary colorimetric methods. Journal of Food and Drug Analysis, 10, 178-182.

Chiang, P., Li, K.P., Hseu, T.M. (1996). Spectrochemical behavior of carcinogenic polycyclic aromatic hydrocarbons in biological systems. Part II: a theoretical rate model for BaP metabolism in living cells. Applied Spectroscopy, 50, 1352–1359. https://doi.org/10.1366/0003702963904782

Collins, C., Fryer, M., Grosso, A. (2006). Plant uptake of nonionic organic chemicals. Environmental Science and Technology, 40, 45-52. https://doi.org/10.1021/es0508166

Dupuy, J., Legliz, P., Vincent, Q., Zelko, I., Mustin, Ch., Ouvard, S., Sterckeman, T. (2016). Effect and localization of phenanthrene in maiz roots. Chemospher, 149, 130-136. https://doi.org/10.1016/j.chemosphere.2016.01.102

Dupuy, J., Ouvrard, S., Leglize, P., Sterckeman, T. (2015). Morphological and physiological responses of maize (Zea mays) exposed on sand contaminated by phenanthrene. Chemosphere, 124, 110-115. https://doi.org/10.1016/j.chemosphere.2014.11.051

Fuxing, K., Dongsheng, C., Yanzheng, G., Yi, Z. (2010). Distribution of polycyclic aromatic hydrocarbons in subcellular root tissues of ryegrass. BMC Plant Biology, 10, 210-216. https://doi.org/10.1186/1471-2229-10-210

Gao, Y., & Zhu, L. (2004). Plant uptake, accumulation and translocation of phenanthrene and pyrene in soils. Chemosphere, 55, 1169-1178. https://doi.org/10.1016/j.chemosphere.2004.01.037

Gong, Z., Alef, A., Wilke, B., Li, P. (2007). Activated Carbon Adsorption of PAHs from Vegetable Oil Used in Soil Remediation. Journal of Hazardous Materials, 143, 372-378. https://doi.org/10.1016/j.jhazmat.2006.09.037

Hartmut, K. L. (1987). Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. In R. D. Lester Packer (Ed.), Methods in enzymology. New York, NY: Academic Press. pp: 350-382.

Houshani, M., Salehi-Lisar, S.Y., Motafakkerazad, R., Movafeghi, A. (2019). Uptake and distribution of phenanthrene and pyrene in roots and shoots of maize (Zea mays L.). Environmental Science and Pollution Research, Published online. https://doi.org/10.1007/s11356-019-04371-3

Hung, H., & Mackay, D. (1997). A novel and simple model of the uptake of organic chemicals by vegetation from air and soil. Chemosphere, 35, 959-977. https://doi.org/10.1016/S0045-6535(97)00182-3

Khan, S., Aijun, L., Zhang, S., Hu, Q., Zhu, Y. (2008). Accumulation of polycyclic aromatic hydrocarbons and heavy metals in lettuce grown in the soils contaminated with long-term wastewater irrigation. Journal of Hazardous Materials, 152, 506-515. https://doi.org/10.1016/j.jhazmat.2007.07.014

Kochert, A. (1978). Carbohydrate determination by phenol-sulfuric acid method. In: J.A. Hellebust and J.S. Craige, Editors, Handbook of physiology and biochemical methods, Cambridge University Press, London, pp: 95-97.

Kosnar, Z., Mercl, F., Tlustos, P. (2018). Ability of natural attenuation and phytoremediation using maize (Zea mays L.) to decrease soil contents of polycyclic aromatic hydrocarbons (PAHs) derived from biomass fly ash in comparison with PAHs–spiked soil. Ecotoxicology and Environmental Safety, 153, 16-22. https://doi.org/10.1016/j.ecoenv.2018.01.049

Kummerova, M., Zezulka, S., Babula, P., Vanova, L. (2013). Root response in Pisum sativum and Zea mays under fluoranthene stress: Morphological and anatomical traits. Chemosphere, 90, 665-673. https://doi.org/10.1016/j.chemosphere.2012.09.047

Kummerova, M., Zezulka, S., Vanova, L., Fiserova, H. (2012). Effect of organic pollutant treatment on the growth of pea and maize seedlings. Central European Journal Biology, 7(1), 159-166. https://doi.org/10.2478/s11535-011-0081-1

Lang-Mladek, C., Popova, O., Kiok, K., Berlinger, M., Rakic, B., Aufastez, W. (2010). Transgenerational inheritance and resetting of stressinduced loss of epigenetic gene silencing in Arabidopsis. Molecular Plant, 3, 594-602 https://doi.org/10.1093/mp/ssq014

Li, F., Zeng, X., Yang, J., Zhou, K., Zan, Q., Lei, A., Tam, N.F.Y. (2014). Contamination of polycyclic aromatic hydrocarbons (PAHs) in surface sediments and plants of Mangroveswamps in Shenzhen, China. Marine Pollution Bulletin, 85(2), 590-596. https://doi.org/10.1016/j.marpolbul.2014.02.025.

Liao, Ch., Xu, W., Lu, G., Liang, X., Guo, Ch., Yang, Ch., Dang, Z. (2015). Accumulation of hydrocarbons by maize (Zea mays L.) in remediation of soils contaminated with crude oil. International Journal of Phytoremediation, 17, 693-700. https://doi.org/10.1080/15226514.2014.964840

Liu, H., Weisman, D., Yuan-bei, Y., Cui, B., Huang, Y., Colon-Carmona, A., Wang, Z. (2009). An oxidative stress response to polycyclic aromatic hydrocarbon exposure is rapid and complex in Arabidopsis thaliana. Plant Science, 176(3), 375- 382. https://doi.org/10.1016/j.plantsci.2008.12.002

Lundstedt, S. (2003). Analysis of PAHs and their transformation products in contaminated soil and remedial processes. Solfjadern Offset AB.Umea University, pp:3-5.

Mita, S., Murano, N., Akaike, M., Nakamura, K. (1997). Mutants of Arabidopsis thaliana with pleiotropic effects on the expression of the gen for beta-amylase and on the accumulation of anthocyanin that is inducible by sugars. Plant Journal, 11, 841-851. https://doi.org/10.1046/j.1365-313X.1997.11040841.x

Obinger, C., Maj, M., Nicholls, P., Loewen, P. (1997). Activity, peroxide compound formation, and hemed synthesis in Escherichia coli HPII catalase. Archives Biochemistry Biophysics, 342(1), 58-67. https://doi.org/10.1006/abbi.1997.9988

Rolland, F., Baena-Gonzalez, E., Sheen, J. (2006). Sugar sensing and signaling in plants: conserved and novel mechanisms. Annual Review of Plant Biology, 57, 675-709. https://doi.org/10.1146/annurev.arplant.57.032905.105441

Salehi-Lisar, S.Y., & Deljoo, S. (2015). Physiological effect of phenanthrene on Triticum aestivum L., Helianthus annus and Medicago sativa. EurAsian Journal BioSciences, 9, 29-37. https://doi.org/10.1080/23311932.2015.1020189

Tomar, R.S., & Jajoo, A. (2014). Fluoranthene, a polycyclic aromatic hydrocarbon, inhibits light as well as dark reactions of photosynthesis in wheat (Triticum aestivum L.). Ecotoxicology and Environmental Safety, 109, 110-115. https://doi.org/10.1016/j.ecoenv.2014.08.009

Watts, A.W., Ballestero, T.P., Gardner, K.H. (2006). Uptake of polycyclic aromatic hydrocarbons (PAHs) in salt marsh plants Spartina alterniflora grown in contaminated sediments. Chemosphere, 62(8), 1253-1260. https://doi.org/10.1016/j.chemosphere.2005.07.006

Wilcke, W. (2000). Polycyclic Aromatic Hydrocarbons (PAHs) in soil. Journal of Plant Nutrition and Soil Science, 163, 229-248. https://doi.org/10.1002/1522-2624(200006)163:3<229::AID-JPLN229>3.0.CO;2-6

Wilson, S.C., & Jones, K.C. (1993). Bioremediation of soil contaminated with polynuclear aromatic hydrocarbons (PAHs). Environmental Pollution, 81, 229-249. https://doi.org/10.1016/0269-7491(93)90206-4

Winterbourn, C.C., Mc Grath, B.W., Carrell, R.W. (1976). Reactions involving superoxide and normal unstable hemoglobins. Biochemical Journal, 155, 493-502. https://doi.org/10.1042/bj1550493

Xu, Sh.Y., Chen, Y.X., Wu, W.X., Zheng, Sh.J., Xue, Sh.G., Yang, Sh.Y., Peng, Y.J. (2007). Protein changes in response to pyrene stress in maize (Zea mays L.) leaves. Journal Integrative Plant Biology, 49(2), 187-19. https://doi.org/10.1111/j.1744-7909.2007.00284.x

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Published

1. 04. 2019

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Section

Agronomy section

How to Cite

HOUSHANI, M., SALEHI-LISAR, S. Y., MOVAFEGHI, A., & MOTAFAKKERAZAD, R. (2019). Growth and antioxidant system responses of maize (Zea mays L.) seedling to different concentration of pyrene in a controlled environment. Acta Agriculturae Slovenica, 113(1), 29–39. https://doi.org/10.14720/aas.2019.113.1.03

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