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Responses of morphological, physiological, and biochemical characteristics of maize (Zea mays L.) seedlings to atrazine stress

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Abstract

Atrazine is a synthetic herbicide applied to control broadleaf weeds in different crops. In many parts of the world, atrazine is mainly applied for controlling weeds in maize fields. However, studies on the possible adverse effects of atrazine on maize crop can hardly be found in literature. The present study was therefore conducted to evaluate the effect of atrazine on different characteristics of maize seedlings including germination, growth, chlorophyll contents, soluble sugars, proteins and proline levels, ions accumulation, cell viability, and cell injury. In addition, the effects of atrazine on reactive oxygen species (ROS) accumulation and antioxidant enzymes activities in maize seedlings were estimated. It was found that at high concentration, atrazine slightly but significantly inhibited seed germination and growth of maize seedlings. Light-harvesting pigments (chlorophylls a and b, and total carotenoids) exhibited a higher sensitivity to atrazine and were negatively impacted by atrazine at doses above 50 ppm. Atrazine caused an increase in soluble sugars at all tested doses and decrease in soluble proteins at the highest tested dose. Exposure of maize seedlings to atrazine resulted in an increased cell injury and decreased cell viability. Atrazine did not affect the concentration of Na+, K+, and Ca2+ ions in maize seedlings to any greater extent; however, some minor changes were observed in some cases. An increase in the stress marker, proline, was found upon exposure to atrazine. The observed effects of atrazine in maize seedlings can be attributed to oxidative stress as revealed by an increase in H2O2 content and higher activities of peroxidase (POD), superoxide dismutase (SOD), and catalase (CAT) enzymes in atrazine-treated seedlings. The present investigation concludes that atrazine has the potential to adversely affect germination and growth of maize seedlings by inducing oxidative stress that causes increased cell injury and decreased cell viability as well as impairs the concentration of light-harvesting pigments.

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References

  • Akbulut, G. B., & Yigit, E. (2010). The changes in some biochemical parameters in Zea mays cv.“Martha F1” treated with atrazine. Ecotoxicology and Environmental Safety, 73(6), 1429–1432.

    Google Scholar 

  • Aladesanwa, R., Adenawoola, A., & Olowolafe, O. (2001). Effects of atrazine residue on the growth and development of celosia (Celosia argentea) under screenhouse conditions in Nigeria. Crop Protection, 20(4), 321–324.

    CAS  Google Scholar 

  • Alla, M. N., & Hassan, N. (2006). Changes of antioxidants levels in two maize lines following atrazine treatments. Plant Physiology and Biochemistry, 44(4), 202–210.

    Google Scholar 

  • Asare-Boamah, N. K., & Fletcher, R. A. (1983). Physiological and cytological effects of BAS 9052 OH on corn (Zea mays) seedlings. Weed Science, 31(1), 49–55.

    CAS  Google Scholar 

  • ASTDR. (2003). Atrazine: potential for human exposure. Agency for Toxic Substances and Disease Registry (ATSDR), U.S. https://www.atsdr.cdc.gov/toxprofiles/tp153.pdf. Accessed June 1, 2018.

  • Azmat, R., & Uddin, F. (2005). The inhibition of bean plant metabolism by CD metal and atrazine: II. The inhibition of bioremediation of atrazine in heavy metal environment and it’s effect on mineral nutrients of bean plant. Biotechnology, 4(4), 262–266.

    CAS  Google Scholar 

  • Badr, A., Zaki, H., Germoush, M. O., Tawfeek, A. Q., & El-Tayeb, M. A. (2013). Cytophysiological impacts of Metosulam herbicide on Vicia faba plants. Acta Physiologiae Plantarum, 35(6), 1933–1941.

    CAS  Google Scholar 

  • Bates, L. S., Waldren, R. P., & Teare, I. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil, 39(1), 205–207.

    CAS  Google Scholar 

  • Blanco, F. M. G., de Almeida, S. D. B., & Matallo, M. B. (2013). Herbicide—soil interactions, applied to maize crop under Brazilian conditions (p. 47). Herbicides: Current Research and Case Studies in Use.

    Google Scholar 

  • Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2), 248–254.

    CAS  Google Scholar 

  • Canakci-Gulengul, S., Kirecci, O. A., & Karabulut, F. (2019). Changes based on oxidative stress in metolachlor and atrazine treated maize seedlings. Pakistan Journal of Botany, 51(2), 421–426.

    CAS  Google Scholar 

  • Chance, B., & Maehly, A. (1955). Assay of catalases and peroxidases. Methods in Enzymology, 2, 764–775.

    Google Scholar 

  • Cheng, M., Zeng, G., Huang, D., Lai, C., Xu, P., Zhang, C., Liu, Y., Wan, J., Gong, X., & Zhu, Y. (2016). Degradation of atrazine by a novel Fenton-like process and assessment the influence on the treated soil. Journal of Hazardous Materials, 312, 184–191.

    Google Scholar 

  • Chhokar, R., Sharma, R., Gill, S., & Singh, R. (2019). Mesotrione and atrazine combination to control diverse weed flora in maize. Indian Journal of Weed Science, 51(2), 145–150.

    Google Scholar 

  • de Campos Ventura, B., de Angelis, D. D. F., & Marin-Morales, M. A. (2008). Mutagenic and genotoxic effects of the atrazine herbicide in Oreochromis niloticus (Perciformes, Cichlidae) detected by the micronuclei test and the comet assay. Pesticide Biochemistry and Physiology, 90(1), 42–51.

    Google Scholar 

  • Dey, P. (1990). Oligosaccharides. In Methods in plant biochemistry (Vol. 2, pp. 189–218). Elsevier.

  • El-Tayeb, M., & Zaki, H. (2009). Cytophysiological response of Vicia faba to a glyphosate-based herbicide. American-Eurasian J Agronomy, 2(3), 168–175.

    Google Scholar 

  • EPA. (2015). Pesticides: topical and chemical fact sheets: atrazine. http://www.epa.gov/pesticides/factsheets/atrazine_background.htm.

  • European Commission. (2004). 2004/248/EC: Commission Decision of 10 March 2004 concerning the non-inclusion of atrazine in Annex I to Council Directive 91/414/EEC and the withdrawal of authorisations for plant protection products containing this active substance (Text with EEA relevance) (notified under document number C(2004) 731).

  • Feng, J., Liu, A., & Zhu, W. (2017). Toxic effects of atrazine on reproductive and immune systems in animal models. Reproductive System & Sexual Disorders: Current Research, 6(2), 208.

    Google Scholar 

  • Gala, W. R., & Giesy, J. P. (1990). Flow cytometric techniques to assess toxicity to algae. In Aquatic toxicology and risk assessment: thirteenth volume (pp. 237-246): ASTM International.

  • Gao, Y., Fang, J., Zhang, J., Ren, L., Mao, Y., Li, B., Zhang, M., Liu, D., & du, M. (2011). The impact of the herbicide atrazine on growth and photosynthesis of seagrass, Zostera marina (L.), seedlings. Marine Pollution Bulletin, 62(8), 1628–1631.

    CAS  Google Scholar 

  • Gao, Y., Fang, J., Du, M., Fang, J., Jiang, W., & Jiang, Z. (2017). Response of the eelgrass (Zostera marina L.) to the combined effects of high temperatures and the herbicide, atrazine. Aquatic Botany, 142, 41–47.

    CAS  Google Scholar 

  • Giannopolitis, C. N., & Ries, S. K. (1977). Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology, 59(2), 309–314.

    CAS  Google Scholar 

  • 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), 909–930.

    CAS  Google Scholar 

  • Gonçalves, M. W., de Campos, C. B. M., Batista, V. G., da Cruz, A. D., de Marco Junior, P., Bastos, R. P., et al. (2017). Genotoxic and mutagenic effects of Atrazine Atanor 50 SC on Dendropsophus minutus Peters, 1872 (Anura: Hylidae) developmental larval stages. Chemosphere, 182, 730–737.

    Google Scholar 

  • Hare, P., Du Plessis, S., Cress, W., & Van Staden, J. (1996). Stress-induced changes in plant gene expression. Prospects for enhancing agricultural productivity in South Africa. South African Journal of Science, 92(9), 431–439.

    CAS  Google Scholar 

  • Harinasut, P., Poonsopa, D., Roengmongkol, K., & Charoensataporn, R. (2003). Salinity effects on antioxidant enzymes in mulberry cultivar. Science Asia, 29(2), 109–113.

    CAS  Google Scholar 

  • Ivanov, S., Alexieva, V., & Karanov, E. (2005). Cumulative effect of low and high atrazine concentrations on Arabidopsis thaliana plants. Russian Journal of Plant Physiology, 52(2), 213–219.

    CAS  Google Scholar 

  • Jiang, Z., Su, G., Li, J., Ma, B., Chen, Y., Shan, D., & Zhang, Y. (2018). Toxicological sensitivity of Pennisetum americanum (L.) K. Schum to atrazine exposure. International Journal of Phytoremediation, 20(7), 635–642.

    CAS  Google Scholar 

  • Knievel, D. P. (1973). Procedure for estimating ratio of live to dead root dry matter in root core samples 1. Crop Science, 13(1), 124–126.

    Google Scholar 

  • Li, X., Wu, T., Huang, H., & Zhang, S. (2012). Atrazine accumulation and toxic responses in maize Zea mays. Journal of Environmental Sciences, 24(2), 203–208.

    Google Scholar 

  • Lichtenthaler, H. K., & Wellburn, A. R. (1983). Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Portland Press Limited.

  • Nakajima, Y., Yoshida, S., & Ono, T.-a. (1996). Differential effects of urea/triazine-type and phenol-type photosystem II inhibitors on inactivation of the electron transport and degradation of the D1 protein during photoinhibition. Plant and Cell Physiology, 37(5), 673–680.

  • Oliveira, H. C., Stolf-Moreira, R., Martinez, C. B., Sousa, G. F., Grillo, R., de Jesus, M. B., et al. (2015). Evaluation of the side effects of poly (epsilon-caprolactone) nanocapsules containing atrazine toward maize plants. Frontiers in Chemistry, 3, 61.

    Google Scholar 

  • Owolabi, O. D., & Omotosho, J. S. (2017). Atrazine-mediated oxidative stress responses and lipid peroxidation in the tissues of Clarias gariepinus. Iranian Journal of Toxicology Volume, 11(2).

  • Pallant, E., & Miller, C. (1998). Atrazine suppression of fine root growth in corn. In Root demographics and their efficiencies in sustainable agriculture, grasslands and forest ecosystems (pp. 499-505): Springer.

  • Pang, S., Duan, L., Liu, Z., Song, X., Li, X., & Wang, C. (2012). Co-induction of a glutathione-S-transferase, a glutathione transporter and an ABC transporter in maize by xenobiotics. PLoS One, 7(7), e40712.

    CAS  Google Scholar 

  • Parveen, R., Shaukat, S. S., & Naqvi, I. I. (2002). Effect of atrazine on carbohydrates, potassium, sodium, phosphate and amino acid contents in bean Vigna radiata (L.) Wilczek. Asian Journal of Plant Sciences, 1(5), 552–553.

    Google Scholar 

  • Pathak, R. K., & Dikshit, A. K. (2012). Effect of various environmental parameters on biosorptive removal of atrazine from WaterEnvironment. International Journal of Environmental Science and Development, 3(3), 289.

    CAS  Google Scholar 

  • Qian, H., Tsuji, T., Endo, T., & Sato, F. (2014). PGR5 and NDH pathways in photosynthetic cyclic electron transfer respond differently to sublethal treatment with photosystem-interfering herbicides. Journal of Agricultural and Food Chemistry, 62(18), 4083–4089.

    CAS  Google Scholar 

  • Rodrigues, B. N., & Almeida, F. (2011). Guia de herbicidas. 6ª. Londrina, PR.

  • Sergiev, I. G., Alexieva, V. S., Ivanov, S. V., Moskova, I. I., & Karanov, E. N. (2006). The phenylurea cytokinin 4PU-30 protects maize plants against glyphosate action. Pesticide Biochemistry and Physiology, 85(3), 139–146.

    CAS  Google Scholar 

  • Shakir, S. K., Kanwal, M., Murad, W., ur Rehman, Z., ur Rehman, S., Daud, M., et al. (2016). Effect of some commonly used pesticides on seed germination, biomass production and photosynthetic pigments in tomato (Lycopersicon esculentum). Ecotoxicology, 25(2), 329–341.

    CAS  Google Scholar 

  • Shaukat, S. (1976). Effects of simazine, atrazine and 2, 4 D on respiration rate, sugar level and amylase activity during germination of Pinus nigra var. calabrica Schneid. Pakistan Journal of Botany, 8(1), 37–45.

    CAS  Google Scholar 

  • Singh, S., Kumar, V., Chauhan, A., Datta, S., Wani, A. B., Singh, N., et al. (2018). Toxicity, degradation and analysis of the herbicide atrazine. Environmental Chemistry Letters, 16(1), 211–237.

    CAS  Google Scholar 

  • Sulmon, C., Gouesbet, G., Couée, I., & El Amrani, A. (2004). Sugar-induced tolerance to atrazine in Arabidopsis seedlings: interacting effects of atrazine and soluble sugars on psbA mRNA and D1 protein levels. Plant Science, 167(4), 913–923.

    CAS  Google Scholar 

  • Velikova, V., Yordanov, I., & Edreva, A. (2000). Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Science, 151(1), 59–66.

    CAS  Google Scholar 

  • Wang, S., He, X., & An, R. (2010). Responses of growth and antioxidant metabolism to nickel toxicity in Luffa cylindrica seedlings. Journal of Animal and Plant Sciences (JAPS), 7(2), 810–821.

    Google Scholar 

  • Wang, Q., Que, X., Zheng, R., Pang, Z., Li, C., & Xiao, B. (2015). Phytotoxicity assessment of atrazine on growth and physiology of three emergent plants. Environmental Science and Pollution Research, 22(13), 9646–9657.

    CAS  Google Scholar 

  • Weber, G., Christmann, N., Thiery, A.-C., Martens, D., & Kubiniok, J. (2018). Pesticides in agricultural headwater streams in southwestern Germany and effects on macroinvertebrate populations. Science of the Total Environment, 619, 638–648.

    Google Scholar 

  • Wirbisky, S. E., Weber, G. J., Schlotman, K. E., Sepúlveda, M. S., & Freeman, J. L. (2016). Embryonic atrazine exposure alters zebrafish and human miRNAs associated with angiogenesis, cancer, and neurodevelopment. Food and Chemical Toxicology, 98, 25–33.

    CAS  Google Scholar 

  • Xing, H., Li, S., Wang, Z., Gao, X., Xu, S., & Wang, X. (2012). Oxidative stress response and histopathological changes due to atrazine and chlorpyrifos exposure in common carp. Pesticide Biochemistry and Physiology, 103(1), 74–80.

    CAS  Google Scholar 

  • Yang, G., Rhodes, D., & Joly, R. J. (1996). Effects of high temperature on membrane stability and chlorophyll fluorescence in glycinebetaine-deficient and glycinebetaine-containing maize lines. Functional Plant Biology, 23(4), 437–443.

    CAS  Google Scholar 

  • Yazdanpak, A., Amiri, A., Faghihi, K., & Karimian, N. (2014). The residual effect of herbicides on the germination and early growth of Shiraz wheat cultivar in the development of healthy agricultural crops. American-Eurasian Journal of Agricultural & Environmental Sciences, 14(2), 161–164.

    CAS  Google Scholar 

  • Yuan, B., Liang, S., Jin, Y.-X., Zhang, M.-J., Zhang, J.-B., & Kim, N.-H. (2017). Toxic effects of atrazine on porcine oocytes and possible mechanisms of action. PLoS One, 12(6), e0179861.

    Google Scholar 

  • Zhang, J. J., Lu, Y. C., & Yang, H. (2014a). Chemical modification and degradation of atrazine in Medicago sativa through multiple pathways. Journal of Agricultural and Food Chemistry, 62(40), 9657–9668.

    CAS  Google Scholar 

  • Zhang, J. J., Lu, Y. C., Zhang, J. J., Tan, L. R., & Yang, H. (2014b). Accumulation and toxicological response of atrazine in rice crops. Ecotoxicology and Environmental Safety, 102, 105–112.

    Google Scholar 

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Acknowledgments

Authors acknowledge all staff at the Department of Botanical & Environmental Sciences and Department of Biotechnology & Genetic Engineering, KUST for their help.

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The study was financially supported by the Higher Education Commission (HEC) of Pakistan through the Startup Research Grant Program.

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Correspondence to Azizullah Azizullah.

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The study was a part of M. Phil thesis of Shagufta Bibi submitted to the Department of Botany, KUST.

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Bibi, S., Khan, S., Taimur, N. et al. Responses of morphological, physiological, and biochemical characteristics of maize (Zea mays L.) seedlings to atrazine stress. Environ Monit Assess 191, 717 (2019). https://doi.org/10.1007/s10661-019-7867-4

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