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Evaluation of Selected Pharmaceuticals on Plant Stress Markers in Wheat

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Abstract

Herein we report on the interactions between two common pharmaceuticals and wheat (Triticum aestivum L.) plants. Pharmaceuticals and personal care products (PPCPs) enter wastewater treatment plants from industrial and household sewers. These chemicals are not completely removed during wastewater processing, and in many countries, are being found in drinking water sources and in surface waters downstream of wastewater treatment plants. If treated wastewater effluent is re-used to irrigate crops, the potential adverse interactions between PPCPs and plants needs to be understood. β-estradiol and gemfibrozil appeared to affect wheat seedlings through oxidative stress, as indicated by increases in lipid peroxidation, hydrogen peroxide, carotenoid, and antioxidant enzyme activities. Additionally, plant cell damage in wheat seedlings was indicated by an increase in electrolyte leakage. Although our study was not designed to elucidate possible mechanisms, the changes in activity of plant enzymes in response to some pharmaceuticals is likely the consequence of oxidative stress and the initiation of pathways to protect the plant from further cell damage.

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References

  • An J, Zhou Q, Zhang L (2009) Ecotoxicological effects of paracetamol on seed germination and seedling development of wheat (Triticum aestivum L.). J Hazardous Mater 169:751–757

    Article  CAS  Google Scholar 

  • Ananieva EA, Alexieva VS, Popova LP (2002) Treatment with salicylic acid decreases the effects of paraquat on photosynthesis. J Plant Physiol 159(7):685–693

    Article  CAS  Google Scholar 

  • Anderson TA, Malaviya P, Osma E (2015) Using conventional HPLC to study the interaction of pharmaceuticals and personal care products (PPCPs) with plants. Pharm Anal Acta 6(9):414–417

    Google Scholar 

  • Aydin E, Talinli I (2013) Analysis, occurrence and fate of commonly used pharmaceuticals and hormones in the Buyucekmece watershed, Turkey. Chemosphere 90:2004–2012

    Article  CAS  Google Scholar 

  • Bajji M, Kinet JM, Lutts S (2002a) The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat. Plant Growth Regul 36:61–70

    Article  CAS  Google Scholar 

  • Bajji M, Kinet JM, Lutts S (2002b) Osmotic and ionic effects of NaCl on germination, early seedling growth and ion content of Atriplex halimus (Chenopodiaceae). Can J Bot 80:297–304

    Article  CAS  Google Scholar 

  • Banks MK, Schultz KE (2005) Comparison of plants for germination toxicity tests in petroleum-contaminated soils. Water Air Soil Pollut 167:211–219

    Article  CAS  Google Scholar 

  • Bartrons M, Peñuelas J (2017) Pharmaceuticals and personal care products in plants. Trends Plant Sci 22:194–203

    Article  CAS  Google Scholar 

  • Bidar G, Garc G, Pruvot C, Dewaele D, Cazier F, Douay F, Shirali P (2007) Behavior of Trifolium repens and Lolium perenne growing in a heavy metal contaminated field: plant metal concentration and phytotoxicity. Environ Pollut 147:546–553

    Article  CAS  Google Scholar 

  • Carter LJ, Williams M, Böttcher C, Kookana RS (2015) Uptake of pharmaceuticals influences plant development and affects nutrient and hormone homeostasis. Environ Sci Technol 49:12509–12518

    Article  CAS  Google Scholar 

  • Carvalho PN, Bast MCP, Almeida CMR, Brix H (2014) A review of plant pharmaceutical interactions: from uptake and effects in crop plants to phytoremediation in constructed wetlands. Environ Sci Pollut Res 21:11729–11763

    Article  Google Scholar 

  • Cheeseman JM (2006) Hydrogen peroxide concentrations in leaves under natural conditions. J Exp Bot 57:2435–2444

    Article  CAS  Google Scholar 

  • Christou A, Antoniou C, Christodoulou C, Hapeshi E, Stavrou I, Michael C, Fatta-Kassinos D, Fotopoulos V (2016) Stress-related phenomena and detoxification mechanisms induced by common pharmaceuticals in alfalfa (Medicago sativa L.) plants. Sci Total Environ 557–558:652–664

    Article  Google Scholar 

  • Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11:163. https://doi.org/10.1186/1471-2229-11-163

    Article  Google Scholar 

  • De Azevedo Neto AD, Prisco JT, Enéas-Filho J, de Abreu CEB, Gomes-Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot 56:87–94

    Article  Google Scholar 

  • Demidchik V, Straltsova D, Medvedev SS, Pozhvanov GA, Sokolik A, Yurin V (2014) Stress-induced electrolyte leakage: the role of K+ -permeable channels and involvement in programmed cell death and metabolic adjustment. J Exp Bot 65(5):1259–1270

    Article  CAS  Google Scholar 

  • Dhindsa RA, Pand PD, Thorpe TA (1981) Leaf senescence correlated with increased permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 126:93–101

    Article  Google Scholar 

  • Di Salvatore M, Carafa AM, Carratù G (2008) Assessment of heavy metals phytotoxicity using seed germination and root elongation tests: a comparison of two growth substrates. Chemosphere 73(9):1461–1464

    Article  Google Scholar 

  • Erdal S (2012) Androsterone-induced molecular and physiological changes in maize seedlings in response to chilling stress. J Plant Physiol 57:1–7

    CAS  Google Scholar 

  • Erdal S, Dumlupinar R (2010) Progesterone and β-estradiol stimulate seed germination in chickpea by causing important changes in biochemical parameters. ZeitschriftfürNaturforschung C 65(3–4):239–244

    CAS  Google Scholar 

  • Fang Y, Karnjanapiboonwong A, Chase DA, Wang J, Morse AN, Anderson TA (2012) Occurrence, fate and persistence of gemfibrozil in water and soil. Environ Toxicol Chem 31:550–555

    Article  CAS  Google Scholar 

  • FAOSTAT (2017). Food and Agriculture Organisation of the United Nations; Rome, Italy

  • Finlay-Moore O, Hartel PG, Cabrera ML (2000) 17β-estradiol and testosterone in soil and runoff from grassland amended with broiler litter. J Environ Qual 29(5):1604–1611

    Article  CAS  Google Scholar 

  • Gong P, Wilke BM, Strozzi E, Fleischmann S (2001) Evaluation and refinement of a continuous seed germination and early seedling growth test for the use in the ecotoxicological assessment of soils. Chemosphere 44:491–500

    Article  CAS  Google Scholar 

  • Griffith M, Ala P, Yang DSC, Hon WC, Moffatt BA (1992) Antifreeze protein produced endogenously in winter rye leaves. Plant Physiol 100:593–596

    Article  CAS  Google Scholar 

  • He Y, Liu Y, Cao W, Huai M, Xu B, Huang B (2005) Effects of salicylic acid on heat tolerance associated with antioxidant metabolism in Kentucky bluegrass. Crop Sci 45:988–995

    Article  CAS  Google Scholar 

  • Kachout SS, Mansoura AB, Leclerc JC, Mechergui R, Rejeb MN, Ouerghi Z (2009) Effects of heavy metals on antioxidant activities of Atriplex hortensis and A. rosea. J Food Agric Environ 7(3–4):938–945

    Google Scholar 

  • Karnjanapiboonwong A, Suski JG, Shah AA, Cai Q, Morse AN, Anderson TA (2011) Occurrence of PPCPs at a wastewater treatment plant and in soil and groundwater at a land application site. Water Air Soil Pollut 216:257–273

    Article  CAS  Google Scholar 

  • Kinney CA, Furlong ET, Werner SL, Cahill JD (2006) Presence and distribution of wastewater derived pharmaceuticals in soil irrigated with reclaimed water. Enriron Toxicol Chem 25(2):317–326

    Article  CAS  Google Scholar 

  • Komesli OT, Muz M, Ak MS, Bakirdere S, Gokcay CF (2015) Occurrence, fate and removal of endocrine disrupting compounds (EDCs) in Turkish wastewater treatment plants. Chem Eng J 277:202–208

    Article  CAS  Google Scholar 

  • Larson RA (1988) The antioxidants of higher plants. Phytochemistry 27(4):969–978

    Article  CAS  Google Scholar 

  • Li MH (2003) Peroxidase and superoxide dismutase activities in fig leaves in response to ambient air pollution in a subtropical city. Arch Environ Contam Toxicol 45:168–176

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV–VIS spectroscopy. In: Wrolstad RE (ed) Current protocols in food analytical chemistry. John Wiley and Sons, NewYork, pp F4.3.1–F4.3.8

    Google Scholar 

  • Mutlu S, Atici O (2009) Allelopathic effect of Nepeta meyeri Benth. extracts on seed germination and seedling growth of some crop plants. Acta Physiol Plant 31(1):89–93

    Article  Google Scholar 

  • Mutlu S, Atici O, Kaya Y (2009) Effect of cement dust on diversity and antioxidant enzyme activities of plants growing around a cement factory. Freseninus Environ Bull 18(10):1827–1923

    Google Scholar 

  • Mutlu S, Atici O, Esim N, Mete E (2011) Essential oils of catmint (Nepeta meyeri Benth.) induce oxidative stress in early seedlings of various weed species. Acta Physiologiae Plantarum 33(3):943–951

    Article  CAS  Google Scholar 

  • Orcutt DM, Nilsen ET (2000) The physiology of plants under stress: soil and abiotic factor. John Wiley and Sons, New York, p 683

    Google Scholar 

  • Osma E, İlhan V, Yalçın İE (2014) Heavy metals accumulation causes toxicological effects in aquatic Typha domingensis Pers. Braz J Bot 37(4):461–467

    Article  Google Scholar 

  • Osma E, Elveren M, Karakoyun G (2016) Heavy metal accumulation affects growth of Scots pine by causing oxidative damage. Air Qual Atmos Health 10(1):85–92

    Article  Google Scholar 

  • Palta J, Levitt J, Stadelmann EJ (1977) Freezing injury in onion bulb cells. I. Evaluation of the conductivity method and analysis of ion and sugar efflux. Plant Physiol 60:393–397

    Article  CAS  Google Scholar 

  • Pan M, Chu LM (2016) Phytotoxicity of veterinary antibiotics to seed germination and root elongation of crops. Ecotoxicol Environ Saf 126:228–237

    Article  CAS  Google Scholar 

  • Pandey P, Irulappan V, Bagavathiannan MV, Senthil-Kumar M (2017) Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits. Front Plant Sci 8:537

    Google Scholar 

  • Posmyk MM, Bailly C, Szafranska K, Janas KM, Corbineau F (2005) Antioxidant enzymes and isoflavonoids in chilled soybean (Glycine max (L.) Merr.) seedlings. J Plant Physiol 162:403–412

    Article  CAS  Google Scholar 

  • Puccinelli P, Anselmi N, Bragaloni M (1998) Peroxidases: usable markers of air pollution in trees from urban environments. Chemosphere 36:889–894

    Article  CAS  Google Scholar 

  • Rao KVM, Raghavendra AS, Reddy KJ (2006) Physiology and molecular biology of stress tolerance in plants. Springer, Netherlands. ISBN 1-4020-4224-8

    Google Scholar 

  • Sato T, Qadir M, Yamamoto S, Endo T, Zahoor A (2013) Global, regional, and country level need for data on wastewater generation, treatment, and use. Agric Water Manag 130:1–13

    Article  Google Scholar 

  • Schmidt W, Redshaw CH (2015) Evaluation of biological endpoints in crop plants after exposure to non-steroidal anti-inflammatory drugs (NSAIDs): implications for phytotoxicological assessment of novel contaminants. Ecotoxicol Environ Saf 112:212–222

    Article  CAS  Google Scholar 

  • Schulze ED, Beck E, Müller-Hohenstein K (2005) Plant ecology. Springer, Berlin, p 702

    Google Scholar 

  • Srivastava S, Srivastava AK, Suprasanna PD, Souza SF (2009) Comparative biochemical and transcriptional profiling of two contrasting varieties of Brassica juncea L. in response to arsenic exposure reveals mechanisms of stress perception and tolerance. J Exp Bot 60(12):3419–3431

    Article  CAS  Google Scholar 

  • Sun C, Dudley S, Trumble J, Gan J (2018) Pharmaceutical and personal care products-induced stress symptoms and detoxification mechanisms in cucumber plants. Environ Pollut 234:39–47

    Article  CAS  Google Scholar 

  • Tasgin E, Atici O, Nalbantoglu B, Popova LP (2006) Effects of salicylic acid and cold treatments on protein levels and on the activities of antioxidant enzymes in the apoplast of winter wheat leaves. Phytochemistry 67:710–715

    Article  CAS  Google Scholar 

  • Tewari RK, Kumar P, Sharma PN, Bisht SS (2002) Modulation of oxidative stress responsive enzymes by excess cobalt. Plant Sci 162:381–388

    Article  CAS  Google Scholar 

  • Turk H, Erdal S, Genisel M, Atici O, Demir Y, Yanmis D (2014) The regulatory effect of melatonin on physiological, biochemical and molecular parameters in cold-stressed wheat seedlings. Plant Growth Regul 74:139–152

    Article  CAS  Google Scholar 

  • Türkoğlu E, Osma E, Elveren M (2017) Effects of acetaminophen (paracetamol) and gemfibrozil on seed development and antioxidant enzyme activities in different wheat varieties. Iran J Sci Technol Trans A Sci. https://doi.org/10.1007/s40995-017-0386-7

    Google Scholar 

  • Upadhyaya A, Sankhla D, Davis N, Sankhla N, Smith BN (1985) Effect of paclobutrazol on the activities of some enzymes of activated oxygen metabolism and lipid peroxidation in senescing soybean leaves. J Plant Physiol 121:453–461

    Article  CAS  Google Scholar 

  • Verlicchi P, Al Aukidy M, Zambello E (2012) Occurrence of pharmaceutical compounds in urban wastewater: removal, mass load and environmental risk after a secondary treatment-a review. Sci Total Environ 429:123–155

    Article  CAS  Google Scholar 

  • Wu X, Conkle JL, Ernst F, Gan J (2014) Treated wastewater irrigation: uptake of pharmaceutical and personal care products by common vegetables under field conditions. Environ Sci Technol 48:11286–11293

    Article  CAS  Google Scholar 

  • Xu Z, Zhou G, Shimizu H (2010) Plant responses to drought and rewatering. Plant Signal Behav 5:649–654

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported in part by Erzincan University BAP FEN-A-080715-0159, by a TÜBITAK 2219 International Postdoctoral Research Fellowship to Etem Osma, and a TÜBITAK 2221-Visiting Scientist Program Fellowship to Todd Anderson. This study is of the second author’s M.S. thesis.

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Authors and Affiliations

  1. Department of Biology, Erzincan University, Erzincan, Turkey

    Etem Osma & Yavuz Cigir

  2. Department of Environmental Toxicology, Texas Tech University, Lubbock, USA

    Adcharee Karnjanapiboonwong & Todd A. Anderson

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  1. Etem Osma
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  2. Yavuz Cigir
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  3. Adcharee Karnjanapiboonwong
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  4. Todd A. Anderson
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Correspondence to Etem Osma.

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Osma, E., Cigir, Y., Karnjanapiboonwong, A. et al. Evaluation of Selected Pharmaceuticals on Plant Stress Markers in Wheat. Int J Environ Res 12, 179–188 (2018). https://doi.org/10.1007/s41742-018-0081-3

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  • DOI: https://doi.org/10.1007/s41742-018-0081-3

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