Abstract
Phthalates or phthalate acid esters (PAEs) belong to a class of chemicals renowned for frequent use in an array of plastic products. Phthalates are basically endocrine disruptors and act as mutagens. These are typical emerging pollutants and are largely debated because of their toxicological implications on living organisms. Phthalates stress is one of the prevailing stress to living organisms nowadays, which is not only limited to animals but also on plants. They interfere with the physiological and morphological characteristics of plants and bring about various metabolic alterations. Therefore, it is essential to explore the exact mechanisms adopted by plants to overcome phthalates induced stress. This review article is a dedicated attempt to unravel the probable mechanisms behind phthalate uptake, accumulation, sequestration, and degradation in plant cells and critically reviewed the plethora of toxicological effects caused by phthalates to plants including agricultural crops. The article will help understand the tolerance strategies adopted by various plants to cope up with stress, which will further help in the identification of plant species for phytoremediation.
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References
Adewuyi GO (2012) High performance liquid chromatographic identification and estimation of phthalates in sewer waste and a receiving river in Ibadan city, southwestern Nigeria. J Water Resour Prot 4(10):851
Bai PY, Wittert G, Taylor AW, Martin SA, Milne RW, Jenkins AJ, Januszewski AS, Shi Z (2017) The association between total phthalate concentration and non-communicable diseases and chronic inflammation in South Australian urban dwelling men. Environ Res 158:366–372
Barber JL, Sweetman AJ, Van Wijk D, Jones KC (2005) Hexachlorobenzene in the global environment: emissions, levels, distribution, trends and processes. Sci Total Environ 349:1–44
Cai QY, Mo CH, Zeng QY, Wu QT, Férard JF, Antizar-Ladislao B (2008) Potential of Ipomoea aquatica cultivars in phytoremediation of soils contaminated with di-n-butyl phthalate. Environ Exper Bot 62:205–211
Chen L, Zhao Y, Li L, Chen B, Zhang Y (2012) Exposure assessment of phthalates in non-occupational populations in China. Sci Total Environ 427:60–69
Cheng LJ, Cheng TS (2012) Oxidative effects and metabolic changes following exposure of greater duckweed (Spirodela polyrhiza) to diethyl phthalate. Aquat Toxicol 109:166–175
Chi J (2009) Phthalate acid esters in Potamogeton crispus L. from Haihe river, China. Chemosphere 77:48–52
Coleman J, Blake-Kalff M, Davies E (1997) Detoxification of xenobiotics by plants: chemical modification and vacuolar compartmentation. Trends Plant Sci 2:144–151
Collins C, Fryer M, Grosso A (2006) Plant uptake of non-ionic organic chemicals. Environ Sci Technol 40:45–52
Cunha C, Paulo J, Faria M, Kaufmann M, Cordeiro N (2019) Ecotoxicological and biochemical effects of environmental concentrations of the plastic-bond pollutant dibutyl phthalate on Scenedesmus sp. Aquat Toxicol 215:105281
Dalla Valle M, Dachs J, Sweetman AJ, Jones KC (2004) Maximum reservoir capacity of vegetation for persistent organic pollutants: Implications for global cycling. Global Biogeochem Cycles 18:1–15
David RM, Moore MR, Finney DC, Guest D (2000) Chronic toxicity of di (2-ethylhexyl) phthalate in rats. Toxicol Sci 55:433–443
Dhir B, Sharmila P, Saradhi PP (2009) Potential of aquatic macrophytes for removing contaminants from the environment. Crit Rev Environ Sci Technol 39:754–781
ECHA (European Chemicals Agency) (2013) Evaluation of new scientific evidence concerning DINP and DIDP in relation to entry 52 of annex XVII to Reach Regulation (EC) No 1907/2006 (Final Review Report). https://echa.europa.eu/documents/10162/31b4067e-de40-4044-93e8-9c9ff1960715 Accessed 2018.
ECPI (2014) European Council for Plasticizers and Intermediates. The plasticizers information centre. www.plasticisers.org Accessed 2019.
Ellington JJ (1999) Octanol/water partition coefficients and water solubilities of phthalate esters. J Chem Eng Data 44:1414–1418
Federal Environmental Agency (2007). https://www.umweltbundesamt.de/uba-infopresse-e/hintergrund/phthalate.pdf
Fitzgerald MA, Allaway WG (1991) Apoplastic and symplastic pathways in the leaf of the grey mangrove Avicennia marina (Forsk.) Vierh. New Phytol 119:217–226
Gavala HN, Alatriste-Mondragon F, Iranpour R, Ahring BK (2003) Biodegradation of phthalate esters during the mesophilic anaerobic digestion of sludge. Chemosphere 52(4):673–682
Gao, M., Liu, Y., Dong, Y., & Song, Z. (2018). Photosynthetic and antioxidant response of wheat to di (2-ethylhexyl) phthalate (DEHP) contamination in the soil. Chemosphere, 209, 258–267
Ge J, Cheng J, Li Y, Li QX, Yu X. (2020). Effects of dibutyl phthalate contamination on physiology, phytohormone homeostasis, rhizospheric and endophytic bacterial communities of Brassica rapa var. chinensis. Environ Res 109953
Gengmao Z, Yu H, Xing S, Shihui L, Quanmei S, Changhai W (2015) Salinity stress increases secondary metabolites and enzyme activity in safflower. Ind Crops Prod 64:175–181
Geoffroy L, Dewez D, Vernet G, Popovic R (2003) Oxyfluorfen toxic effect on S. obliquus evaluated by different photosynthetic and enzymatic biomarkers. Arch Environ Contam Toxicol 45:445–452
Ghorpade N, Mehta V, Khare M, Sinkar P, Krishnan S, Rao CV (2002) Toxicity study of diethyl phthalate on freshwater fish Cirrhina mrigala. Ecotoxicol Environ Safe 53(2):255–258
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physio Biochem 48:909–930
Groom CA, Halasz A, Paquet L, Morris N, Olivier L, Dubois C, Hawari J (2002) Accumulation of HMX (octahydro-1, 3, 5, 7-tetranitro-1, 3, 5, 7-tetrazocine) in indigenous and agricultural plants grown in HMX-contaminated anti-tank firing-range soil. Environ Sci Technol 36:112–118
Gu S, Zheng H, Xu Q, Sun C, Shi M, Wang Z, Li F (2017) Comparative toxicity of the plasticizer dibutyl phthalate to two freshwater algae. Aquatic Toxicol 191:122–130
Haslam R, Raveton M, Cole DJ, Pallett KE, Coleman JO (2001) The identification and properties of apoplastic carboxylesterases from wheat that catalyse deesterification of herbicides. Pest Biochem Physiol 71:178–189
Hays SM, Aylward LL, Kirman CR, Krishnan K, Nong A (2011) Biomonitoring equivalents for di-isononylphthalate (DINP). Regul Toxicol Pharmacol 201160:181–188
Herklotz PA, Gurung P, Heuvel BV, Kinney CA (2010) Uptake of human pharmaceuticals by plants grown under hydroponic conditions. Chemosphere 78:1416–1421
Herring R, Bering CL (1988) Effects of phthalate esters on plant seedlings and reversal by a soil microorganism. Bull Environ Contam Toxicol 40:626–632
Heudorf U, Mersch-Sundermann V, Angerer J (2007) Phthalates: toxicology and exposure. Int J Hygiene Env Health 210:623–634
Holling CS, Bailey JL, Heuvel BV, Kinney CA (2012) Uptake of human pharmaceuticals and personal care products by cabbage (Brassica campestris) from fortified and biosolids-amended soils. J Environ Monitor 14:3029–3036
Huang Q, Wang Q, Tan W, Song G, Lu G, Li F (2006) Biochemical responses of two typical duckweeds exposed to dibutyl phthalate. J Environ Sci Health Part A 41:1615–1626
Kong S, Ji Y, Liu L, Chen L, Zhao X, Wang J, Sun Z (2012) Diversities of phthalate esters in suburban agricultural soils and wasteland soil appeared with urbanization in China. Environ Poll 170:161–168
Kransler KM, Bachman AN, McKee RH (2013) Estimates of daily di-isodecyl phthalate (DIDP) intake calculated from urinary biomonitoring data. Regul Toxicol Pharmacol 65(1):29–33
Kumar P (2018) Role of plastics on human health. Indian J Pediatr 85:384–389
Kumari A, Kaur R, Sharma R, Kaur R (2019) Assessment of toxicological effects of di-n-butyl phthalate to a cereal crop (Hordeum vulgare L.). J Adv Agric Technol 6:20–26
Kvesitadze E, Sadunishvili T, Kvesitadze G (2009) Mechanisms of organic contaminants uptake and degradation in plants. World Acad Sci Eng Technol 55(6):458–468
Kvesitadze G, Khatisashvili G, Sadunishvili T, Ramsden JJ (2006) Biochemical mechanisms of detoxification in higher plants: basis of phytoremediation. Springer, New York
Latini G, De Felice C, Presta G, Del Vecchio A, Paris I, Ruggieri F, Mazzeo P (2003) In utero exposure to di-(2-ethylhexyl) phthalate and duration of human pregnancy. Environ Health Perspect 111:1783–1785
Li JH, Guo HY, Mu JL, Wang XR, Yin DQ (2006) Physiological responses of submerged macrophytes to dibutyl phthalate (DBP) exposure. Aquat Ecosyst Health Manag 9:43–47
Li Y, Yan H, Liu Q, Li X, Ge J, Yu X. (2020). Accumulation and transport patterns of six phthalic acid esters (PAEs) in two leafy vegetables under hydroponic conditions. Chemosphere 126457
Liang DW, Zhang T, Fang HH, He J (2008) Phthalates biodegradation in the environment. Appl Microbiol Biot 80:183
Liao CS, Yen JH, Wang YS (2006) Effects of endocrine disruptor di-n-butyl phthalate on the growth of Bok choy (Brassica rapa subsp. chinensis). Chemosphere 65:1715–1722
Liao CS, Yen JH, Wang YS (2009) Growth inhibition in Chinese cabbage (Brassica rapa var. chinensis) growth exposed to di-n-butyl phthalate. J Hazard Mater 163:625–631
Lin Q, Chen S, Chao Y, Huang X, Wang S, Qiu R (2017) Carboxylesterase-involved metabolism of di-n-butyl phthalate in pumpkin (Cucurbita moschata) seedlings. Environ Pollut 220:421–430
Lyche JL. (2017). Phthalates. In Repro Dev Toxicol (pp. 829-856). Academic Press
Ma T, Christie P, Teng Y, Luo Y (2013) 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
Ma T, Teng Y, Christie P, Luo Y (2015) Phytotoxicity in seven higher plant species exposed to di-n-butyl phthalate or bis (2-ethylhexyl) phthalate. Frontiers Environ Sci Eng 9:259–268
Ma TT, Wu LH, Chen L, Zhang HB, Teng Y, Luo YM (2015) Phthalate esters contamination in soils and vegetables of plastic film greenhouses of suburb Nanjing, China and the potential human health risk. Environ Sci Pollut Res 22(16):12018–12028
Macek T, Mackova M, Káš J (2000) Exploitation of plants for the removal of organics in environmental remediation. Biotech Adv 18:23–34
Main KM, Mortensen GK, Keleva MM, Boisen KA, Damgaard IN, Chellakooty M, Anderson AM (2006) Human breast milk contamination with phthalates and alterations of endogenous reproductive hormones in infants three months of age. Environ Health Perspect 114:270–276
Mankidy R, Wiseman S, Ma H, Giesy JP (2013) Biological impact of phthalates. Toxicol Lett 217:50–58
Maurya VK, Kumar D, Pathak C, Tiwari BS (2018) Involvement of Reactive Species of Oxygen and Nitrogen in Triggering Programmed Cell Death in Plants. Biotic and Abiotic Stress Tolerance in Plants. Springer, Singapore, pp 257–278
McCarroll N (2006) Reassessment of the one exemption from the requirement of a tolerance for diethyl phthalate. USEPA, Washington
Morant M, Bak S, Werck-Reichhart Møller BL, D, (2003) Plant cytochromes P450: tools for pharmacology, plant protection and phytoremediation. Curr Opin Biotech 14:151–162
Niu L, Xu Y, Xu C, Yun L, Liu W (2014) Status of phthalate esters contamination in agricultural soils across China and associated health risks. Environ Pollut 195:16–23
Nzengung VA, Jeffers P (2001) Sequestration, phytoreduction, and phytooxidation of halogenated organic chemicals by aquatic and terrestrial plants. Int J Phytorem 3:13–40
Pałaszewska-Tkacz A, Czerczak S (2012) Ftalan dibutylu - frakcja wdychana. Dokumentacja dopuszczalnychwielkości narażenia zawodowego (Di-n-butyl phthalate - inhaled fraction. Occupational exposure limits for phthalates). Podstawy i Metody Oceny Środ Pracy. 73(3):37–70
Peijnenburg WJ, Struijs J (2006) Occurrence of phthalate esters in the environment of the Netherlands. Ecotoxicol Environ Saf 63(2):204–215
Pilon-Smits E (2005) Phytoremediation. Ann Rev Plant Bio 56:15–39
Pilon-Smits E, Pilon M (2002) Phytoremediation of metals using transgenic plants. Criti Rev Plant Sci 21(5):439–456
Przybylińska PA, Wyszkowski M (2016) Environmental contamination with phthalates and its impact on living organisms. Eco Chem Eng S 23(2):347–356
Rudel RA, Camann DE, Spengler JD, Korn LR, Brody JG (2003) Phthalates, alkylphenols, pesticides, polybrominated diphenyl ethers, and other endocrine-disrupting compounds in indoor air and dust. Environ Sci Technol 37:4543–4553
Saarma K, Tarkka MT, Itavaara M, Fagerstedt KV (2003) Heat shock protein synthesis is induced by diethyl phthalate but not by di (2-ethylhexyl) phthalate in radish (Raphanus sativus). J Plant Physiol 160:1001–1010
Sandermann JH (1994) Higher plant metabolism of xenobiotics: the green liver concept. Pharmacogenetics 4:225–241
Sathyanarayana S, Karr CJ, Lozano P, Brown E, Calafat AM, Liu F, Swan SH (2008) Baby care products: possible sources of infant phthalate exposure. Pediatrics 121(2):e260–e268
Sha Y, Xia X, Yang Z, Huang GH (2007) Distribution of PAEs in the middle and lower reaches of the Yellow River, China. Environ Monit Assess 124:277–287
Sharma R, Kaur R (2017) Fluoride mediated biochemical responses and removal potential in hydroponically grown duckweed (Spirodela polyrhiza L. Schledein). J Pharma Sci Res 9(11):2072–2078
Sharma R, Kaur R (2018) Insights into fluoride-induced oxidative stress and antioxidant defences in plants. Acta Physio Plantar 40(10):181
Sharma R, Kaur R (2019a) Diallyl phthalate triggered oxidative stress in Spirodela polyrhiza L. Schleiden: physiological effects and role of antioxidant defence system. Int J Environ Sci Tech 17(4):2245–2258
Sharma R, Kaur R (2019b) Fluoride toxicity triggered oxidative stress and the activation of antioxidative defence responses in Spirodela polyrhiza L. Schleiden. J Plant Interact 14(1):440–452
Sharma R, Kumari A, Rajput S, N, R R, Arora S, Kaur R (2019c). Accumulation, morpho-physiological and oxidative stress induction by single and binary treatments of fluoride and low molecular weight phthalates in Spirodela polyrhiza L. Schleiden. Sci Rep 9:20006
Sharma R, Kaur R (2020) Elucidating physiological and biochemical alterations in giant duckweed (Spirodela polyrhiza L. Schleiden) under diethyl phthalate stress: insights into antioxidant defence system. PeerJ 8:e8267
Sharma R, Kumari A, Rajput S, Nishu, Arora S, Kaur R (2019) Accumulation, morpho-physiological and oxidative stress induction by single and binary treatments of fluoride and low molecular weight phthalates in Spirodela polyrhiza L. Schleiden. Sci Rep 9:20006
Shea KM, Committee on Environmental Health (2003) Pediatric exposure and potential toxicity of phthalate plasticizers. Pediatrics 111:1467–1474
Silva MJ, Reidy JA, Herbert AR, Preau JL, Needham LL, Calafat AM (2004) Detection of phthalate metabolites in human amniotic fluid. Bull Environ Contam Toxicol 72:1226–1231
Singh J, Thakur JK (2018) Photosynthesis and abiotic stress in plants. In: Vats S (ed) Biotic and abiotic stress tolerance in plants. Springer, Singapore, pp 27–46
Staples CA, Peterson DR, Parkerton TF, Adams WJ (1997) The environmental fate of phthalate esters: a literature review. Chemosphere 35:667–749
Sun J, Pan L, Tsang DCW, Li Z, Zhu L, Li X (2018) Phthalate esters and organochlorine pesticides in agricultural soils and vegetables from fast-growing regions: a case study from eastern China. Environ Sci Pollut Res 25:34–42
Sun J, Wu X, Gan J (2015) Uptake and metabolism of phthalate esters by edible plants. Environ Sci Technol 49:8471–8478
Szewczyńska M, Dobrzyńska E, Pośniak M (2020) Determination of phthalates in particulate matter and gaseous phase emitted in indoor air of offices. Environ Sci Pollut Res 1–9
Ting-Ting MA, Christie P, Yong-Ming LUO, Ying TENG (2014) Physiological and antioxidant responses of germinating mung bean seedlings to phthalate esters in soil. Pedosphere 24:107–115
Trasande L, Sathyanarayana S, Trachtman H (2014) Dietary phthalates and low-grade albuminuria in US children and adolescents. Clin J Am Soc Nephrol 9:100–109
United States Environmental Protection Agency (USEPA) (2013) Electronic code of federal regulations, Title 40-protection of environment, Part-423-team electric power generating point source category. Appendix A to Part 423-126, priority pollutants. https://www.ecfr.gov/cgi-bin/text
Vats S, Singh RK, Tyagi P (2013) Phthalates-a priority pollutant. Int J Advan Biol Res 3:1–8
Ventrice P, Ventrice D, Russo E, De Sarro G (2013) Phthalates: European regulation, chemistry, pharmacokinetic and related toxicity. Environ Toxicol Pharmaco 36(1):88–96
Wang J, Chen G, Christie P, Zhang M, Luo Y, Teng Y (2015) Occurrence and risk assessment of phthalate esters (PAEs) in vegetables and soils of suburban plastic film greenhouses. Sci Total Environ 523:129–137
Whyatt RM, Perzanowski MS, Just AC, Rundle AG, Donohue KM, Calafat AM, Hoepner LA, Perera FP, Miller RL (2014) Asthma in inner-city children at 5–11 years of age and prenatal exposure to phthalates: the Columbia Center for Children’s Environmental Health Cohort. Environ Health Perspect 122:1141–1146
Wu YL, Wang XH, Li YY, Hong HS (2011) Occurrence of polycyclic aromatic hydrocarbons (PAHs) in seawater from the Western Taiwan Strait, China. Marine Pollut Bull 63:459–463
Wu Z, Zhang X, Wu X, Shen G, Du Q, Mo C (2013) Uptake of di (2-ethylhexyl) phthalate (DEHP) by the plant Benincasa hispida and its use for lowering DEHP content of intercropped vegetables. J Agric Food Chem 61:5220–5225
Wyszkowski M, Wyszkowska J (2009) The effect of soil contamination with cadmium on the growth and chemical composition of spring barley (Hordeum vulgare L.) and its relationship with the enzymatic activity of soil. Fresen Environ Bull 18(7):1046–1053
Wyszkowski M, Ziółkowska A (2013) Content of polycyclic aromatic hydrocarbons in soils polluted with petrol and diesel oil after emediation with plants and various substances. Plant Soil Environ 59(7):287–294
Xie Z, Ebinghaus R, Temme C, Lohmann R, Caba A, Ruck W (2007) Occurrence and air–sea exchange of phthalates in the arctic. Environ Sci Technol 41:4555–4560
Xu G, Liu N, Wu MH, Guo RY, Zhou JX, Shi WY, Li FS (2010) Aquatic toxicity of di (2-eihylhexyl) phthalate to duckweeds. J Shanghai Univ 14:100–105
Yin R, Lin XG, Wang SG, Zhang HY (2003) Effect of DBP/DEHP in vegetable planted soil on the quality of capsicum fruit. Chemosphere 50:801–805
Yu J, Yang C, Yu RA, Fu G (2007) Toxic response of dimethyl phthalate (DMP) to Gracilaria lemaneiformis. Elec J Biol 3:80–86
Zai XM, Zhu SN, Qin P, Wang XY, Che L, Luo FX (2012a) Effect of different light qualities on seedling growth and chlorophyll fluorescence parameters of Dendrobium officinale. Biologia 72:735–744
Zai XM, Zhu SN, Qin P, Wang XY, Che L, Luo FX (2012b) Effect of Glomus mosseae on chlorophyll content, chlorophyll fluorescence parameters, and chloroplast ultrastructure of beach plum (Prunus maritima) under NaCl stress. Photosynthetica 50:323–328
Zeng F, Cui K, Xie Z, Wu L, Liu M, Sun G, Zeng Z (2008) Phthalate esters (PAEs): emerging organic contaminants in agricultural soils in peri-urban areas around Guangzhou. China. Environ Poll 156(2):425–434
Zhang Q, Song J, Li X, Peng Q, Yuan H, Li N, Ma J (2019) Concentrations and distribution of phthalate esters in the seamount area of the Tropical Western Pacific Ocean. Marine Pollut Bull 140:107–115
Zhang Y, Meng X, Chen L, Li D, Zhao L, Zhao Y, Shi H (2014) Age and sex-specific relationships between phthalate exposures and obesity in Chinese children at puberty. PloS One 9:e104852
Zhang Y, Tao Y, Sun G, Wang L (2014) Effects of di-n-butyl phthalate on the physiology and ultrastructure of cucumber seedling roots. Environ Sci Pollut Res 21:6662–6670
Zhang Y, Wang L, Du N, Ma GP, Yang AM, Zhang H, Song QX (2014) Effects of diethylphthalate and di-(2-ethyl) hexylphthalate on the physiology and ultrastructure of cucumber seedlings. Environ Sci Pollut Res 21:1020–1028
Zhang Y, Du N, Wang L, Zhang H, Zhao JY, Sun GQ, Wang PJ (2015) Physical and chemical indices of cucumber seedling leaves under dibutyl phthalate stress. Environ Sci Pollut Res 22:3477–3488
Zhang Y, Zhang H, Sun X, Wang L, Du N, Tao Y, Duan S (2016) Effect of dimethyl phthalate (DMP) on germination, antioxidant system, and chloroplast ultrastructure in Cucumis sativus L. Environ Sci Pollut Res 23:1183–1192
Zhao FJ, Ma JF, Meharg AA, McGrath SP (2009) Arsenic uptake and metabolism in plants. New Phytologist 181:777–794
Zorníková G, Jarošová A, Hřivna L (2014) Distribution of phthalic acid esters in agricultural plants and soil. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 59:233–238
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Sharma, R., Kaur, R. Physiological and metabolic alterations induced by phthalates in plants: possible mechanisms of their uptake and degradation. Environmental Sustainability 3, 391–404 (2020). https://doi.org/10.1007/s42398-020-00141-x
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DOI: https://doi.org/10.1007/s42398-020-00141-x