Skip to main content
Log in

Uptake and decomposition of the herbicide propanil in the plant Bidens pilosa L. dominating in the Yangtze Three Gorges Reservoir (TGR), China

  • Recent Advances in Chemistry and the Environment
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Propanil (3′,4′-dichloropropionanilide) is a selective post emergence herbicide for controlling broad leaf and grass weeds in rice (Oryza sativa L.). After being taken up by plants, the fate of propanil in decomposing plant material is of particular importance to the phytoremediation of the environment. Therefore, we investigated the biotransformation of propanil in the plant Bidens pilosa under conditions close to those present in the Three Gorges Reservoir (TGR), China. Plants pre-treated with 14C-ring-labeled propanil were either (treatment a) directly submerged in TGR water for 90 days or (treatment b) pre-extracted with organic solvents, and subsequently only insoluble materials and non-extractable residues (NER) of the pesticide fractions were similarly incubated. After incubation in TGR water (treatment a), 30 % of applied radioactivity was released into water and simultaneously, amounts of NER in the plant debris appeared to increase with time finally amounting to 40 % of applied 14C. The radioactivity contained in the extractable fractions were identified as propanil, 3,4-dichloroaniline (DCA), and N-β-D-glucopyranosyl-3,4-dichloroaniline (DCA-Glu). In treatment b, significant 14C amounts were released to the water (6 % of applied 14C) and the solubilized radioactivity fractions were demonstrated to agree with those found in the extractable fractions. Therefore, if residues of the pesticide propanil are taken up by plants, it may enter again the aquatic environment after plant death and submergence. This phenomenon may have a potential impact on aquatic organisms, which to our knowledge has not been reported before. As plant uptake and degradation of xenobiotics are recognized as detoxification, we consider B. pilosa with its high uptake potential, at least for propanil, as suitable species for phytoremediation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

TGR:

Three Gorgers Reservoir

DOC:

Dissolved organic carbon

NER:

Non-extractable residues

AR:

Applied radioactivity

CFU:

Colony forming units

LSC:

Liquid scintillation counter

References

  • Abdel-Saterar MA, Ei-Said AHM (2001) Xylan-decomposing fungi and xylanolytic activity in agricultural and industrial wastes. Int Biodeter Biodegr 47:15–21

    Article  Google Scholar 

  • APHA (2005) Standard methods for the examination of water and wastewater, 21st edn. American Public Health Association, Washington

    Google Scholar 

  • Aumen NG, Bottomley PJ, Ward GM, Gregory SV (1983) Microbial decomposition of wood in streams: distribution of microflora and factors affecting [14 C] lignocellulose mineralization. Appl Environ Microbiol 46:1409–1416

    CAS  Google Scholar 

  • Austin AT, Ballare CL (2010) Dual role of lignin in plant litter decomposition in terrestrial ecosystems. Proc Natl Acad Sci U S A 107:4618–4622

    Article  CAS  Google Scholar 

  • Battle JM, Golladay SW (2001) Hydroperiod influence on breakdown of leaf litter in cypress-gum wetlands. Am Midl Nat 146:128–145

    Article  Google Scholar 

  • Belova M (1993) Microbial decomposition of freshwater macrophytes in the littoral zone of lakes. Hydrobiologia 251:59–64

    Article  CAS  Google Scholar 

  • Berendse F, Berg B, Bosatta E (1987) The effect of lignin and nitrogen on the decomposition of litter in nutrient poor ecosystems: a theoretical approach. Can J Bot 65:1116–1121

    Article  CAS  Google Scholar 

  • Birgelen APJM, Hebert CD, Wenk ML et al (1999) Toxicity of 3,3′,4,4′-Tetrachloroazobenzene in rats and mice. Toxicol Appl Pharmacol 156:147–159

    Article  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  Google Scholar 

  • Bockers M, Rivero C, Thiede B, Jankowski T, Schmidt B (1994) Uptake, translocation, and metabolism of 3,4-dichloroaniline in soybean and wheat plants. Z Naturforsch 49c:719–726

    Google Scholar 

  • Brunow G, Raiskila S, Sipilä J (1998) The incorporation of 3,4-dichloroaniline, a pesticide metabolite, into dehydrogenation polymers of coniferyl alcohol (DHPs). Acta Chem Scand 52:1338–1342

    Article  CAS  Google Scholar 

  • Bucher VVC, Hyde KD, Pointing SB, Reddy CA (2004) Production of wood decay enzymes, mass loss and lignin solubilization in wood by marine ascomycetes and their anamorphs. Fungal Divers 15:1–14

    Google Scholar 

  • Casida JE, Lykken L (1969) Metabolism of organic pesticide chemicals in higher plants. Annu Rev Plant Physiol 20:607–636

    Article  CAS  Google Scholar 

  • Chen H, Yuan X, Chen Z, Wu Y et al (2011) Methane emissions from the surface of the Three Gorges Reservoir. J Geophys Res 116:1984–2012

    Article  Google Scholar 

  • Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899

    Article  CAS  Google Scholar 

  • Cronk JK, Fennessy MS (2001) Wetland plants: biology and ecology. CRC Press, USA

    Book  Google Scholar 

  • Crossland NO (1990) A review of the fate and toxicity of 3,4-dichloroaniline in aquatic environments. Chemosphere 21:1489–1497

    Article  CAS  Google Scholar 

  • Deba F, Xuan TD, Yasuda M, Tawata S (2007) Herbicidal and fungicidal activities and identification of potential phytotoxins from Bidens pilosa L. var. radiata Scherff. Weed Biol Manag 7:77–83

    Article  CAS  Google Scholar 

  • Duarte S, Pascoal C, Cassio F, Barlocher F (2006) Aquatic hyphomycete diversity and identity affect leaf litter decomposition in microcosms. Oecologia 147:658–666

    Article  Google Scholar 

  • EFSA (2011) Conclusion on the peer review of the pesticide risk assessment of the active substance propanil. EFSA J 9:2085–2147

    Article  Google Scholar 

  • EFSA (2013) Review of the existing MRLs for propanil. EFSA J 11:3280–3301

    Article  Google Scholar 

  • EPA (2003) The propanil RED and fact sheet. United States Environmental Protection Agency, Washington, DC

    Google Scholar 

  • Facell JM (1991) Plant litter: its dynamics and effects on plant community structure. Bot Rev 57:1–32

    Article  Google Scholar 

  • Fisher PJ, Davey RA, Webster JR (1983) Degradation of lignin by aquatic and aero-aquatic hyphomycetes. Trans Br Mycol Soc 80:166–168

    Article  CAS  Google Scholar 

  • Gareis C, Rivero C, Schuphan I, Schmidt B (1992) Plant metabolism of xenobiotics. Comparison of the metabolism of 3,4-dichloroaniline in soybean excised leaves and soybean cell suspension cultures. Z Naturforsch 47c:823–829

    Google Scholar 

  • Gessner MO, Gulis V, Kuehn KA, Chauvet E, Suberkropp K (2007) Fungal decomposers of plant litter in aquatic ecosystems. Environmental and microbial relationships. Mycota 4:301–324

    Article  Google Scholar 

  • Giacomazzi S, Cochet N (2004) Environmental impact of diuron transformation: a review. Chemosphere 56:1021–1032

    Article  CAS  Google Scholar 

  • Godshalk GL, Wetzel RG (1978a) Decomposition of aquatic angiosperms.1. Dissolved components. Aquat Bot 5:281–300

    Article  CAS  Google Scholar 

  • Godshalk GL, Wetzel RG (1978b) Decomposition of aquatic angiosperms. 2. Particulate components. Aquat Bot 5:301–327

    Article  CAS  Google Scholar 

  • Goldman E, Green LH (2008) Practical handbook of microbiology, second edition. CRC Press

  • Gooddy DC, Chilton PJ, Harrison I (2002) A field study to assess the degradation and transport of diuron and its metabolites in a calcareous soil. Sci Total Environ 297:67–83

    Article  CAS  Google Scholar 

  • HC (2006) Heterotrophic plate count in guidelines for Canadian drinking water quality—guideline technical document. Health Canada, Ottawa

    Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil, 347. Berkeley, Calif.: University of California, College of Agriculture, Agriculture Experiment Station

  • Hofstra G, Switzer CM (1968) The phytotoxicity of propanil. Weed Sci 16:23–28

    CAS  Google Scholar 

  • HPA (2005) Colony count by the pour plate method, national standard method w4. Health Protection Agency, UK

    Google Scholar 

  • Kästner M, Nowak KM, Miltner A, Trapp S, Schäffer A (2014) Classification and modelling of nonextractable residue (NER) formation of xenobiotics in soil—a synthesis. Crit Rev Environ Sci Technol 44:2107–2171

    Article  Google Scholar 

  • Khan SU, Kacew S, Akhtar MH (1990) Bound 14C residues in stored wheat treated with [14C] deltamethrin and their bioavailability in rats. J Agric Food Chem 38:1077–1082

    Article  CAS  Google Scholar 

  • Komínková D, Kuehn KA, Büsing N, Steiner D, Gessner MO (2000) Microbial biomass, growth, and respiration associated with submerged litter of Phragmites australis decomposing in a littoral reed stand of a large lake. Aquat Microb Ecol 22:271–282

    Article  Google Scholar 

  • Leroy CJ, Marks JC (2006) Litter quality, stream characteristics and litter diversity influence decomposition rates and macroinvertebrates. Freshw Biol 51:605–617

    Article  Google Scholar 

  • Li B, Yuan X, Xiao H, Chen Z (2011) Design of the dike-pond system in the littoral zone of a tributary in the Three Gorges Reservoir, China. Ecol Eng 37:1718–1725

    Article  Google Scholar 

  • Li B, Xiao H, Yuan X, Willison JHM, Liu H, Chen Z, Zhang Y, Deng W, Yue J (2013) Analysis of ecological and commercial benefits of a dike-pond project in the drawdown zone of the Three Gorges Reservoir. Ecol Eng 61:1–11

    Article  Google Scholar 

  • Lieb HB, Still GG (1969) Herbicide metabolism in plants: specificity of peroxidases for aniline substrates. Plant Physiol 44:1672–1673

    Article  CAS  Google Scholar 

  • Martins M, Rodrigues-Lima F, Dairou J, Lamouri A, Malagnac F, Silar P, Dupret JM (2009) An acetyltransferase conferring tolerance to toxic aromatic amine chemicals: molecular and functional studies. J Biol Chem 284:18726–18733

    Article  CAS  Google Scholar 

  • McMillan DC, Freeman JP, Hinson JA (1990a) Metabolism of the arylamide herbicide propanil. I. Microsomal metabolism and in vitro methemoglobinemia. Toxicol Appl Pharmacol 103:90–101

    Article  CAS  Google Scholar 

  • McMillan DC, Leakey JE, Arlotto MP, McMillan JM, Hinson JA (1990b) Metabolism of the arylamide herbicide propanil. II. Effects of propanil and its derivatives on hepatic microsomal drug-metabolizing enzymes in the rat. Toxicol Appl Pharmacol 103:102–112

    Article  CAS  Google Scholar 

  • Minderman G (1968) Addition, decomposition and accumulation of organic matter in forests. J Ecol 56:355–362

    Article  Google Scholar 

  • Mitsou K, Koulianou A, Lambropoulou D, Papps P, Albanis T, Lekka M (2006) Growth rate effects, responses of antioxidant enzymes and metabolic fate of the herbicide propanil in the aquatic plant Lemna minor. Chemosphere 62:275–284

    Article  CAS  Google Scholar 

  • Mordaunt CJ, Gevao B, Jones KC, Semple KT (2005) Formation of non-extractable pesticide residues: observations on compound differences, measurement and regulatory issues. Environ Pollut 133:25–34

    Article  CAS  Google Scholar 

  • Nakai A, Shiwaku T, Hasegawa H, Hashimoto T (1986) Spinodal decomposition of polymer mixtures with a thermotropic liquid-crystalline polymer as one-component. Macromolecules 19:3008–3010

    Article  CAS  Google Scholar 

  • Oda M, Yukimoto M (1975) Fate of propanil in soils 1. The formation of 3,4-dichloroacetanilide (DCAA). J Weed Sci Technol 20:12–17

    Article  CAS  Google Scholar 

  • Paul RWJ, Benfield EF, Cairns JJ (1983) Dynamics of leaf processing in a medium-sized river. See Ref 97:403–423

    Google Scholar 

  • Poland A, Clover E, Kende AS, DeCamp M, Giandomenico CM (1976) 3,4,3′,4′-Tetrachloro azoxybenzene and azobenzene: potent inducers of aryl hydrocarbon hydroxylase. Science 194:627–630

    Article  CAS  Google Scholar 

  • Pothuluri JV, Hinson JA, Cerniglia CE (1991) Propanil: toxicological characteristics, metabolism, and biodegradation potential in soil. J Environ Qual 20:330–347

    Article  CAS  Google Scholar 

  • Romaní AM, Fischer H, Mille-Lindblom C, Tranvik LJ (2006) Interactions of bacterial and fungi on decomposing litter: differential extracellular enzyme activities. Ecology 87:2559–2569

    Article  Google Scholar 

  • Sánchez C (2009) Lignocellulosic residues: biodegradation and bioconversion by fungi. Biotechnol Adv 27:185–194

    Article  Google Scholar 

  • Sandermann H Jr (2004) Bound and unextractable pesticidal plant residues: chemical characterization and consumer exposure. Pest Manag Sci 60:613–623

    Article  CAS  Google Scholar 

  • Sandermann H Jr, Arjmand M, Gennity I, Winkler R (1990) Animal bioavailability of defined xenobiotic lignin metabolites. J Agric Food Chem 38:1877–1880

    Article  CAS  Google Scholar 

  • Sandermann JH, Heller W, Hertkorn N et al (1998) A new intermediate in the mineralization of 3,4-dichloroaniline by the white rot fungus Phanerochaete chrysosporium. Appl Environ Microbiol 64:3305–3312

    CAS  Google Scholar 

  • Schmidt B (1999) Non-extractable residues of pesticide and xenobiotics in plants—a review. Recent Res Dev Agric Food Chem 3:329–354

    CAS  Google Scholar 

  • Schmidt B, Schuphan I (2002) Metabolism of the environmental estrogen bisphenol A by plant cell suspension cultures. Chemosphere 49:51–59

    Article  CAS  Google Scholar 

  • Schmitz A, Nagel R (1995) Influence of 3,4-dichloroaniline (3,4-DCA) on benthic invertebrates in indoor experimental streams. Ecotoxicol Environ Saf 30:63–71

    Article  CAS  Google Scholar 

  • Singh J, Bingley R (1991) Levels of 3,3′,4,4′-tetrachloroazobenzene in propanil herbicide. Bull Environ Contam Toxicol 47:822–826

    Article  CAS  Google Scholar 

  • Skidmore MW, Paulson GD, Kuiper HA, Ohlin B, Reynolds S (1998) Bound xenobiotic residues in food commodities of plant and animal origin. IUPAC, Great Britain

    Google Scholar 

  • Still GG (1968) Metabolism of 3,4-dichloropropionanilide in plants: the metabolic fate of the 3,4-dichloroanilide moiety. Science. 159:992–993

  • Still GG (1969) 3,4,3′,4′-Tetrachloroazobenzene: its translocation and metabolism in rice plants. Weed Res 9:211–217

    Article  CAS  Google Scholar 

  • Still GG, Mansager ER (1969) The presence of 3,4-dichloroaniline in rice grain hydrolysates. Weed Res 9:218–223

    Article  CAS  Google Scholar 

  • Still GG, Balba HM, Mansager ER (1981) Studies on the nature and identity of bound chloroaniline residues in plants. J Agric Food Chem 29:739–746

    Article  CAS  Google Scholar 

  • Suberkropp K, Klug MJ (1980) The maceration of deciduous leaf litter by aquatic hyphomycetes. Can J Bot 58:1025–1031

    Article  CAS  Google Scholar 

  • Sun R, Yuan X, Chen Z, Zhang Y, Liu H (2012) Effect of Three Gorges Reservoir (Yangzi River) on the plant species richness in drawdown zone of downstream the tributary river (Pengxi River). Russ J Ecol 43:307–314

    Article  Google Scholar 

  • Sydes C, Grime JP (1981) Effects of tree leaf litter on herbaceous vegetation in the deciduous woodlands. II An experimental investigation. J Ecol 69:249–262

    Article  Google Scholar 

  • Taylor BR, Parkinson D, Parsons WFJ (1989) Nitrogen and lignin content as predictors of litter decay rates: a microcosm test. Ecology 70:97–104

    Article  Google Scholar 

  • Trenck KT, Hunkler D, Sandermann JH (1981) Incorporation of chlorinated anilines into lignin. Z Naturforsch 36c:714–720

    Google Scholar 

  • Tristan Gingerich R, Anderson JT (2011) Litter decomposition in created and reference wetlands in west Virginia, USA. Wetl Ecol Manag 19:449–458

    Article  Google Scholar 

  • Villeneuve A, Larroudé S, Humbert JF (2011): Pesticides - formulations, effects, fate. Herbicide contamination of freshwater ecosystems: impact on microbial communities. In Tech, 285–313 pp

  • Volnova AI, Surovtseva EG, Vasieva GK (1980) Acetylation of 3,4-dichloroaniline by representatives of the genus Pseudomonas. Microbiologiia 49:167–170

    CAS  Google Scholar 

  • Vymazala J, Kröpfelová L (2009) Removal of organics in constructed wetlands with horizontal sub-surface flow: a review of the field experience. Sci Total Environ 407:3911–3922

    Article  Google Scholar 

  • Wang Q, Yuan X, Liu H et al (2012) Effect of long-term winter flooding on the vascular flora in the drawdown area of the Three Gorges Reservoir, China. Pol J Ecol 60:95–106

    Google Scholar 

  • Webster JR, Benfield EF (1986) Vascular plant breakdown in freshwater ecosystems. Annu Rev Ecol Syst 17:567–594

    Article  Google Scholar 

  • Williams JB (2002) Phytoremediation in wetland ecosystems: progress, problems, and potential. Crit Rev Plant Sci 21:607–635

    Article  CAS  Google Scholar 

  • Willison JHM, Li R, Yuan X (2013) Conservation and ecofriendly utilization of wetlands associated with the Three Gorges Reservoir. Environ Sci Pollut Res 20:6907–6916

    Article  Google Scholar 

  • Witt KL, Zeiger E, Tice RR, Birgelen APJM (2000) The genetic toxicity of 3,3′,4,4′-tetrachloroazobenzene and 3,3′,4,4′-tetrachloroazoxybenzene: discordance between acute mouse bone marrow and peripheral blood subchronic mouse micronucleus test results. Mutat Res 472:147–154

    Article  CAS  Google Scholar 

  • Yang WC (2014) Botanical, pharmacological, phytochemical, and toxicological aspects of the antidiabetic plant Bidens pilosa L. Evid Based Complement Alternat Med 2014:698617

    Google Scholar 

  • Yih RY, McRae DH, Wilson HF (1968) Mechanism of selective action of 3′,4′-dichloropropionanilide. Plant Physiol 43:1291–1296

    Article  CAS  Google Scholar 

  • Yuan X, Zhang Y, Liu H, Xiong S, Li B, Deng W (2013) The littoral zone in the Three Gorges Reservoir, China: challenges and opportunities. Environ Sci Pollut Res 20:7092–7102

    Article  Google Scholar 

  • Zemek J, Linek K, Kadlecikova B, Kucar S, Somogyi L (1985) Antimicrobial effect of osazones of sugars and anhydro sugars. Folia Microbiol 30:396

    Article  CAS  Google Scholar 

  • Zhang P (2013) The fate of 14C-labeled 3,4-dichloroaniline in a water-sediment system. RWTH Aachen University, Aachen, Germany

    Google Scholar 

  • Zok S, Görge K, Kalsch W, Nagel R (1991) Bioconcentration, metabolism and toxicity of substituted anilines in the zebrafish (Brachydanio rerio). Sci Total Environ 109–110:411–421

    Article  Google Scholar 

Download references

Acknowledgments

This research has been supported by the Yangtze project of German Federal Ministry of Education and Research (BMBF) (No. FKZ 02WT1141) and the China Scholarship Council (CSC). We thank Dr. Joachim Jahnke for help with the analysis of C, H, N contents of B. pilosa and great advices regarding the microbial plate count method.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhongli Chen.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, Z., Schmidt, B. & Schäffer, A. Uptake and decomposition of the herbicide propanil in the plant Bidens pilosa L. dominating in the Yangtze Three Gorges Reservoir (TGR), China. Environ Sci Pollut Res 24, 11141–11153 (2017). https://doi.org/10.1007/s11356-016-6068-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-6068-8

Keywords

Navigation