Cytochrome P450 monooxygenase specific activity reduction in wheat Triticum aestivum induced by soil roxithromycin stress

Abstract

Roxithromycin, as widely used medicine and livestock growth promoter, arouses concern because its occurrence and persistence in soil environments. However, effects of roxithromycin in higher plants are still vague. Accordingly, we hypothesized that roxithromycin-contaminated soil may exhibits ecotoxicological effects in wheat (Triticum aestivum). In this study, effects induced by a gradient concentration of roxithromycin stress (0.01, 0.1, 1, 10, and 100 mg·kg⁻¹) was investigated in a 7-d soil test in T. aestivum. Results indicated that the specific activity of cytochrome P450 (CYP450) monooxygenase was decreased dramatically with the concentration of roxithromycin in soil. The IC₅₀ value was 8.78 mg·kg⁻¹ of roxithromycin. On the contrary, the growth related endpoints (i.e., the germination percentage, the biomass and the height), the content related endpoints (i.e., soluble protein content and CYP450 content), and the superoxide dismutase (SOD) activity failed to reveal the roxithromycin-induced effects. Further analysis revealed that the CYP450 monooxygenase specific activity reduction was enzymatic mechanism mediated, other than oxidative stress induced. We conclude that the soil roxithromycin declined the CYP450 monooxygenase activity in T. aestivum by the inhibition of the enzymatic mechanism. Further efforts can include, but are not limited to, investigation of joint effects induced by combined exposure of roxithromycin and the pesticides and evaluation of the similar effects in other higher plants.

Keywords

roxithromycin / toxic effect / cytochrome P450 monooxygenase / soil environment / Triticum aestivum / biomarker

References

[1] Zhou Q X. Ecology of Combined Pollution. Beijing: China Environmental Science Press, 1995 (in Chinese)

[2] Yu B, Wang X, Yu S, Li Q, Zhou Q. Effects of roxithromycin on ammonia-oxidizing bacteria and nitrite-oxidizing bacteria in the rhizosphere of wheat. Applied Microbiology and Biotechnology, 2014, 98(1): 263–272

[3] Schlüsener M P, von Arb M A, Bester K. Elimination of macrolides, tiamulin, and salinomycin during manure storage. Archives of Environmental Contamination and Toxicology, 2006, 51(1): 21–28

[4] Schlüsener M P, Bester K. Persistence of antibiotics such as macrolides, tiamulin and salinomycin in soil. Environmental Pollution, 2006, 143(3): 565–571

[5] Kumar K, Gupta S, Chander Y, Singh A K. Antibiotic use in agriculture and its impact on the terrestrial environment. Advances in Agronomy, 2005, 87(1): 1–54

[6] Walsh C. Antibiotics: Actions, Origins, Resistance. 1st ed. Washington, DC: ASM Press, 2003, 145–163

[7] Luo Y, Mao D, Rysz M, Zhou Q, Zhang H, Xu L, Alvarez P. Trends in antibiotic resistance genes occurrence in the Haihe River, China. Environmental Science & Technology, 2010, 44(19): 7220–7225

[8] Villa P, Sassella D, Corada M, Bartosek I. Toxicity, uptake, and subcellular distribution in rat hepatocytes of roxithromycin, a new semisynthetic macrolide, and erythromycin base. Antimicrobial Agents and Chemotherapy, 1988, 32(10): 1541–1546

[9] Chang H R, Pechere J C. Effect of roxithromycin on acute toxoplasmosis in mice. Antimicrobial Agents and Chemotherapy, 1987, 31(7): 1147–1149

[10] Choi K, Kim Y, Jung J, Kim M H, Kim C S, Kim N H, Park J. Occurrences and ecological risks of roxithromycin, trimethoprim, and chloramphenicol in the Han River, Korea. Environmental Toxicology and Chemistry, 2008, 27(3): 711–719

[11] Yin C Y, Luo Y M, Teng Y, Zhang H B, Chen Y S, Zhao Y G. Pollution characteristics and accumulation of antibiotics in typical protected vegetable soils. Environmental Sciences, 2012, 33(8): 2810–2816

[12] d<?Pub Caret?>e Liguoro M, Cibin V, Capolongo F, Halling-Sørensen B, Montesissa C. Use of oxytetracycline and tylosin in intensive calf farming: evaluation of transfer to manure and soil. Chemosphere, 2003, 52(1): 203–212

[13] Tamaoki J, Kadota J, Takizawa H. Clinical implications of the immunomodulatory effects of macrolides. American Journal of Medicine Supplements, 2004, 117(9 Suppl 9A): 5S–11S

[14] Zhou Q X, Kong F X, Zhu L. Introduction to Ecotoxicology. Beijing: Science Press, 2004 (in Chinese)

[15] Newhouse K E, Smith W A, Starrett M A, Schaefer T J, Singh B K. Tolerance to imidazolinone herbicides in wheat. Plant Physiology, 1992, 100(2): 882–886

[16] Christopher J T, Powles S B, Liljegren D R, Holtum J A. Cross-resistance to herbicides in annual ryegrass (Lolium rigidum) : II. chlorsulfuron resistance involves a wheat-like detoxification system. Plant Physiology, 1991, 95(4): 1036–1043

[17] Hurt R A, Qiu X, Wu L, Roh Y, Palumbo A V, Tiedje J M, Zhou J. Simultaneous recovery of RNA and DNA from soils and sediments. Applied and Environmental Microbiology, 2001, 67(10): 4495–4503

[18] Masubuchi Y, Horie T. Toxicological significance of mechanism-based inactivation of cytochrome p450 enzymes by drugs. Critical Reviews in Toxicology, 2007, 37(5): 389–412

[19] Murray M. Drug-mediated inactivation of cytochrome P450. Clinical and Experimental Pharmacology & Physiology, 1997, 24(7): 465–470

[20] Bonjoch N, Tamayo P. Protein Content Quantification by Bradford Method, Handbook of Plant Ecophysiology Techniques. Berlin: Springer, 2011, 283–295

[21] Li X X, Song Y F, Yang D L, Zhang W, Song X Y. Cytochorme P450 in wheat as a biomarker for diagnosing pollution in soil. Environmental Chemistry, 2006, 25(3): 284–287 (in Chinese)

[22] Xiang W S, Wang X J, Ren T R. Expression of a wheat cytochrome P450 monooxygenase cDNA in yeast catalyzes the metabolism of sulfonylurea herbicides. Pesticide Biochemistry and Physiology, 2006, 85(1): 1–6

[23] Lin D, Xie X, Zhou Q, Liu Y. Biochemical and genotoxic effect of triclosan on earthworms (Eisenia fetida) using contact and soil tests. Environmental Toxicology, 2012, 27(7): 385–392

[24] Chen Y M, Hu X G, Jing S, Zhou Q X. Specific nanotoxicity of graphene oxide during zebrafish embryogenesis. Nanotoxicology, online on February 23, 2015,

[25] Coon M J, Ding X X, Pernecky S J, Vaz A D. Cytochrome P450: progress and predictions. FASEB Journal, 1992, 6(2): 669–673

[26] Goksøyr A. A semi-quantitative cytochrome P450IA1 ELISA: a simple method for studying the monooxygenase induction response in environmental monitoring and ecotoxicological testing of fish. Science of the Total Environment, 1991, 101(3): 255–262

[27] Xiao R, Wang J, Chen J, Sun L, Chen Y. Effects of arecoline on hepatic cytochrome P450 activity and oxidative stress. Journal of Toxicological Sciences, 2014, 39(4): 609–614

[28] Dupont I, Bodénez P, Berthou F, Simon B, Bardou L G, Lucas D. Cytochrome P-450 2E1 activity and oxidative stress in alcoholic patients. Alcohol and Alcoholism (Oxford, Oxfordshire), 2000, 35(1): 98–103

[29] Carillon J, Rouanet J M, Cristol J P, Brion R. Superoxide dismutase administration, a potential therapy against oxidative stress related diseases: several routes of supplementation and proposal of an original mechanism of action. Pharmaceutical Research, 2013, 30(11): 2718–2728

[30] Hu X, Mu L, Kang J, Lu K, Zhou R, Zhou Q. Humic acid acts as a natural antidote of graphene by regulating nanomaterial translocation and metabolic fluxes in vivo. Environmental Science & Technology, 2014, 48(12): 6919–6927

Acknowledgements

This research is financially supported by the National Natural Science Foundation of China as a general project (Grant No. 31170473) and a joint Guangdong project (No. U1133006), and by the Ministry of Education of China as an innovative team project (No. IRT 13024).

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