Abstract
This is the first study reporting the presence of endogenous caffeine, theobromine, and theophylline in all organs of poplar plants. Liquid chromatography coupled with tandem mass spectrometry (LC-MS/MS) was used in order to evaluate the uptake, translocation, and metabolism of caffeine-(trimethyl-13C) in Populus alba L. Villafranca clone grown in hydroponic conditions. We investigated the remediation of caffeine since it is one of the most widely consumed drugs and it is frequently detected in wastewater treatment plant effluents, surface water, and groundwater worldwide. Our results demonstrated that poplar can absorb and degrade exogenous caffeine without negative effects on plant health. Data showed that concentrations of all endogenous compounds varied depending on caffeine-(trimethyl-13C) treatments. In particular, in control conditions, endogenous caffeine, theobromine, and theophylline were mainly distributed in roots. On the other hand, once caffeine-(trimethyl-13C) was provided, this compound and its dimethy-13C metabolites are mainly localized at leaf level. In conclusion, our results support the possible use of Villafranca clone in association with other water treatment systems in order to complete the process of caffeine remediation.
Similar content being viewed by others
References
Abhilash PC, Jamil S, Singh N (2009) Transgenic plants for enhanced biodegradation and phytoremediation of organic xenobiotics. Biotechnol Adv 27:474–488
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
Ashihara H, Crozier A (2001) Caffeine: a well known but little mentioned compound in plant science. Trends Plant Sci 6:407–413
Ashihara H, Sano H, Crozier A (2008) Caffeine and related purine alkaloids: biosynthesis, catabolism, function and genetic engineering. Phytochemistry 69:841–856
Ashihara H, Kato M, Chuang-xing Y (1998) Biosynthesis and metabolism of purine alkaloids in leaves of cocoa tea (Camellia ptilophyla). J Plant Res 111:599–604
Behera SK, Kim HW, Oh J-E, Park H-S (2011) Occurrence and removal of antibiotics, hormones and several other pharmaceuticals in wastewater treatment plants of the largest industrial city of Korea. Sci Total Environ 409:4351–4360
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
Buerge II, Poiger T, Müller MD, Buser HR (2003) Caffeine, an anthropogenic marker for wastewater contamination of surface waters. Environ Sci Technol 37:691–700
Burken JG, Schnoor JL (1998) Predictive relationships for uptake of organic contaminants by hybrid poplar trees. Environ Sci Technol 32:3379–3385
Coleman JOD, Blake-Kalff MMA, Davies TGE (1997) Detoxification of xenobiotics by plants: chemical modification and vacuolar compartmentation. Trends Plant Sci 4:144–151
Dettenmaier EM, Doucette WJ, Bugbee B (2009) Chemical hydrophobicity and uptake by plant roots. Environ Sci Technol 43:324–329
Fatta-Kassinos D, Kalavrouzitis IK, Koukoulakis PH, Vasquez MI (2011) The risk associated with wastewater reuse and xenobiotics in the agroecological environment. Sci Total Environ 409:3555–3563
Giachetti G, Sebastiani L (2006) Metal accumulation in poplar plant grown with industrial wastes. Chemosphere 64:446–454
González Alonso S, Valcárel Y, Montero JC, Catalá M (2012) Nicotine occurrence in bottled mineral water: analysis of 10 brands of water in Spain. Sci Total Environ 416:527–531
Herklotz PA, Gurung P, VandenHeuvel B, Kinney CA (2010) Uptake of human pharmaceuticals by plants grown under hydroponic conditions. Chemosphere 78:1416–1421
Huber C, Bartha B, Schröder P (2012) Metabolism of diclofenac in plants—hydroxylation is followed by glucose conjugation. J Hazard Mater 243:250–256
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
Iori V, Zacchini M, Pietrini F (2013) Growth, physiological response and phytoremoval capability of two willow clones exposed to ibuprofen under hydroponic culture. J Hazard Mater 262:796–804
Kretschmar JA, Baumann TW (1999) Caffeine in Citrus flowers. Phytochemistry 52:19–23
Lawrence JR, Zhu B, Swerhone GDW, Roy J, Tumber V, Waiser MJ, Topp E, Korber DR (2012) Molecular and microscopic assessment of the effects of caffeine, acetaminophen, diclofenac, and their mixtures on river biofilm communities. Environ Toxicol Chem 31:508–517
Li WC (2014) Occurrence, sources, and fate of pharmaceuticals in aquatic environment and soil. Environ Pollut 187:193–201
Liu L, Liu Y-H, Liu C-X, Wang Z, Dong J, Zhu G-F, Huang X (2013) Potential effect and accumulation of veterinary antibiotics in Phragmites australis under hydroponic conditions. Ecol Eng 53:138–143
Lloyd G, McCown B (1981) Commercially feasible micropropagation of mountain laurel, Kolmia latifolia, by use of shoot tip culture. Int Plant Propagators Soc 30:421–427
Loos R, Locoro G, Comero S, Contini S, Schwesig D, Werres F, Balsaa P, Gans O, Weiss S, Blaha L et al (2010) Pan-European survey on the occurrence of selected polar organic persistent pollutants in ground water. Water Res 44:4115–4126
Loos R, Carvalho R, António DC, Comero S, Locoro G, Tavazzi S, Paracchini B, Ghiani M, Lettieri T, Blaha L et al (2013) EU-wide monitoring survey on emerging polar organic contaminants in wastewater treatment plant effluents. Water Res 47:6475–6487
Luo Y, Guo W, Ngo HH, Nghiem LD, Hai FI, 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 473–474:619–641
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 31:1319–1334
Matamoros V, Nguyen LX, Arias CA, Salvadó V, Brix H (2012) Evaluation of aquatic plants for removing polar microcontaminants: a microcosm experiment. Chemosphere 88:1257–1264
Mazzafera P (2004) Catabolism of caffeine in plants and microorganisms. Front Biosci 9:1348–1359
Mench M, Schwitzuéguebel JP, Schroeder P, Bert V, Gawronski S, Gupta S (2009) Assessment of successful experiments and limitations of phytotechnologies: contaminant uptake, detoxification and sequestration, and consequences for food safety. Environ Sci Pollut Res 16:879–900
Nathanson JA (1984) Caffeine and related methylxantines: possible naturally occurring pesticides. Science 226:184–187
Rivera-Utrilla J, Sánchez-Polo M, Ferro-García MÁ, Prados-Joya G, Ocampo-Pérez R (2013) Pharmaceuticals as emerging contaminants and their removal from water. A review. Chemosphere 93:1268–1287
Romeo S, Francini A, Ariani A, Sebastiani L (2014) Phytoremediation of Zn: identify of diverging resistance, uptake and biomass production behaviours of poplar clones under high zinc stress. Water, Air, Soil Pollut 225:1813–1824
Santos JL, Aparicio I, Alonso E (2007) Occurrence and risk assessment of pharmaceutically active compounds in wastewater treatment plants. A case study: Seville City (Spain). Environ Int 33:596–601
Schnoor JL, Licht LA, McCutcheon SC, Wolfe NL, Carreira LH (1995) Phytoremediation of organic and nutrient contaminants. Environ Sci Technol 29:318–323
Schröder P, Navarro-Aviñó J, Azaizeh H, Goldhirsh AG, Di Gregorio S, Komives T, Langergraber G, Lenz A, Maestri E, Memon AR et al (2007) Using phytoremediation technologies to upgrade waste water treatment in Europe. Environ Sci Pollut Res 7:490–497
Sebastiani L, Scebba F, Tognetti R (2004) Heavy metal accumulation and growth responses in poplar clones Eridano (Populus deltoides × maximowiczii) and I-214 (P. × euramericana) exposed to industrial waste. Environ Exp Bot 52:79–88
Sui Q, Huang J, Deng S, Yu G, Fan Q (2010) Occurrence and removal of pharmaceuticals, caffeine and DEET in wastewater treatment plants of Beijing, China. Water Res 44:417–426
Vitória AP, Mazzafera P (1997) Cytokinin-like effects of caffeine in bioassays. Biol Plant 40:329–335
Wu X, Ernst F, Conkle JL, Gan J (2013) Comparative uptake and translocation of pharmaceutical and personal care products (PPCPs) by common vegetables. Environ Int 60:15–22
Zacchini M, Pietrini F, Scarascia Mugnozza G, Iori V, Pietrosanti L, Massacci A (2009) Metal tolerance, accumulation and translocation in poplar and willow clones treated with cadmium in hydroponics. Water, Air, Soil Pollut 197:23–34
Zhang DQ, Gersberg RM, Hua T, Zhu JF, Tuan NA, Tan SK (2012a) Pharmaceutical removal in tropical subsurface flow constructed wetlands at varying hydraulic loading rates. Chemosphere 87:273–277
Zhang DQ, Hua T, Gersberg RM, Zhu J, Ng WJ, Tan SK (2012b) Fate of diclofenac in wetland mesocosms planted with Scirpus validus. Ecol Eng 49:59–64
Zhang DQ, Hua T, Gersberg RM, Zhu J, Ng WJ, Tan SK (2013a) Fate of caffeine in mesocosms wetland planted with Scirpus validus. Chemosphere 90:1568–1572
Zhang DQ, Gersberg RM, Hua T, Zhu J, Ng WJ, Tan SK (2013b) Assessment of plant-driven uptake and translocation of clofibric acid by Scirpus validus. Environ Sci Pollut Res 20:4612–4620
Zhang DQ, Gersberg RM, Ng WJ, Tan SK (2014) Removal of pharmaceuticals and personal care products in aquatic plant-based systems: a review. Environ Pollut 184:620–639
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Philippe Garrigues
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 3010 kb)
Rights and permissions
About this article
Cite this article
Pierattini, E.C., Francini, A., Raffaelli, A. et al. Degradation of exogenous caffeine by Populus alba and its effects on endogenous caffeine metabolism. Environ Sci Pollut Res 23, 7298–7307 (2016). https://doi.org/10.1007/s11356-015-5935-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-015-5935-z