Skip to main content

Populus alba dioctyl phthalate uptake from contaminated water

Abstract

Phthalates are micro-pollutants of great concern due to their negative effects on ecosystem functioning and human health. Thanks to its capability in uptake and accumulation of organic pollutants, Populus alba L. “Villafranca” clone could be a good candidate for reducing the impacts derived by the persistence of such compounds in the environment. We investigated plant response and uptake of dioctyl phthalate (DOP) by poplar, grown in hydroponics condition, for 21 days with 0, 40, and 400 μg L−1 of d4-DOP. Treated plants, after 21 days of 400 μg L−1 d4-DOP, showed an increase in root dry biomass (+ 29%) at the expense of aerial parts (− 8%) compared with control. The root development could be sustained by the increase of Mg uptake by poplar. LC-MS/MS analysis demonstrated the uptake and accumulation in roots of d4-DOP starting from day one (3.5 ± 3.29 and 7.1 ± 3.28 in 40 and 400 μg L−1 d4-DOP respectively), despite volatilization of d4-DOP was observed from nutritive solution. The chemical interaction between d4-DOP and Zn occurred in roots of plants treated with the high d4-DOP concentration, without limiting the Zn concentration in leaves. Results confirm the high tolerance of “Villafranca” clone to xenobiotic and suggest the poplar capability in d4-DOP uptake and accumulation at root level.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Abdel daiem MM, Rivera-Utrilla J, Ocampo-Pérez R, Méndez-Díaz JD, Sánchez-Polo M (2012) Environmental impact of phthalic acid esters and their removal from water and sediments by different technologies–a review. J Environ Manag 109:164–178

    CAS  Article  Google Scholar 

  • Arnon DI, Hoagland DR (1940) Crop production in artificial culture solutions and in soils with special reference to factors influencing yields and absorption of inorganic nutrients. Soil Sci 50:463–485

    CAS  Google Scholar 

  • Baca SG (2013) Zinc(II) complexes based on ortho-phthalic acid and ancillary N-donor ligands. ChemInform. https://doi.org/10.1002/chin.201341223

  • Baca SG, Filippova IG, Gherco OA, Gdaniec M, Simonov YA, Gerbeleu NV, Franz P, Basler R, Decurtins S (2004) Nickel (II)-, cobalt (II)-, copper (II)-, and zinc (II)-phthalate and 1-methylimidazole coordination compounds: synthesis, crystal structures and magnetic properties. Inorg Chim Acta 357(12):3419–3429

    CAS  Article  Google Scholar 

  • Briggs GG, Bromilow RH, Evans AA (1982) Relationships between lipophilicity and root uptake and translocation of non-ionized chemicals by barley. Pestic Sci 13:495–504

    CAS  Article  Google Scholar 

  • 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 Exp Bot 62(3):205–211

    CAS  Article  Google Scholar 

  • Chen WC, Huang HC, Wang YS, Yen JH (2011) Effect of benzyl butyl phthalate on physiology and proteome characterization of water celery (Ipomoea aquatica Forsk.). Ecotoxicol Environ Saf 74(5):1325–1330

    CAS  Article  Google Scholar 

  • Chen HL, Yao J, Wang F (2013) Soil microbial and enzyme properties as affected by long-term exposure to phthalate esters. Adv Mater Res 726:3653–3656

    Article  Google Scholar 

  • Chi J (2009) Phthalate acid esters in Potamogeton crispus L. from Haihe River China. Chemosphere 77(1):48–52

    CAS  Article  Google Scholar 

  • Clara M, Windhofer G, Hartl W, Braun K, Simon M, Gans O, Scheffknecht C, Chovanec A (2010) Occurrence of phthalates in surface runoff, untreated and treated wastewater and fate during wastewater treatment. Chemosphere 78(9):1078–1084

    CAS  Article  Google Scholar 

  • Fu X, Du Q (2011) Uptake of di-(2-ethylhexyl) phthalate of vegetables from plastic film greenhouses. J Agric Food Chem 59(21):11585–11588

    CAS  Article  Google Scholar 

  • Gani KM, Tyagi VK, Kazmi AA (2017) Occurrence of phthalates in aquatic environment and their removal during wastewater treatment processes: a review. Environ Sci Pollut Res Int 24(21):17267–17284

    CAS  Article  Google Scholar 

  • Gao D, Li Z, Wen Z, Ren N (2014) Occurrence and fate of phthalate esters in full-scale domestic wastewater treatment plants and their impact on receiving waters along the Songhua River in China. Chemosphere 95:24–32

    CAS  Article  Google Scholar 

  • Gao M, Qi Y, Song W, Xu H (2016) Effects of di-n-butyl phthalate and di (e-ethylhexyl) phthlate on the growth, photosynthesis, and chlorophyll fluorescence of wheat seedlings. Chemosphere 151:76–83

    CAS  Article  Google Scholar 

  • Giachetti G, Sebastiani L (2006) Metal accumulation in poplar plant grown with industrial wastes. Chemosphere 64(3):446–454

    CAS  Article  Google Scholar 

  • Hafsi C, Debez A, Abdelly C (2014) Potassium deficiency in plants: effects and signaling cascades. Acta Physiol Plant 36(5):1055–1070

    CAS  Article  Google Scholar 

  • He L, Gielen G, Bolan NS, Zhang X, Qin H, Huang H, Wang H (2015) Contamination and remediation of phthalic acid esters in agricultural soils in China: a review. Agron Sustain Dev 35(2):519–534

    CAS  Article  Google Scholar 

  • Hermans C, Vuylsteke M, Coppens F, Cristescu SM, Harren FJ, Inzé D, Verbruggen N (2010) Systems analysis of the responses to long-term magnesium deficiency and restoration in Arabidopsis thaliana. New Phytol 187(1):132–144

    CAS  Article  Google Scholar 

  • Iori V, Pietrini F, Zacchini M (2012) Assessment of ibuprofen tolerance and removal capability in Populus nigra L. by in vitro culture. J Hazard Mater 229-230:217–223

    CAS  Article  Google Scholar 

  • Katsikantami I, Sifakis S, Tzatzarakis MN, Vakonaki E, Kalantzi OI, Tsatsakis AM, Rizos AK (2016) A global assessment of phthalates burden and related links to health effects. Environ Int 97:212–236

    CAS  Article  Google Scholar 

  • Krell HW, Sandermann H (1984) Plant biochemistry of xenobiotics purification and properties of a wheat esterase hydrolyzing the plasticizer chemical, bis(2-ethylhexy1)phthalate. Eur J Blochem 143(1):57–62

    CAS  Article  Google Scholar 

  • Li C, Chen J, Wang J, Han P, Luan Y, Ma X, Lu A (2016) Phthalate esters in soil, plastic film, and vegetable from greenhouse vegetable production bases in Beijing, China: concentrations, sources, and risk assessment. Sci Total Environ 568:1037–1043

    CAS  Article  Google Scholar 

  • Liang DW, Zhang T, Fang HH, He J (2008) Phthalates biodegradation in the environment. Appl Microbiol Biotechnol 80(2):183–198

    CAS  Article  Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • Lloyd G, McCown B (1980) Commercially-feasible micropropagation of mountain laurel, Kolmialatifolia, by use of shoot tip culture. Combined Proceedings of International Plant Propagators’ Society 30:421–427

  • Luo Y, Guo W, HaoNgo H, DucNghiem L, IbneyHai F, Zhang J, Liang S, Wang XC (2014) A review on the occurrence of micropollutants in the aquatic environment and their fate and removal during wastewater treatment. Sci Total Environ 473:619–641

    Article  CAS  Google Scholar 

  • Ma T, Luo Y, Christie P, Teng Y, Liu W (2012) Removal of phthalic esters from contaminated soil using different cropping systems: a field study. Eur J Soil Biol 50:76–82

    CAS  Article  Google Scholar 

  • 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(8):5289–5298

    CAS  Article  Google Scholar 

  • Magdouli S, Daghrir R, Brar SK, Drogui P, Tyagi RD (2013) Di 2-ethylhexylphtalate in the aquatic and terrestrial environment: a critical review. Environ Manag 127:36–49

    CAS  Google Scholar 

  • Markert B (1992) Presence and significance of naturally occurring chemical elements of the periodic system in the plant organism and consequences for future investigations on inorganic environmental chemistry in ecosystems. Vegetatio 103(1):1–30

    Google Scholar 

  • Marmiroli M, Pietrini F, Maestri E, Zacchini M, Marmiroli N, Massacci A (2011) Growth, physiological and molecular traits in Salicaceae trees investigated for phytoremediation of heavy metals and organics. Tree Physiol 31(12):1319–1334

    CAS  Article  Google Scholar 

  • Martínez-Hernández V, Leal M, Meffe R, De Miguel Á, Alonso-Alonso C, De Bustamante I et al (2018) Removal of emerging organic contaminants in a poplar vegetation filter. J Hazard Mater 342:482–491

    Article  CAS  Google Scholar 

  • Miller EL, Nason SL, Karthikeyan KG, Pedersen JA (2016) Root uptake of pharmaceuticals and personal care product ingredients. Environ Sci Technol 50:525–541

    CAS  Article  Google Scholar 

  • Net S, Sempéré R, Delmont A, Paluselli A, Ouddane B (2015) Occurrence, fate, behavior and ecotoxicological state of phthalates in different environmental matrices. Environ Sci Technol 49(7):4019–4035

    CAS  Article  Google Scholar 

  • Niu Y, Jin G, Zhang YS (2014) Root development under control of magnesium availability. Plant Signal Behav 9(9):e29720

    Article  CAS  Google Scholar 

  • Oca ML, Rubio L, Sarabia LA, Ortiz MC (2016) Dealing with the ubiquity of phthalates in the laboratory when determining plasticizers by gas chromatography/mass spectrometry and PARAFAC. J Chromatogr A 1464:124–140

    CAS  Article  Google Scholar 

  • Pierattini EC, Francini A, Raffaelli A, Sebastiani L (2016a) Degradation of exogenous caffeine by Populus alba and its effects on endogenous caffeine metabolism. Environ Sci Pollut Res 23(8):7298–7307

    CAS  Article  Google Scholar 

  • Pierattini EC, Francini A, Raffaelli A, Sebastiani L (2016b) Morpho-physiological response of Populus alba to erythromycin: a timeline of the health status of the plant. Sci Total Environ 569–570:540–547

    Article  CAS  Google Scholar 

  • Pierattini EC, Francini A, Huber C, Sebastiani L, Schröder P (2018) Poplar and diclofenac pollution: a focus on physiology, oxidative stress and uptake in plant organs. Sci Total Environ 636:944–952

    CAS  Article  Google Scholar 

  • Pilipović A, Orlović S, Rončević S, Nikolić N, Župunski M, Spasojević J (2015) Results of selection of poplars and willows for water and sediment phytoremediation. Agricult Forest 61:205–211

  • Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MA (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12(3):98–105

    CAS  Article  Google Scholar 

  • Romè C, Romeo S, Francini A, Andreucci A, Sebastiani L (2016a) Leaves position in Populus alba Villafranca clone reveals a strategy towards cadmium uptake response. Plant Growth Regul 79(3):355–366

    Article  CAS  Google Scholar 

  • Romè C, Huang XY, Danku J, Salt DE, Sebastiani L (2016b) Expression of specific genes involved in Cd uptake, translocation, vacuolar compartmentalization and recycling in Populus alba Villafranca clone. Indian J Plant Physiol 202:83–91

    Article  CAS  Google Scholar 

  • Romeh AA (2013) Diethyl phthalate and dioctyl phthalate in Plantago major L. Afr J Agric Res 8(32):4360–4364

  • Romeo S, Francini A, Ariani A, Sebastiani L (2014) Phytoremediation of Zn: identify the diverging resistance, uptake and biomass production behaviours of poplar clones under high zinc stress. Water Air Soil Pollut 225:1813–1819

    Article  CAS  Google Scholar 

  • Romeo S, Francini A, Sebastiani L, Morabito D (2017) High Zn concentration does not impair biomass, cutting radial growth, and photosynthetic activity traits in Populus alba L. J Soils Sediments 17(5):1394–1402

    CAS  Article  Google Scholar 

  • Sandermann H (1994) Higher plant metabolism of xenobiotics: the ‘green liver’ concept. Pharmacogenetics 4(5):225–241

    CAS  Article  Google Scholar 

  • Schröder P, Navarro-Aviñó J, Azaizeh H, Goldhirsh AG, DiGregorio S, Komives T, Langergraber G, Lenz A, Maestri E, Memon AR, Ranalli A, Sebastiani L, Smrcek S, Vanek T, Vuilleumier S, Wissing F (2007) Using phytoremediation technologies to upgrade waste water treatment in Europe. Environ Sci Pollut Res Int 14(7):490–497

    Article  CAS  Google Scholar 

  • Stasinakis AS (2012) Review on the fate of emerging contaminants during sludge anaerobic digestion. Bioresour Technol 121:432–440

    CAS  Article  Google Scholar 

  • Sun J, Wu X, Gan J (2015) Uptake and metabolism of phthalate esters by edible plants. Environ Sci Technol 49:8471–8478

    CAS  Article  Google Scholar 

  • Vaz JLL, Duc G, Petit-Ramel M, Faure R, Vittori O (1996) Cd (II) complexes with phthalic acids: solution study and crystal structure of cadmium (II) phthalate hydrate. Can J Chem 74(3):359–364

    Article  Google Scholar 

  • Visscher AM, Paul AL, Kirst M, Guy CL, Schuerger AC, Ferl RJ (2010) Growth performance and root transcriptome remodeling of Arabidopsis in response to Mars-like levels of magnesium sulfate. PLoS One 5:e12348

    Article  CAS  Google Scholar 

  • 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(22):5220–5225

    CAS  Article  Google Scholar 

  • Zavoda J, Cutright T, Szpak J, Fallon E (2001) Uptake, selectivity, and inhibition of hydroponic treatment of contaminants. J Environ Eng 127(6):502–508

    CAS  Article  Google Scholar 

  • Zeng QY, Mo CH, Cai QY, Mo C, Wen R (2010) Root morphological and physiological characteristics of two genetypes of Brassica parachinensis and their effect on di (2-ethylhexil) phtalate (DEHP) uptake. Acta Sci Vet 30:1280–1285

    CAS  Google Scholar 

  • Zhang Y, Zhang H, Sun X, Wang L, Du N, Tao Y, Sun G, Erinle KO, Wang P, Zhou C, Duan S (2016) Effect of dimethyl phthalate (DMP) on germination, antioxidant system, and chloroplast ultrastructure in Cucumis sativus L. Environ Sci Pollut Res 23(2):1183–1192

    CAS  Article  Google Scholar 

  • Zhao HM, Du H, Xiang L, Li YW, Li H, Cai QY et al (2016) Physiological differences in response to di-n-butyl phthalate (DBP) exposure between low-and high-DBP accumulating cultivars of Chinese flowering cabbage (Brassica parachinensis L.). Environ Pollut 208:840–849

    CAS  Article  Google Scholar 

  • Zhou X, Cui K, Zeng F, Li S, Zeng Z (2016) A simple and selective method for determination of phthalate biomarkers in vegetable samples by high pressure liquid chromatography–electrospray ionization-tandem mass spectrometry. Food Chem 200:336–342

    CAS  Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alessandra Francini.

Additional information

Responsible editor: Elena Maestri

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Vannucchi, F., Francini, A., Pierattini, E.C. et al. Populus alba dioctyl phthalate uptake from contaminated water. Environ Sci Pollut Res 26, 25564–25572 (2019). https://doi.org/10.1007/s11356-019-05829-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-05829-0

Keywords

  • DOP
  • Micro-pollutants
  • Phthalates
  • Poplar
  • Nutrients
  • Volatility