Biologia plantarum 64: 110-118, 2020 | DOI: 10.32615/bp.2019.095

Di-n-butyl phthalate-induced phytotoxicity in Hordeum vulgare seedlings and subsequent antioxidant defense response

A. KUMARI, R. KAUR*
Department of Botanical and Environmental Sciences, Guru Nanak Dev University
Amritsar-143005, Punjab, India

Di-n-butyl phthalate (DBP) is one of the frequently detected phthalates in environmental samples. The effects of phthalates are extensively studied in the animals but the effects on plants are scarce. Therefore, the present study is aimed to envisage the effects of DBP on the antioxidative defense system in Hordeum vulgare L. seedlings grown under laboratory conditions for 7 d. The activities of different antioxidative enzymes were enhanced in the shoots. In the roots, the activity of guaiacol peroxidase increased and the catalase activity decreased initially but increased at higher DBP concentrations, whereas the activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase declined. Furthermore, the content of polyphenols elevated after exposure of seedlings to DBP. The possible reason for these responses of barley seedlings is the oxidative burst, i.e., enhanced production of reactive oxygen species, which were confirmed using confocal microscopy in terms of loss in plasma membrane integrity. DBP also disturbed the normal stomatal morphology of barley seedlings. The study may help to provide insights into the defense of crop plants against phthalate stress.

Keywords: barley, confocal microscopy, plasma membrane integrity, SEM, stomata

Received: December 6, 2018; Revised: April 7, 2019; Accepted: July 26, 2019; Published online: February 18, 2020Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
KUMARI, A., & KAUR, R. (2020). Di-n-butyl phthalate-induced phytotoxicity in Hordeum vulgare seedlings and subsequent antioxidant defense response. Biologia plantarum64, 110-118. doi: 10.32615/bp.2019.095.
Download citation

Supplementary files

Download fileKumari 6025Suppl.pdf

File size: 163.16 kB

References

  1. Abbas, G., Murtaza, B., Bibi, I., Shahid, M., Niazi, N., Khan, M., Amjad, M., Hussain, M.: Arsenic uptake, toxicity, detoxification, and speciation in plants: physiological, biochemical, and molecular aspects. - Int. J. Environ. Res. Public Health 15: 59, 2018. Go to original source...
  2. Aebi, H. Catalase in vitro. - Methods Enzymol. 105: 121-126, 1984. Go to original source...
  3. Ahmad, R.: Basics of free radicals and antioxidants. - In: Ahmad, R. (ed.): Free Radicals, Antioxidants and Diseases. Pp. 1-5. IntechOpen, London 2018. Go to original source...
  4. Anjum, N.A., Ahmad, I., Mohmood, I., Pacheco, M., Duarte, A.C., Pereira, E., Umar, S., Ahmad, A., Khan, N.A., Iqbal M., Prasad, M.N.V.: Modulation of glutathione and its related enzymes in plants' responses to toxic metals and metalloids. - Environ. exp. Bot. 75: 307-324, 2012.
  5. Bai, R., Ma, F., Liang, D., Zhao, X.: Phthalic acid induces oxidative stress and alters the activity of some antioxidant enzymes in roots of Malus prunifolia. - J. chem. Ecol. 35: 488-494, 2009. Go to original source...
  6. Benjamin, S., Masai, E., Kamimura, N., Takahashi, K., Anderson, R.C., Faisal, P.A.: Phthalates impact human health: epidemiological evidences and plausible mechanism of action. - J. Hazard Mater. 340: 360-383, 2017. Go to original source...
  7. Berwal, M., Ram, C.: Superoxide dismutase: a stable biochemical marker for abiotic stress tolerance in higher plants. - In: de Oliveira, A.B. (ed.): Abiotic and Biotic Stress in Plants. Pp. 1-10. IntechOpen, London 2018.
  8. Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. - Anal. Biochem. 72: 248-254, 1976. Go to original source...
  9. Cai, Q.Y., Mo, C.H., Wu, Q.T., Zeng, Q.Y., Katsoyiannis, A.: Occurrence of organic contaminants in sewage sludges from eleven wastewater treatment plants, China. - Chemosphere 68: 1751-1762, 2007. Go to original source...
  10. Carlberg, I., Mannervik, B. Glutathione reductase. - Methods Enzymol. 133: 484-490, 1985. Go to original source...
  11. Cheng, L.J., Cheng, T.S.: Oxidative effects and metabolic changes following exposure of greater duckweed (Spirodela polyrhiza) to diethyl phthalate. - Aquat. Toxicol. 109: 166-175, 2012. Go to original source...
  12. Choudhary, R., Saroha, A.E., Swarnkar, P.L.: Effect of abscisic acid and hydrogen peroxide on antioxidant enzymes in Syzygium cumini plant. - J. Food Sci. Technol. 49: 649-652, 2012. Go to original source...
  13. Corpas, F.J., Gupta, D.K., Palma, J.M.: Production sites of reactive oxygen species (ROS) in organelles from plant cells. - In: Gupta, D., Palma, J., Corpas, F.J. (ed.): Reactive Oxygen Species and Oxidative Damage in Plants under Stress. Pp. 1-22. Springer, Cham 2015. Go to original source...
  14. Czarnocka, W., Karpiński, S.: Friend or foe? Reactive oxygen species production, scavenging and signaling in plant response to environmental stresses. - Free Radical Biol. Med. 122: 4-20, 2018. Go to original source...
  15. Díaz, J., Bernal, A., Pomar, F., Merino, F.: Induction of shikimate dehydrogenase and peroxidase in pepper (Capsicum annuum L.) seedlings in response to copper stress and its relation to lignification. - Plant Sci. 161: 179-188, 2001.
  16. Dixon, R.A., Paiva, N.L.: Stress-induced phenylpropanoid metabolism. - Plant Cell 7: 1085-1097, 1995.
  17. Flügel, F., Timm, S., Arrivault, S., Florian, A., Stitt, M., Fernie, A.R., Bauwe, H.: The photorespiratory metabolite 2-phosphoglycolate regulates photosynthesis and starch accumulation in Arabidopsis. - Plant Cell 29: 2537-2551, 2017. Go to original source...
  18. Foyer, C.H., Noctor, G.: Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. - Plant Cell 17: 1866-1875, 2005.
  19. Gao, M., Dong, Y., Zhong, Z., Song, W., Qi, Y.: Growth and antioxidant defence responses of wheat to di-n-butyl phthalate and di(2-ethylhexyl) phthalate stress. - Chemosphere 172: 418-428, 2017. Go to original source...
  20. Gao, M., Liu, Y., Dong, Y., Song, Z.: Photosynthetic and antioxidant response of wheat to di (2-ethylhexyl) phthalate (DEHP) contamination in the soil. - Chemosphere 209: 258-267, 2018. Go to original source...
  21. Gao, M., Liu, Y., Dong, Y., Song, Z.: Physiological responses of wheat planted in fluvo-aquic soils to di (2-ethylhexyl) and di-n-butyl phthalates. - Environ. Pollut. 244: 774-782, 2019. Go to original source...
  22. Guo, Y., Kannan, K.: Challenges encountered in the analysis of phthalate esters in foodstuffs and other biological matrices. - Anal. Bioanal. Chem. 404: 2539-2554, 2012. Go to original source...
  23. He, L., Gielen, G., Bolan, N.S., Zhang, X., Qin, H., Huang, H., Wang, H.: Contamination and remediation of phthalic acid esters in agricultural soils in China: a review. - Agron. Sustain. Dev. 35: 519-534, 2015. Go to original source...
  24. Jiménez-Arias, D., García-Machado, F.J., Morales-Sierra, S., Suárez, E., Pérez, J.A., Luis, J.C., Garrido-Orduña, C., Herrera, A.J., Valdés, F., Sandalio, L.M., Borges, A.A.: Menadione sodium bisulphite (MSB): beyond seed-soaking. Root pretreatment with MSB primes salt stress tolerance in tomato plants. - Environ. exp. Bot. 157: 161-170, 2019. Go to original source...
  25. Jovanović, S.V., Kukavica, B., Vidović, M., Morina, F., Menckhoff, L.: Class III peroxidases: functions, localization and redox regulation of isoenzymes. - In: Gupta, D., Palma, J., Corpas, F.J. (ed.): Antioxidants and Antioxidant Enzymes in Higher Plants. Pp. 269-300. Springer, Cham 2018. Go to original source...
  26. Kanojia, A., Dijkwel, P.P.: Abiotic stress responses are governed by reactive oxygen species and age. - Annu. Plant Rev. 1: 1-32, 2018. Go to original source...
  27. Kaur, R.: Growth and biochemical and antimutagenic studies on Chlorophytum borivilianum Sant et Fernand. - Ph.D. Thesis, Department of Botanical and Environmental Sciences, Guru Nanak Dev University, Amritsar (Punjab), India, 2013.
  28. Khorobrykh, S.A., Karonen, M., Tyystjärvi, E.: Experimental evidence suggesting that H2O2 is produced within the thylakoid membrane in a reaction between plastoquinol and singlet oxygen. - FEBS Lett. 589: 779-786, 2015. Go to original source...
  29. Kong, S., Ji, Y., Liu, L., Chen, L., Zhao, X., Wang, J., Bai, Z., Sun, Z.: Diversities of phthalate esters in suburban agricultural soils and wasteland soil appeared with urbanization in China. - Environ. Pollut 170: 161-168, 2012. Go to original source...
  30. Kono, Y., Takahashi, M.A., Asada, K.: Superoxide dismutases from kidney bean leaves. - Plant Cell Physiol. 20: 1229-1235, 1979. Go to original source...
  31. Kumari, A., Kaur, R.: Germination and early growth toxicity to barley seedlings (Hordeum vulgare L.) under di-n-butyl phthalate (DBP) stress. - J. Pharm. Sci. Res. 9: 2361-2366, 2017.
  32. Kumari, A., Kaur, R., Sharma, R., Kaur, R.: Assessment of toxicological effects of di-n-butyl phthalate to a cereal crop (Hordeum vulgare L.). - J. Adv. Agric. Technol. 6: 20-26, 2019. Go to original source...
  33. Li, Y., Zhang, X., Yang, Y., Duan, B.: Soil cadmium toxicity and nitrogen deposition differently affect growth and physiology in Toxicodendron vernicifluum seedlings. - Acta Physiol. Plant. 35: 529-540, 2013. Go to original source...
  34. Liao, C.S., Chen, L.C., Chen, B.S., Lin, S.H.: Bioremediation of endocrine disruptor di-n-butyl phthalate ester by Deinococcus radiodurans and Pseudomonas stutzeri. - Chemosphere 78: 342-346, 2010. Go to original source...
  35. Liu, D., Jiang, W., Qinghen, M., Liu, Q., Li, H., Gao, X., Guo, S.: Observation of root tips of garlic (Allium sativum L.) by electron microscopy after treatment with cadmium. - Isr. J. Plant Sci. 48: 289-295, 2000. Go to original source...
  36. Ma, T., Christie, P., Teng, Y., Luo, Y.: Rape (Brassica chinensis L.) seed germination, seedling growth, and physiology in soil polluted with di-n-butyl phthalate and bis (2-ethylhexyl) phthalate. - Environ. Sci. Pollut. Res. 20: 5289-5298, 2013. Go to original source...
  37. Ma, Y., Wang, P., Wang, M., Sun, M., Gu, Z., Yang, R.: GABA mediates phenolic compounds accumulation and the antioxidant system enhancement in germinated hulless barley under NaCl stress. - Food Chem 270: 593-601, 2019. Go to original source...
  38. Michalak, A.: Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. - Pol. J. environ. Stud. 15: 523-530, 2006.
  39. Naczk, M., Shahidi, F. Extraction and analysis of phenolics in food. - J. Chromatogr. A 1054: 95-111, 2004. Go to original source...
  40. Nakano, Y., Asada, K. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. - Plant Cell Physiol. 22: 867-880, 1981.
  41. Putter, J. Peroxidases. - In: Bergmeyer, H.U. (ed.): Methods of Enzymatic Analysis. 2nd Ed. Vol. 2. Pp. 685-690. Academic Press, New York 1974. Go to original source...
  42. Sasaki, M., Yamamoto, Y., Ma, J.F., Matsumoto, H.: Early events induced by aluminium stress in elongating cells of wheat root. - In: Ando, T., Fujita, K., Mae, T., Matsumoto, H., Mori, S., Sekiya, J. (ed.): Plant Nutrition for Sustainable Food Production and Environment. Pp. 439-444. Springer, Dordrecht 1997. Go to original source...
  43. Sharma, P., Jha, A.B., Dubey, R.S., Pessarakli, M.: Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. - J. Bot. 2012: 217037, 2012. Go to original source...
  44. Shi, H., Jiang, C., Ye, T., Tan, D.X., Reiter, R.J., Zhang, H., Liu, R., Chan, Z.: Comparative physiological, metabolomic, and transcriptomic analyses reveal mechanisms of improved abiotic stress resistance in Bermudagrass [Cynodon dactylon (L). Pers.] by exogenous melatonin. - J. exp. Bot. 66: 681-694, 2015. Go to original source...
  45. Smirnoff, N., Arnaud, D.: Hydrogen peroxide metabolism and functions in plants. - New Phytol. 221: 1197-1214, 2019. Go to original source...
  46. Ma, T.T., Christie, P., Luo, Y.M., Teng, Y.: Physiological and antioxidant responses of germinating mung bean seedlings to phthalate esters in soil. - Pedosphere 24: 107-115, 2014. Go to original source...
  47. Wang, J., Luo, Y., Teng, Y., Ma, W., Christie, P., Li, Z.: Soil contamination by phthalate esters in Chinese intensive vegetable production systems with different modes of use of plastic film. - Environ. Pollut. 180: 265-273, 2013a Go to original source...
  48. Wang, W., Zhang, Y., Wang, S., Fan, C. Q., Xu, H.: Distributions of phthalic esters carried by total suspended particulates in Nanjing, China. - Environ. Monitor. Assess. 184: 6789-6798, 2012. Go to original source...
  49. Wang, X., Lin, Q., Wang, J., Lu, X., Wang, G.: Effect of wetland reclamation and tillage conversion on accumulation and distribution of phthalate esters residues in soils. - Ecol. Eng. 51: 10-15, 2013b. Go to original source...
  50. Waraich, E.A., Ahmad, R., Halim, A., Aziz, T. Alleviation of temperature stress by nutrient management in crop plants. - J. Soil Sci. Plant Nutr. 12: 221-244, 2012. Go to original source...
  51. Welinder, K.G.: Superfamily of plant, fungal and bacterial peroxidases. - Curr. Opin. Struct. Biol. 2: 388-393, 1992. Go to original source...
  52. Weschler, C.J., Salthammer, T., Fromme, H.: Partitioning of phthalates among the gas phase, airborne particles and settled dust in indoor environments. - Atm. Environ. 42: 1449-1460, 2008. Go to original source...
  53. Wright, J.S., Johnson, E.R., DiLabio, G.A. Predicting the activity of phenolic antioxidants: theoretical method, analysis of substituent effects, and application to major families of antioxidants. - J. amer. chem. Soc. 123: 1173-1183, 2001. Go to original source...
  54. Yadav, P., Kaur, R., Kohli, S.K., Sirhindi, G., Bhardwaj, R.: Castasterone assisted accumulation of polyphenols and antioxidant to increase tolerance of B. juncea plants towards copper toxicity. - Cogent Food Agr. 2: 1276821, 2016. Go to original source...
  55. Yang, S., Huang, C., Wu, Z., Hu, J., Li, T., Liu, S., Jia, W.: Stomatal movement in response to long distance-communicated signals initiated by heat shock in partial roots of Commelina communis L. - Science in China Series C 49: 18-25, 2006. Go to original source...
  56. Yin, R., Lin, X.G., Wang, S.G., Zhang, H.Y.: Effect of DBP/DEHP in vegetable planted soil on the quality of Capsicum fruit. - Chemosphere 50: 801-805, 2003. Go to original source...
  57. Yin, R., Lin, X.G., Wang, S. G., Zhang, H.Y.: Influence of phthalic acid esters in vegetable garden soil on quality of capsicum fruit. - Agro Environ. Protocols 21: 1-4, 2002.
  58. Zhang, Y., Du, N., Wang, L., Zhang, H., Zhao, J., Sun, G., Wang, P. Physical and chemical indices of cucumber seedling leaves under dibutyl phthalate stress. - Environ. Sci. Pollut. Res. 22: 3477-3488, 2015. Go to original source...
  59. Zhang, Y., Wang, L., Du, N., Ma, G., Yang, A., Zhang, H., Wang, Z., Song, Q.: Effects of diethyl phthalate and di-(2-ethyl) hexylphthalate on the physiology and ultrastructure of cucumber seedlings. - Environ. Sci. Pollut. Res. 21: 1020-1028, 2014. Go to original source...
  60. Zhang, Y., Zhang, H., Sun, X., Wang, L., Du, N., Tao, Y., Sun, G., Erinle, K.O., Wang, P., Zhou, C., Duan, S.: Effect of dimethyl phthalate (DMP) on germination, antioxidant system, and chloroplast ultrastructure in Cucumis sativus L. - Environ. Sci. Pollut. Res. 23: 1183-1192, 2016. Go to original source...