Abstract
Paracetamol is considered a priority pharmaceutical because its presence in the environment may have an impact on human health and in food chains. To remediate this problem, the use of Solanum nigrum L. plants for the clean-up of paracetamol-contaminated sites was investigated. The study revealed that this plant species can be used as a remarkable paracetamol phytoremediation instrument, thus delivering a cost-effective and eco-friendly cleanup technology for its environmental removal. Paracetamol was not toxic to plants, exerting a growth-promoting effect up to 0.5 mg L−1. Plant tolerance mechanisms resided essentially on root GST-mediated conjugation of paracetamol to GSH, powered by the γ-ECS increased activity that locally provided the GSH needed. Increased activities for GST and γ–ECS were detected in roots and shoots of treated plants and these enzymes were regulated in an organ- and gene-specific manner: at the transcription level in roots and post-transcriptionally in shoots, with GSTs of the classes Theta and Phi playing the most relevant role in the plant detoxification process.
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References
Alkorta I, Garbisu C (2001) Phytoremediation of organic contaminants in soils. Bioresour Technol 79:273–276
An J, Zhou Q, Sun Y, Xu Z (2009) Ecotoxicological effects of typical personal care products on seed germination and seedling development of wheat (Triticum aestivum L.). Chemosphere 76:1428–1434. https://doi.org/10.1016/j.chemosphere.2009.06.004
Bartha B, Huber C, Harpaintner R, Schroder P (2010) Effects of acetaminophen in Brassica juncea L. Czern.: investigation of uptake, translocation, detoxification, and the induced defense pathways. Environ Sci Pollut Res Int 17:1553–1562. https://doi.org/10.1007/s11356-010-0342-y
Bertolini A, Ferrari A, Ottani A, Guerzoni S, Tacchi R, Leone S (2006) Paracetamol: new vistas of an old drug. CNS Drug Rev 12:250–275. https://doi.org/10.1111/j.1527-3458.2006.00250.x
Bradford MM (1976) 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
Brandao FP, Pereira JL, Goncalves F, Nunes B (2014) The impact of paracetamol on selected biomarkers of the mollusc species Corbicula fluminea. Environ Toxicol 29:74–83. https://doi.org/10.1002/tox.20774
Chen J, Goldsbrough PB (1994) Increased activity of [gamma]-glutamylcysteine synthetase in tomato cells selected for cadmium tolerance. Plant Physiol 106:233–239
Christou A et al (2016) Stress-related phenomena and detoxification mechanisms induced by common pharmaceuticals in alfalfa (Medicago sativa L.) plants. Sci Total Environ 557–558:652–664. https://doi.org/10.1016/j.scitotenv.2016.03.054
De Groeve MR, Tran GH, Van Hoorebeke A, Stout J, Desmet T, Savvides SN, Soetaert W (2010) Development and application of a screening assay for glycoside phosphorylases. Anal Biochem 401:162–167. https://doi.org/10.1016/j.ab.2010.02.028
de Sousa A, Teixeira J, Regueiras MT, Azenha M, Silva F, Fidalgo F (2013) Metalaxyl-induced changes in the antioxidant metabolism of Solanum nigrum L. suspension cells. Pestic Biochem Physiol 107:235–243. https://doi.org/10.1016/j.pestbp.2013.07.006
de Voogt P, Janex-Habibi ML, Sacher F, Puijker L, Mons M (2009) Development of a common priority list of pharmaceuticals relevant for the water cycle. Water Sci Technol 59:39–46. https://doi.org/10.2166/wst.2009.764
Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3(3):reviews3004.1–3004.10. https://doi.org/10.1186/gb-2002-3-3-reviews3004
Fatima RA, Ahmad M (2005) Certain antioxidant enzymes of Allium cepa as biomarkers for the detection of toxic heavy metals in wastewater. Sci Total Environ 346:256–273. https://doi.org/10.1016/j.scitotenv.2004.12.004
Ferrat L, Pergent-Martini C, Romeo M (2003) Assessment of the use of biomarkers in aquatic plants for the evaluation of environmental quality: application to seagrasses. Aquat Toxicol 65:187–204. https://doi.org/10.1016/S0166-445x(03)00133-4
Ferraz P, Fidalgo F, Almeida A, Teixeira J (2012) Phytostabilization of nickel by the zinc and cadmium hyperaccumulator Solanum nigrum L. Are metallothioneins involved? Plant Physiol Bioch 57:254–260. https://doi.org/10.1016/J.Plaphy.2012.05.025
Fidalgo F, Freitas R, Ferreira R, Pessoa AM, Teixeira J (2011) Solanum nigrum L. antioxidant defence system isozymes are regulated transcriptionally and posttranslationally in Cd-induced stress. Environ Exp Bot 72:312–319. https://doi.org/10.1016/j.envexpbot.2011.04.007
Gill SS et al (2013) Glutathione and glutathione reductase: A boon in disguise for plant abiotic stress defense operations. Plant Physiol Bioch 70:204–212. https://doi.org/10.1016/j.plaphy.2013.05.032
Grung M, Kallqvist T, Sakshaug S, Skurtveit S, Thomas KV (2008) Environmental assessment of Norwegian priority pharmaceuticals based on the EMEA guideline. Ecotox Environ Safe 71:328–340. https://doi.org/10.1016/j.ecoenv.2007.10.015
Hajkova M, Kummerova M (2014) Growth response of Lemna minor L. to paracetamol. MendelNet 2014:457–462
Huber C, Bartha B, Harpaintner R, Schroder P (2009) Metabolism of acetaminophen (paracetamol) in plants-two independent pathways result in the formation of a glutathione and a glucose conjugate. Environ Sci Pollut R 16:206–213. https://doi.org/10.1007/s11356-008-0095-z
Khalvati M, Bartha B, Dupigny A, Schroder P (2010) Arbuscular mycorrhizal association is beneficial for growth and detoxification of xenobiotics of barley under drought stress. J Soil Sediment 10:54–64. https://doi.org/10.1007/s11368-009-0119-4
Kotyza J, Soudek P, Kafka Z, Vanek T (2010) Phytoremediation of pharmaceuticals—preliminary study. Int J Phytoremediation 12:306–316. https://doi.org/10.1080/15226510903563900
Kummerer K (2003) Significance of antibiotics in the environment. J Antimicrob Chemoth 52:5–7. https://doi.org/10.1093/jac/dkg293
Kummerova M, Zezulka S, Babula P, Triska J (2016) Possible ecological risk of two pharmaceuticals diclofenac and paracetamol demonstrated on a model plant Lemna minor. J Hazard Mater 302:351–361. https://doi.org/10.1016/j.jhazmat.2015.09.057
Leclercq J et al (2002) LeCTR1, a tomato CTR1-like gene, demonstrates ethylene signaling ability in Arabidopsis and novel expression patterns in tomato. Plant Physiol 130:1132–1142. https://doi.org/10.1104/pp.009415
Li YY, Song WH, Fu WJ, Tsang DCW, Yang X (2015) The roles of halides in the acetaminophen degradation by UV/H2O2 treatment: Kinetics, mechanisms, and products analysis. Chem Eng J 271:214–222. https://doi.org/10.1016/j.cej.2015.02.090
Lyubenova L, Schroder P (2011) Plants for waste water treatment - effects of heavy metals on the detoxification system of Typha latifolia. Bioresource Technol 102:996–1004. https://doi.org/10.1016/j.biortech.2010.09.072
Macek T, Mackova M, Kas J (2000) Exploitation of plants for the removal of organics in environmental remediation. Biotechnol Adv 18:23–34. https://doi.org/10.1016/S0734-9750(99)00034-8
Moreira JT, Moreira TM, Cunha JB, Azenha M, Fidalgo F, Teixeira J (2018) Differential effects of acetophenone on shoots’ and roots’ metabolism of Solanum nigrum L. plants and implications in its phytoremediation. Plant Physiol Bioch 130:391–398. https://doi.org/10.1016/j.plaphy.2018.07.027
Noctor G et al (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484. https://doi.org/10.1111/j.1365-3040.2011.02400.x
Nodler K, Voutsa D, Licha T (2014) Polar organic micropollutants in the coastal environment of different marine systems. Mar Pollut Bull 85:50–59. https://doi.org/10.1016/j.marpolbul.2014.06.024
Nunes B, Pinto G, Martins L, Goncalves F, Antunes SC (2014) Biochemical and standard toxic effects of acetaminophen on the macrophyte species Lemna minor and Lemna gibba. Environ Sci Pollut Res 21:10815–10822. https://doi.org/10.1007/s11356-014-3059-5
Nunes B, Verde MF, Soares AMVM (2015) Biochemical effects of the pharmaceutical drug paracetamol on Anguilla anguilla. Environ Sci Pollut Res 22:11574–11584. https://doi.org/10.1007/s11356-015-4329-6
Pereira RC, Camps-Arbestain M, Garrido BR, Macias F, Monterroso C (2006) Behaviour of alpha-, beta-, gamma-, and delta-hexachlorocyclohexane in the soil-plant system of a contaminated site. Environ Pollut 144:210–217. https://doi.org/10.1016/j.envpol.2005.12.030
Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39. https://doi.org/10.1146/annurev.arplant.56.032604.144214
Rezek J, Macek T, Mackova M, Triska J (2007) Plant metabolites of polychlorinated biphenyls in hairy root culture of black nightshade Solanum nigrum SNC-90. Chemosphere 69:1221–1227. https://doi.org/10.1016/j.chemosphere.2007.05.090
Rouhier N, Lemaire SD, Jacquot JP (2008) The role of glutathione in photosynthetic organisms: Emerging functions for glutaredoxins and glutathionylation. Annu Rev Plant Biol 59:143–166. https://doi.org/10.1146/annurev.arplant.59.032607.092811
Schmidt DD, Kessler A, Kessler D, Schmidt S, Lim M, Gase K, Baldwin IT (2004) Solanum nigrum: a model ecological expression system and its tools. Mol Ecol 13:981–995
Schroder P, Collins C (2002) Conjugating enzymes involved in xenobiotic metabolism of organic xenobiotics in plants. Int J Phytoremediat 4:247–265. https://doi.org/10.1080/15226510208500086
Sebben VC, Lugoch RW, Schllnker CS, Arbo MD, Vlanna RL (2010) Analytical methodology validation and stability study for serum quantification of acetaminophen. J Bras Patol Med Lab 46:143–148
Sengupta D, Ramesh G, Mudalkar S, Kumar KRR, Kirti PB, Reddy AR (2012) Molecular cloning and characterization of gamma-glutamyl cysteine synthetase (vr gamma ECS) from roots of Vigna radiata (L.) Wilczek under progressive drought stress and recovery. Plant Mol Biol Rep 30:894–903. https://doi.org/10.1007/s11105-011-0398-y
Silva AMT, Zilhão NR, Segundo RA et al (2012) Photo-Fenton plus Solanum nigrum L. weed plants integrated process for the abatement of highly concentrated metalaxyl on waste waters. Chem Eng J 184:213–220. https://doi.org/10.1016/J.Cej.2012.01.038
Srinivasan L, Mathew N, Karunan T, Muthuswamy K (2011) Biochemical studies on glutathione S-transferase from the bovine filarial worm Setaria digitata. Parasitol Res 109:213–219. https://doi.org/10.1007/s00436-010-2227-x
Teixeira J, Sousa Ad, Azenha M et al (2011) Solanum nigrum L. weed plants as a remediation tool for metalaxyl-polluted effluents and soils. Chemosphere 85:744–750. https://doi.org/10.1016/J.Chemosphere.2011.06.049
Teixeira J, Ferraz P, Gouveia C, Azevedo F, Neves S, Fidalgo F, Silva AM (2015) Targeting key metabolic points for an enhanced phytoremediation of wastewaters pre-treated by the photo-Fenton process using Solanum nigrum L. Ecotoxicol Environ Saf 120:124–129. https://doi.org/10.1016/j.ecoenv.2015.05.035
Teixeira J, Pereira S, Canovas F, Salema R (2005) Glutamine synthetase of potato (Solanum tuberosum L. cv. Desiree) plants: cell- and organ-specific expression and differential developmental regulation reveal specific roles in nitrogen assimilation and mobilization. J Exp Bot 56:663–671. https://doi.org/10.1093/jxb/eri042
Vuilleumier S (1997) Bacterial glutathione S-transferases: what are they good for? J Bacteriol 179:1431–1441. https://doi.org/10.1128/jb.179.5.1431-1441.1997
Xiang CB, Oliver DJ (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10:1539–1550. https://doi.org/10.1105/tpc.10.9.1539
Zhang T, Li B (2011) Occurrence, transformation, and fate of antibiotics in municipal wastewater treatment plants. Crit Rev Environ Sci Technol 41:951–998. https://doi.org/10.1080/10643380903392692
Acknowledgments
This work was partially supported by Fundação para a Ciência e a Tecnologia (FCT) through BioISI [PEst-OEBIA/UI 4046/2014]. The authors also thank GreenUPorto for equipment and facilities.
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Martins, L., Teixeira, J. Gene- and organ-specific impact of paracetamol on Solanun nigrum L.’s γ-glutamylcysteine synthetase and glutathione S-transferase and consequent phytoremediation fitness. Acta Physiol Plant 43, 53 (2021). https://doi.org/10.1007/s11738-021-03224-2
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DOI: https://doi.org/10.1007/s11738-021-03224-2