Phytotoxicity and oxidative effects of typical quaternary ammonium compounds on wheat (Triticum aestivum L.) seedlings

  • Yafei Li
  • Can Zhou
  • Shizhong Wang
  • Qingqi LinEmail author
  • Zhuobiao Ni
  • Hao Qiu
  • Jean Louis Morel
  • Rongliang Qiu
Research Article


The large-scale use of quaternary ammonium compounds (QACs) in medicines or disinfectants can lead to their release into the environment, posing a potential risk to organisms. This study examined the effects of three typical QACs, dodecyltrimethylammonium chloride (DTAC), dodecyldimethylbenzylammonium chloride (DBAC), and didodecyldimethylammonium chloride (DDAC), on hydroponically cultured wheat seedlings. After 14 days of exposure, both hormesis and phytotoxicity were observed in the wheat seedlings. The shoot and root fresh weight gradually increased as QAC concentrations rose from 0.05 to 0.8 mg L−1. However, higher QAC concentrations severely inhibited plant growth by decreasing shoot and root fresh weight, total root length, and photosynthetic pigment content. Moreover, the increase in malondialdehyde and O2.- contents, as well as root membrane permeability, reflected an oxidative burst and membrane lipid peroxidation caused by QACs. However, the effects of QACs on the levels of these oxidative stress markers were compound-specific, and the changes in superoxide dismutase, peroxidases, and catalase activity were partly related to reactive oxygen species levels. Considering the order of median effective concentration values (EC50) and the levels of oxidative stress induced by the three tested QACs, their phytotoxicities in wheat seedlings increased in the following order: DDAC < DTAC < DBAC, which mainly depended on their characteristics and applied concentrations. These results, which illustrated the complexity of QAC toxicity to plants, could potentially be used to assess the risk posed by these compounds in the environment.


Quaternary ammonium compounds Phytotoxicity Oxidative stress Antioxidant enzyme activity Wheat seedlings 



This study was supported by the National Key R&D Program of China (No. 2018YFD0800700), the 111 Project (No. B18060), the National Natural Science Foundation of China (No. 41671313, 41703098 and 41471020), the China Postdoctoral Science Foundation Grant (No. 2017 M622868), and the Research Fund Program of Guangdong Provincial Key Laboratory of Environmental Pollution Control and Remediation Technology (No. 2016 K0005).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

This research does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

11356_2019_5822_MOESM1_ESM.docx (701 kb)
ESM 1 (DOCX 701 kb)


  1. Alpaslan M, Gunes A (2001) Interactive effects of boron and salinity stress on the growth, membrane permeability and mineral composition of tomato and cucumber plants. Plant Soil 236(1):123–128Google Scholar
  2. 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(10):1428–1434Google Scholar
  3. Arrebola-Liébanas FJ, Abdo MAH, Moreno JLF, Martínez-Vidal JL, Frenich AG (2014) Determination of quaternary ammonium compounds in oranges and cucumbers using QuEChERS extraction and ultra-performance liquid chromatography/tandem mass spectrometry. J AOAC Int 97(4):1021–1026Google Scholar
  4. Bellino A, Lofrano G, Carotenuto M, Libralato G, Baldantoni D (2018) Antibiotic effects on seed germination and root development of tomato (Solanum lycopersicum L.). Ecotoxicol Environ Saf 148:135–141Google Scholar
  5. Biczak R (2016) Quaternary ammonium salts with tetrafluoroborate anion: phytotoxicity and oxidative stress in terrestrial plants. J Hazard Mater 304:173–185Google Scholar
  6. Cao H, Kang M, Chen Z, Li L, Cui M, Chen M, Zhang H, Wang Y (2014) Determination of five quaternary ammonium compounds in foodstuffs using high performance liquid chromatography-tandem mass spectrometry. Anal Methods 6(13):4790–4796Google Scholar
  7. Carvalho PN, Basto 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 R 21(20):11729–11763Google Scholar
  8. Chen Y, Geurts M, Sjollema SB, Kramer NI, Hermens JLM, Droge STJ (2014a) Acute toxicity of the cationic surfactant C12-benzalkonium in different bioassays: how test design affects bioavailability and effect concentrations. Environ Toxicol Chem 33(3):606–615Google Scholar
  9. Chen Y, Lin F, Yang H, Yue L, Hu F, Wang J, Luo Y, Cao F (2014b) Effect of varying NaCl doses on flavonoid production in suspension cells of Ginkgo biloba: relationship to chlorophyll fluorescence, ion homeostasis, antioxidant system and ultrastructure. Acta Physiol Plant 36(12):3173–3187Google Scholar
  10. Chen Z, Bertin R, Froldi G (2013) EC50 estimation of antioxidant activity in DPPH. assay using several statistical programs. Food Chem 138(1):414–420Google Scholar
  11. Cheng T-S (2012) The toxic effects of diethyl phthalate on the activity of glutamine synthetase in greater duckweed (Spirodela polyrhiza L.). Aquat Toxicol 124–125:171–178Google Scholar
  12. 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 557-558:652–664Google Scholar
  13. Christou A, Michael C, Fatta-Kassinos D, Fotopoulos V (2018) Can the pharmaceutically active compounds released in agroecosystems be considered as emerging plant stressors? Environ Int 114:360–364Google Scholar
  14. Clarke BO, Smith SR (2011) Review of ‘emerging’ organic contaminants in biosolids and assessment of international research priorities for the agricultural use of biosolids. Environ Int 37(1):226–247Google Scholar
  15. Comber SDW, Rule KL, Conrad AU, Höss S, Webb SF, Marshall S (2008) Bioaccumulation and toxicity of a cationic surfactant (DODMAC) in sediment dwelling freshwater invertebrates. Environ Pollut 153(1):184–191Google Scholar
  16. Czarnocka W, Karpiński S (2018) Friend or foe? Reactive oxygen species production, scavenging and signaling in plant response to environmental stresses. Free Radic Biol Med 122:4–20Google Scholar
  17. 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):1259–1270Google Scholar
  18. Gao M, Qi Y, Song W, Xu H (2016) Effects of di-n-butyl phthalate and di (2-ethylhexyl) phthalate on the growth, photosynthesis, and chlorophyll fluorescence of wheat seedlings. Chemosphere 151:76–83Google Scholar
  19. Garcı́a MT, Ribosa I, Guindulain T, Sánchez-Leal J, Vives-Rego J (2001) Fate and effect of monoalkyl quaternary ammonium surfactants in the aquatic environment. Environ Pollut 111(1):169–175Google Scholar
  20. Gengmao Z, Yu H, Xing S, Shihui L, Quanmei S, Changhai W (2015) Salinity stress increases secondary metabolites and enzyme activity in safflower. Ind Crop Prod 64:175–181Google Scholar
  21. Gerba CP (2015) Quaternary ammonium biocides: efficacy in application. Appl Environ Microbiol 81(2):464–469Google Scholar
  22. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts :I Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125(1):189–198Google Scholar
  23. Ismail ZZ, Tezel U, Pavlostathis SG (2010) Sorption of quaternary ammonium compounds to municipal sludge. Water Res 44(7):2303–2313Google Scholar
  24. Jing G, Zhou Z, Zhuo J (2012) Quantitative structure–activity relationship (QSAR) study of toxicity of quaternary ammonium compounds on Chlorella pyrenoidosa and Scenedesmus quadricauda. Chemosphere 86(1):76–82Google Scholar
  25. Juhler RK, Henriksen T, Rosenbom AE, Kjaer J (2010) Fate and transport of chlormequat in subsurface environments. Environ Sci Pollut Res Int 17(6):1245–1256Google Scholar
  26. Khan AH, Libby M, Winnick D, Palmer J, Sumarah M, Ray MB, Macfie SM (2018) Uptake and phytotoxic effect of benzalkonium chlorides in Lepidium sativum and Lactuca sativa. J Environ Manag 206:490–497Google Scholar
  27. Lara-Martín PA, Li X, Bopp RF, Brownawell BJ (2010) Occurrence of alkyltrimethylammonium compounds in urban estuarine sediments: behentrimonium as a new emerging contaminant. Environ Sci Technol 44(19):7569–7575Google Scholar
  28. Li X, Luo X, Mai B, Liu J, Chen L, Lin S (2014) Occurrence of quaternary ammonium compounds (QACs) and their application as a tracer for sewage derived pollution in urban estuarine sediments. Environ Pollut 185:127–133Google Scholar
  29. Liang Z, Ge F, Zeng H, Xu Y, Peng F, Wong M (2013) Influence of cetyltrimethyl ammonium bromide on nutrient uptake and cell responses of Chlorella vulgaris. Aquat Toxicol 138-139(2):81–87Google Scholar
  30. Liu H, Zhang S, Hu X, Chen C (2013) Phytotoxicity and oxidative stress effect of 1-octyl-3-methylimidazolium chloride ionic liquid on rice seedlings. Environ Pollut 181:242–249Google Scholar
  31. Liu H, Zhang S, Zhang X, Chen C (2015) Growth inhibition and effect on photosystem by three imidazolium chloride ionic liquids in rice seedlings. J Hazard Mater 286:440–448Google Scholar
  32. Masisi K, Diehl-Jones WL, Gordon J, Chapman D, Moghadasian MH, Beta T (2015) Carotenoids of aleurone, germ, and endosperm fractions of barley, corn and wheat differentially inhibit oxidative stress. J Agric Food Chem 63(10):2715–2724Google Scholar
  33. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410Google Scholar
  34. Olkowska E, Polkowska Ż, Namieśnik J (2013) A solid phase extraction-ion chromatography with conductivity detection procedure for determining cationic surfactants in surface water samples. Talanta 116(22):210–216Google Scholar
  35. Osma E, Cigir Y, Karnjanapiboonwong A, Anderson TA (2018) Evaluation of selected pharmaceuticals on plant stress markers in wheat. Int J Environ Res 12(2):179–188Google Scholar
  36. 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 8:537Google Scholar
  37. Pawłowska B, Biczak R (2016) Evaluation of the effect of tetraethylammonium bromide and chloride on the growth and development of terrestrial plants. Chemosphere 149:24–33Google Scholar
  38. Pawłowska B, Telesiński A, Płatkowski M, Stręk M, Śnioszek M, Biczak R (2017) Reaction of spring barley and common radish on the introduction of ionic liquids containing asymmetric cations to the soil. J Agric Food Chem 65(23):4562–4571Google Scholar
  39. Peng XT, Shi ZG, Feng YQ (2011) Rapid and high-throughput determination of cationic surfactants in environmental water samples by automated on-line polymer monolith microextraction coupled to high performance liquid chromatography-mass spectrometry. J Chromatogr A 1218(23):3588–3594Google Scholar
  40. Qiu RL, Zhao X, Tang YT, Yu FM, Hu PJ (2008) Antioxidative response to Cd in a newly discovered cadmium hyperaccumulator, Arabis paniculata F. Chemosphere 74(1):6–12Google Scholar
  41. Rademacher W (2000) Growth retardants: effects on gibberellin biosynthesis and other metabolic pathways. Annu Rev Plant Physiol Plant Mol Biol 51(1):501–531Google Scholar
  42. Roghair CJ, Buijze A, Schoon HNP (1992) Ecotoxicological risk evaluation of the cationic fabric softener DTDMAC. I. Ecotoxicological effects. Chemosphere 24(5):599–609Google Scholar
  43. Ruan T, Song S, Wang T, Liu R, Lin Y, Jiang G (2014) Identification and composition of emerging quaternary ammonium compounds in municipal sewage sludge in China. Environ Sci Technol 48(8):4289–4297Google Scholar
  44. Sütterlin H, Alexy R, Kümmerer K (2008) The toxicity of the quaternary ammonium compound benzalkonium chloride alone and in mixtures with other anionic compounds to bacteria in test systems with Vibrio fischeri and Pseudomonas putida. Ecotoxicol Environ Saf 71(2):498–505Google Scholar
  45. Sandbacka M, Christianson I, Isomaa B (2000) The acute toxicity of surfactants on fish cells, Daphnia magna and fish—a comparative study. Toxicol in Vitro 14(1):61–68Google Scholar
  46. Sun C, Dudley S, Trumble J, Gan J (2018) Pharmaceutical and personal care products-induced stress symptoms and detoxification mechanisms in cucumber plants. Environ Poll 234:39–47Google Scholar
  47. Tsai PC, Ding WH (2004) Determination of alkyltrimethylammonium surfactants in hair conditioners and fabric softeners by gas chromatography-mass spectrometry with electron-impact and chemical ionization. J Chromatogr A 1027(1–2):103–108Google Scholar
  48. Wang C, Zhang SH, Wang PF, Hou J, Li W, Zhang WJ (2008) Metabolic adaptations to ammonia-induced oxidative stress in leaves of the submerged macrophyte Vallisneria natans (Lour.) Hara. Aquat Toxicol 87(2):88–98Google Scholar
  49. Wang LS, Wang L, Wang L, Wang G, Li ZH, Wang JJ (2009) Effect of 1-butyl-3-methylimidazolium tetrafluoroborate on the wheat (Triticum aestivum L.) seedlings. Environ Toxicol 24(3):296–303Google Scholar
  50. Xiang L, Wang XK, Li YW, Huang XP, Wu XL, Zhao HM, Li H, Cai QY, Mo CH (2015) Analysis of trace quaternary ammonium compounds(QACs) in vegetables using ultrasonic-assisted extraction and gas chromatography mass spectrometry. J Agric Food Chem 63(30):6689–6697Google Scholar
  51. Xiang L, Sun TF, Mo CH, Li YW, Cai QY, Li H (2016) Related environmental problems and research progresses of quaternary ammonium compounds (QACs). Prog Chem 28(5):727–736Google Scholar
  52. Zhang C, Cui F, Zeng GM, Jiang M, Yang ZZ, Yu ZG, Zhu MY, Shen LQ (2015) Quaternary ammonium compounds (QACs): a review on occurrence, fate and toxicity in the environment. Sci Total Environ 518-519:352–362Google Scholar
  53. Zhang Y, Wang L, Du N, Ma G, Yang A, Zhang H, Wang Z, Song Q (2014) Effects of diethylphthalate and di-(2-ethyl)hexylphthalate on the physiology and ultrastructure of cucumber seedlings. Environ Sci Pollut Res Int 21(2):1020–1028Google Scholar
  54. Zheng MJ, Xiang L, Li YW, Mo CH, Cai QY, Huang XP, Wu XL, Zhao HM (2014) Simultaneous extraction and determination of three quatermary ammonium compouds in water using liquid-liquid exaction and gas chromatography-mass spectrometry. Chinese J Anal Chem 42(5):735–740Google Scholar
  55. Zhu M, Ge F, Zhu R, Wang X, Zheng X (2010) A DFT-based QSAR study of the toxicity of quaternary ammonium compounds on Chlorella vulgaris. Chemosphere 80(1):46–52Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Environmental Science and EngineeringSun Yat-Sen UniversityGuangzhouChina
  2. 2.Guangdong Provincial Key Laboratory of Environmental Pollution Control and Remediation Technology (Sun Yat-Sen University)GuangzhouChina
  3. 3.Guangdong Provincial Engineering Research Center for Heavy Metal Contaminated Soil Remediation (Sun Yat-Sen University)GuangzhouChina
  4. 4.School of Geography and PlanningSun Yat-Sen UniversityGuangzhouChina
  5. 5.School of Environmental Science and EngineeringShanghai Jiao Tong UniversityShanghaiChina
  6. 6.Laboratoire Sols et Environnement INRAUniversité de LorraineNancy CédexFrance

Personalised recommendations