Phytotoxicity in seven higher plant species exposed to di-n-butyl phthalate or bis (2-ethylhexyl) phthalate

Abstract

We investigated phytotoxicity in seven plant species exposed to a range of concentrations (0– 500 mg·kg⁻¹ soil) of di-n-butyl phthalate (DnBP) or bis (2-ethylhexyl) phthalate (DEHP), two representative phthalate esters (PAEs) nominated by USEPA as priority pollutants and known environmental estrogens. We studied seed germination, root elongation, seedling growth, biomass (fresh weight, FW) and malondialdehyde (MDA) content of shoots and roots of wheat (Triticum aestivum L.), alfalfa (Medicago sativa L.), perennial ryegrass (Lolium perenne), radish (Raphanus sativus L.), cucumber (Cucumis sativus L.), oat (Avena sativa) and onion (Allium cepa L.), together with monitoring of plant pigment content (chlorophyll a, b and carotinoids) in alfalfa, radish and onion shoots. Root elongation, seedling growth and biomass of the test species were generally inhibited by DnBP but not by DEHP, indicating a lower level of phytotoxicity of DEHP than of DnBP. MDA contents of four species were promoted by PAE exposure, but not in alfalfa, ryegrass or onion shoots, indicating lower sensitivity of these three species to PAE pollutants. Plant pigment contents were clearly affected under the stress of both pollutants, implying the potential damage to the photosynthetic system of test plants, mainly by decreasing the content of chlorophyll a and b. Results of DnBP and DEHP phytotoxicity to the primary growth of test plants has provided information for the assessment of their environmental risk in the soil and also forms a basis for the further analysis of their toxic effects over the whole growth period of different plant species.

Graphical abstract

Keywords

phytotoxicity / di- n-butyl phthalate / bis(2-ethylhexyl) phthalate / malondialdehyde / plant pigments (chlorophyll a / b and carotinoids)

References

[1] Scholz N. Ecotoxicity and biodegradation of phthalate monoesters. Chemosphere, 2003, 53(8): 921–926

[2] Liu W L, Shen C F, Zhang Z, Zhang C B. Distribution of phthalate esters in soil of e-waste recycling sites from Taizhou city in China. Bulletin of Environmental Contamination and Toxicology, 2009, 82(6): 665–667

[3] Zeng F, Cui K Y, Xie Z Y, Wu L N, Luo D L, Chen L X, Lin Y J, Liu M, Sun G X. Distribution of phthalate esters in urban soils of subtropical city, Guangzhou, China. Journal of Hazardous Materials, 2009, 164(2–3): 1171–1178

[4] Vikelsøe J, Thomsen M, Carlsen L. Phthalates and nonylphenols in profiles of differently dressed soils. Science of the Total Environment, 2002, 296(1–3): 105–116

[5] Gibson R, Wang M J, Padgett E, Beck A J. Analysis of 4-nonylphenols, phthalates, and polychlorinated biphenyls in soils and biosolids. Chemosphere, 2005, 61(9): 1336–1344

[6] Hu X X, Han Z H, Liu B Y, Zhang F B, Li F, Wang W H. Distribution of phthalic acid esters in environment and its toxicity. Environmental Science and Management, 2007, 32(1): 37–40

[7] Schowanek D, Carr R, David H, Douben P, Hall J, Kirchmann H, Patria L, Sequi P, Smith S, Webb S. A risk-based methodology for deriving quality standards for organic contaminants in sewage sludge for use in agriculture—Conceptual Framework. Regulatory Toxicology and Pharmacology, 2004, 40(3): 227–251

[8] Chang L W, Meier J R, Smith M K. Application of plant and earthworm bioassays to evaluate remediation of a lead-contaminated soil. Archives of Environmental Contamination and Toxicology, 1997, 32(2): 166–171

[9] An Q, Jin W, Li Y, Xu R W. Influence of plasticizer PAEs to the soil-plant system. Acta Pedologica Sinica, 1999, 2(1): 118–126 (in Chinese)

[10] 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-Environmental Protection, 2002, 21(1): 1–4 (in Chinese)

[11] Liao C S, Yen J H, Wang Y S. Growth inhibition in Chinese cabbage (Brassica rapa var. chinensis) growth exposed to di-n-butyl phthalate. Journal of Hazardous Materials, 2009, 163(2–3): 625– 631

[12] US Environmental Protection Agency. 1996. Ecological Effects Test Guidelines (OPPTS 850.4200): Seed Germination / Root Elongation Toxicity Test.

[13] Wang X D, Sun C, Gao S X, Wang L S, Shuokui H. Validation of germination rate and root elongation as indicator to assess phytotoxicity with Cucumis sativus. Chemosphere, 2001, 44(8): 1711–1721

[14] Zhang C G, Leung K K, Wong Y S, Tam N F Y. Germination, growthand physiological responses of mangrove plant (Bruguiera gymnorrhiza) to lubricating oil pollution. Environmental and Experimental Botany, 2007, 60(1): 127–136

[15] Lichtenthaler H K, Wellburn A R. Determination of total carotenoids and chlorophyls a and b of leaf extracts in different solvents. Biochemical Society Transactions, 1983, 603(11): 591–592

[16] Wang W, Keturi P H. Comparative seed germination tests using ten plant species for toxicity assessment of metals engraving effluent sample. Water, Air, and Soil Pollution, 1990, 52(3–4): 369–376

[17] Kordan H A. Seed viability and germination: a multi-purpose experimental system. Journal of Biological Education, 1992, 26(4): 247–251

[18] Moore M T, Huggett D B, Huddleston G M III, Rodgers J H Jr, Cooper C M. Herbicide effects on Typha latifolia (Linneaus) germination and root and shoot development. Chemosphere, 1999, 38(15): 3637–3647

[19] Munzuroglu O, Geckil H. Effects of metals on seed germination, root elongation, and coleoptile and hypocotyl growth in Triticum aestivum and Cucumis sativus. Archives of Environmental Contamination and Toxicology, 2002, 43(2): 203–213

[20] Murata M R, Hammes P S, Zharare G E. Effect of solution pH and calcium concentration on germination and early growth of groundnut. Journal of Plant Nutrition, 2003, 26(6): 1247–1262

[21] Lin D H, Xing B S. Phytotoxicity of nanoparticles: inhibition of seed germination and root growth. Environmental Pollution, 2007, 150(2): 243–250

[22] Zheng Z, He P J, Shao L M, Lee D J. Phthalic acid esters in dissolved fractions of landfill leachates. Water Research, 2007, 41(20): 4696–4702

[23] Xu X R, Li X Y. Adsorption behavior of dibutyl phthalate on marine sediments. Marine Pollution Bulletin, 2008, 57(6–12): 430–408

[24] Shiota K, Chou M J, Nishimura H. Embryotoxic effects of di-2-ethylhexyl phthalate (DEHP) and di-n-buty phthalate (DBP) in mice. Environmental Research, 1980, 22(1): 245–253

[25] Defoe D L, Holcombe G W, Hammermeister D E, Biesinger K E. Solubility and toxicity of eight phthalate esters to four aquatic organisms. Environmental Toxicology and Chemistry, 1990, 9(5): 623–636

[26] Staples C A, Adams W J, Parkerton T F, Gorsuch J W, Biddinger G R, Reinert K H. Aquatic toxicity of eighteen phthalate esters. Environmental Toxicology and Chemistry, 1997, 16(5): 875–891

[27] Roslev P, Vorkamp K, Aarup J, Frederiksen K, Nielsen P H. Degradation of phthalate esters in an activated sludge wastewater treatment plant. Water Research, 2007, 41(5): 969–976

[28] Liu Y, Guan Y T, Yang Z H, Cai Z H, Mizuno T, Tsuno H, Zhu W P, Zhang X H. Toxicity of seven phthalate esters to embryonic development of the abalone Haliotis diversicolor supertexta. Ecotoxicology (London, England), 2009, 18(3): 293–303

[29] Santibáñez C, Verdugo C, Ginocchio R. Phytostabilization of copper mine tailings with biosolids: implications for metal uptake and productivity of Lolium perenne. Science of the Total Environment, 2008, 395(1): 1–10

[30] Story K B. Oxidative stress: animal adaptations in nature. Brazilian Journal of Medical and Biological Research, 2006, 29(12): 1715–1733

[31] Jones G J, Nichols P D, Johns B, Smith J D. The effect of mercury and cadmiumon the fatty acid and sterol composition of the marine diatom Asterionella glacialis. Phytochemistry, 1987, 26(5): 1343–1348

[32] Gupta M, Sinha S, Chandra P. Copper-induced toxicity in aquatic macrophyte, Hydrilla verticillata: effect of pH. Ecotoxicology (London, England), 1996, 5(1): 23–33

[33] Singh S, Eapen S, D’Souza S F. Cadmium accumulation and its influence on lipid peroxidation and antioxidative system in an aquatic plant, Bacopa monnieri L. Chemosphere, 2006, 62(2): 233–246

[34] Zou T J, Li T X, Zhang X Z, Yu H Y, Luo H B. Lead accumulation and tolerance characteristics of Athyrium wardii (Hook.) as a potential phytostabilizer. Journal of Hazardous Materials, 2011, 186(1): 683–689

[35] Wang S H, Yang Z M, Lu B, Li S Q, Lu Y P. Copper induced stress and antioxidative responses in roots of Brassica juncea L. Botanical Bulletin of Academia Sinica, 2004, 45: 203–212 (in Chinese)

[36] Song N H, Yin X L, Chen G F, Yang H. Biological responses of wheat (Triticum aestivum) plants to the herbicide chlorotoluron in soils. Chemosphere, 2007, 68(9): 1779–1787

[37] Fábregas J, Domínguez A, Álvarez D G, Lamela T, Otero A. García álvarez D, Lamela T, Otero A. Induction of astaxanthin accumulation by nitrogen and magnesium deficiencies in Haematococcus pluvialis. Biotechnology Letters, 1998, 20(6): 623–626

[38] Mascher R, Lippmann B, Holzinger S, Bergmann H. Arsenate toxicity: effects on oxidative stress response molecules and enzymes in red clover plants. Plant Science, 2002, 163(5): 961–969

[39] Lagriffoul A, Mocquot B, Mench M, Vangronsveld J. Cadmium toxicity effects on growth, mineral and chlorophyll contents, and activities of stress related enzymes in young maize plants (Zea mays L.). Plant and Soil, 1998, 200(2): 241–250

[40] Ralph P J. Herbicide toxicity of Halophila ovalis assessed by chlorophyll a fluorescence. Aquatic Botany, 2000, 66(2): 141–152

[41] Sinha S, Saxena R, Singh S. Comparative studies on accumulation of Cr from metal solution and tannery effluent under repeated metal exposure by aquatic plants: its toxic effects. Environmental Monitoring and Assessment, 2002, 80(1): 17–31

[42] Aslan M, Unlü M Y, Türkmen N, Yilmaz Y Z. Sorption of cadmium and effects on growth, protein content, and photosynthetic pigment composition of Nasturtium officinale R. Br. and Mentha aquatica L. Bulletin of Environmental Contamination and Toxicology, 2003, 71(2): 323–329

[43] Vange V, Heuch I, Vandvik V. Do seed mass and family affect germination and juvenile performance in Knautia arvensis? A study using failure-time methods. Acta Oecologica, 2004, 25(3): 169–178

[44] Dolan R W. The effect of seed size and maternal source on individual size in a population of Ludwigia leptocarpa (Onagraceae). American Journal of Botany, 1984, 71(9): 1302–1307

[45] Stanton M L. Seed variation in wild radish: effect of seed size on components of seedling and adult fitness. Ecology, 1984, 65(4): 1105–1112

[46] Winn A A. Ecological and evolutionary consequences of seed size in Prunella vulgaris. Ecology, 1988, 69(5): 1537–1544

[47] Houssard C, Escarré J. The effects of seed weight on growth and competitive ability of Rumex acetosella from two successional oldfields. Oecologia, 1991, 86(2): 236–242

[48] Simons A M, Johnston M O. Variation in seed traits of Lobelia inflata (Campanulaceae): sources and fitness consequences. American Journal of Botany, 2000, 87(1): 124–132

[49] Wulff R D. Seed size variation in Desmodium paniculatum. II. Effects on seedling growth and physiological performance. Journal of Ecology, 1986, 74(1): 99–114

[50] Vaughton G, Ramsey M. Relationships between seed mass, seed nutrients, and seedling growth in Banksia cunninghamii (Proteaceae). International Journal of Plant Sciences, 2001, 162(3): 599–606

[51] George N C, Sands J E. The control of seed germination by moisture as a soil physical property. Australian Journal of Agricultural Research, 1959, 10(5): 628–636

[52] Come D. Obstacles to germination. Monographies de Physiologie Vegetale, 1970, 6: 162

[53] Takemoto B K, Noble R D. Differential sensitivity of duckweeds (Lemnaceae) to sulphite. I. Carbon assimilation and frond replication rate as factors influencing sulphite phytotoxicity under low and high irradiance. New Phytologist, 1986, 103(3): 525–539

[54] Ait B, Audran J C. Response of champenoise grapevine to low temperatures: Changes of shoot and bud proline concentrations in response to low temperatures and correlations with freezing tolerance. Journal of Horticultural Science, 1987, 72(4): 577–582

[55] Blokhina O, Virolainen E, Fagerstedt K V. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Annals of Botany, 2003, 91(2 Spec No): 179–194

[56] Shaharuddin N A, Kawamura F, Sulaiman O, Hashim R. Evaluation on antioxidant activity, antifungal activity and total phenolic of selected commercial Malaysian timbers. In: Proceedings of International Conference on Environmental Research and Technology. Penang Malaysia: Press of the National University of Malaysia, 2008, 970–974

[57] Posmyk M M, Kontek R, Janas K M. Antioxidant enzymes activity and phenolic compounds content in red cabbage seedlings exposed to copper stress. Ecotoxicology and Environmental Safety, 2009, 72(2): 596–602

[58] Sgherri C, Cosi E, Navari-Izzo F. Phenols and antioxidative status of Raphanus sativus grown in copper excess. Plant Physiology, 2003, 118(1): 21–28

[59] Terry N. Limiting factors in photosynthesis. 1. Use of iron stress to control photochemical capacity in vivo. Plant Physiology, 1980, 65(1): 114–120

[60] Manthey J A, Crowley D E. Leaf and root responses to iron deficiency in avocado. Journal of Plant Nutrition, 1997, 20(1): 683–693

RIGHTS & PERMISSIONS

Higher Education Press and Springer-Verlag Berlin Heidelberg