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Biological responses of maize (Zea mays) plants exposed to chlorobenzenes. Case study of monochloro-, 1,4-dichloro- and 1,2,4-trichloro-benzenes

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Abstract

A 7-day-exposure time experiment was designed to investigate the phytotoxicity of chlorobenzenes (CBs) on Zea mays seedlings, focusing on the growth and generation of oxidative stress. Significant growth inhibition (based on biomass gain) was observed for exposure to monochlorobenzene (MCB), dichlorobenzene (DCB) and trichlorobenzene (TCB) concentrations higher than 10 mg l−1. It would seem that CBs inhibit cell division, since the mitotic index decreased for roots exposed to DCB at 80 mg l−1 dose (8%) and to all the TCB concentrations tested (20% inhibition). CBs exposure resulting in an increase in the oxidative stress response in maize seedlings [reactive oxygen species like H2O2, antioxidant enzymes (POD, GR), lipid peroxidation] correlated to the compound’s degree of chlorination, where damage increasing with the number of chlorine atoms (MCB < DCB < TCB). This biological response was also dependent on the dose-exposure. Z. mays exposed to CBs at concentrations <10 mg l−1 did not induce sufficient oxidative damage to cause root cell death. Therefore, CBs at current environmental concentrations are unlikely to produce evident phytotoxic effects on Z. mays seedlings.

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References

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  Google Scholar 

  • Bakkali Y, Ruiz-Santaella JP, Osuna MD, Wagner J, Fischer AJ, De Prado R (2007) Late watergrass (Echinochloa phyllopogon): mechanisms involved in the resistance to fenoxaprop-p-ethyl. J Agric Food Chem 55:4052–4058

    Article  CAS  Google Scholar 

  • Bohme F, Welsch-Pausch K, McLachlan MS (1999) Uptake of airborne semivolatile organic compounds in agricultural plants: field measurements of interspecies variability. Environ Sci Technol 33:1805–1813

    Article  Google Scholar 

  • Calabrese EJ, Baldwin LA (2002) Hormesis and high-risk groups. Regul Toxicol Pharmacol 35:414–428

    Article  CAS  Google Scholar 

  • Calabrese V, Cornelius C, Dinkova-Kostova AT, Calabrese EJ, Mattson MP (2010) Cellular stress responses, the hormesis paradigm, and vitagenes: novel targets for therapeutic intervention in neurodegenerative disorders. Antioxid Redox Signal 13:1763–1811

    Article  CAS  Google Scholar 

  • Chaudhry Q, Schroder P, Werck-Reichhart D, Grajek W, Marecik R (2002) Prospects and limitations of phytoremediation for the removal of persistent pesticides in the environment. Environ Sci Pollut Res 9:4–17

    Article  CAS  Google Scholar 

  • Cherifi M, Raveton M, Picciocchi A, Ravanel P, Tissut M (2001) Atrazine metabolism in corn seedlings. Plant Physiol Biochem 39:665–672

    Article  CAS  Google Scholar 

  • Cummins I, Cole DJ, Edwards R (1999) A role for glutathione transferases functioning as glutathione peroxidases in resistance to multiple herbicides in black-grass. Plant J 18:285–292

    Article  CAS  Google Scholar 

  • Cuypers A, Vangronsveld J, Clijsters H (2002) Peroxidases in roots and primary leaves of Phaseolus vulgaris copper and zinc phytotoxicity: a comparison. J Plant Physiol 159:869–876

    Article  CAS  Google Scholar 

  • Dat J, Vandenabeele S, Vranova E, Van Montagu M, Inze D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795

    Article  CAS  Google Scholar 

  • Deng XY, Li JW, Zhou ZQ, Fan HY (2010) Cell death in wheat roots induced by the powdery mildew fungus Blumeria graminis f. sp tritici. Plant Soil 328:45–55

    Article  CAS  Google Scholar 

  • Dobrowolska G, Muszynska G, Shugar D (1991) Benzimidazole nucleoside analogs as inhibitors of plant (maize seedling) casein kinases. Biochim Biophys Acta 1080:221–226

    Article  CAS  Google Scholar 

  • Feidieker D, Kampfer P, Dott W (1994) Microbiological and chemical evaluation of a site contaminated with chlorinated aromatic-compounds and hexachlorocyclohexanes. FEMS Microbiol Ecol 15:265–278

    Article  CAS  Google Scholar 

  • Feidieker D, Kampfer P, Dott W (1995) Field-scale investigations on the biodegradation of chlorinated aromatic-compounds and HCH in the subsurface environment. J Contam Hydrol 19:145–169

    Article  CAS  Google Scholar 

  • Figueiredo MVB, Burity HA, Martinez CR, Chanway CP (2007) Drought stress response on some key enzymes of cowpea (Vigna unguiculata L. Walp.) nodule metabolism. World J Microbiol Biotechnol 23:187–193

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071

    Article  CAS  Google Scholar 

  • Geoffroy L, Frankart U, Eullaffroy P (2004) Comparison of different physiological parameter responses in Lemna minor and Scenedesmus obliquus exposed to herbicide flumioxazin. Environ Pollut 131:233–241

    Article  CAS  Google Scholar 

  • Hatton PJ, Cummins I, Price LJ, Cole DJ, Edwards R (1998) Glutathione transferases and herbicide detoxification in suspension-cultured cells of giant foxtail (Setaria faberi). Pestic Sci 53:209–216

    Article  CAS  Google Scholar 

  • Hatzios KK, Burgos N (2004) Metabolism-based herbicide resistance: regulation by safeners. Weed Sci 52:454–467

    Article  CAS  Google Scholar 

  • He YY, Hader DP (2002) UV-B-induced formation of reactive oxygen species and oxidative damage of the cyanobacterium Anabaena sp.: protective effects of ascorbic acid and N-acetyl-l-cysteine. J Photochem Photobiol B 66:115–124

    Article  CAS  Google Scholar 

  • Kawahigashi H, Hirose S, Ohkawa H, Ohkawa Y (2005) Phytoremediation of metolachlor by transgenic rice plants expressing human CYP2B6. J Agric Food Chem 53:9155–9160

    Article  CAS  Google Scholar 

  • Kong FX, Hu W, Liu Y (1998) Molecular structure and biochemical toxicity of four halogeno-benzenes on the unicellular green alga Selenastrum capricornutum. Environ Exp Bot 40:105–111

    Article  CAS  Google Scholar 

  • Kraaij H, Connell DW (1997) Bioconcentration and uptake kinetics of chlorobenzenes in soy-bean roots. Chemosphere 34:2607–2620

    Article  CAS  Google Scholar 

  • Lammel G, Klanova J, Kohoutek J, Prokes R, Ries L, Stohl A (2009) Observation and origin of organochlorine compounds and polycyclic aromatic hydrocarbons in the free troposphere over central Europe. Environ Pollut 157:3264–3271

    Article  CAS  Google Scholar 

  • Landberg T, Greger M (2002) Differences in oxidative stress in heavy metal resistant and sensitive clones of Salix viminalis. J Plant Physiol 159:69–75

    Article  CAS  Google Scholar 

  • Lee CL, Song HJ, Fang MD (2000) Concentrations of chlorobenzenes, hexachlorobutadiene and heavy metals in surficial sediments of Kaohsiung coast, Taiwan. Chemosphere 41:889–899

    Article  CAS  Google Scholar 

  • Liu W, Zhou QX, Li PJ, Sun TH, Yang YS, Xiong XZ (2003) 1,2,4-Trichlorobenzene induction of chromosomal aberrations and cell division of root-tip cells in Vicia faba seedlings. Bull Environ Contam Toxicol 71:689–697

    Article  CAS  Google Scholar 

  • Liu W, Yang YS, Li P, Zhou Q, Sun T (2004) Root growth inhibition and induction of DNA damage in soybean (Glycine max) by chlorobenzenes in contaminated soil. Chemosphere 57:101–106

    Article  CAS  Google Scholar 

  • Liu H, Weisman D, Ye YB, Cui B, Huang YH, Colon-Carmona A, Wang ZH (2009) An oxidative stress response to polycyclic aromatic hydrocarbon exposure is rapid and complex in Arabidopsis thaliana. Plant Sci 176:375–382

    Article  CAS  Google Scholar 

  • Lomonte C, Sgherri C, Baker AJM, Kolev SD, Navari-Izzo F (2010) Antioxidative response of Atriplex codonocarpa to mercury. Environ Exp Bot 69:9–16

    Article  CAS  Google Scholar 

  • Ma XM, Havelka MM (2009) Phytotoxicity of chlorinated benzenes to Typha angustifolia and Phragmites communis. Environ Toxicol 24:43–48

    Article  CAS  Google Scholar 

  • Mackay D, Di Guardo A, Paterson S, Kicsi G, Cowan CE, Kane M (1996) Assessment of chemical fate in the environment using evaluative, regional and local-scale models: illustrative application to chlorobenzene and linear alkylbenzene sulfonates. Environ Toxicol Chem 15:1638–1648

    Article  CAS  Google Scholar 

  • Malcolm HM, Howe PD, Dobson S (2004) Chlorobenzenes other than hexachlorobenzene: environmental aspects. World Health Organization, Geneva

    Google Scholar 

  • Marcacci S, Raveton M, Ravanel P, Schwitzguebel JP (2006) Conjugation of atrazine in vetiver (Chrysopogon zizanioides Nash) grown in hydroponics. Environ Exp Bot 56:205–215

    Article  CAS  Google Scholar 

  • Meharg AA, Wright J, Osborn D (2000) Chlorobenzenes in rivers draining industrial catchments. Sci Total Environ 251:243–253

    Article  Google Scholar 

  • Menone ML, Pflugmacher S (2005) Effects of 3-chlorobiphenyl on photosynthetic oxygen production, glutathione content and detoxication enzymes in the aquatic macrophyte Ceratophyllum demersum. Chemosphere 60:79–84

    Article  CAS  Google Scholar 

  • Menone ML, Pesce SF, Diaz MP, Moreno VJ, Wunderlin DA (2008) Endosulfan induces oxidative stress and changes on detoxication enzymes in the aquatic macrophyte Myriophyllum quitense. Phytochemistry 69:1150–1157

    Article  CAS  Google Scholar 

  • Michalowicz J, Duda W (2009) The effects of 2,4,5-trichlorophenol on some antioxidative parameters and the activity of glutathione S-transferase in reed canary grass leaves (Phalaris arudinacea). Pol J Environ Stud 18:845–852

    CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  CAS  Google Scholar 

  • Monferran MV, Wunderlin DA, Nimptsch J, Pflugmacher S (2007) Biotransformation and antioxidant response in Ceratophyllum demersum experimentally exposed to 1,2- and 1,4-dichlorobenzene. Chemosphere 68:2073–2079

    Article  CAS  Google Scholar 

  • Murshed R, Lopez-Lauri F, Sallanon H (2008) Microplate quantification of enzymes of the plant ascorbate–glutathione cycle. Anal Biochem 383:320–322

    Article  CAS  Google Scholar 

  • Paradiso A, Berardino R, de Pinto MC, di Toppi LS, Storelli MM, Tommasi F, De Gara L (2008) Increase in ascorbate–glutathione metabolism as local and precocious systemic responses induced by cadmium in durum wheat plants. Plant Cell Physiol 49:362–374

    Article  CAS  Google Scholar 

  • Park JW, Dec J, Kim JE, Bollag JM (2000) Transformation of chlorinated phenols and anilines in the presence of humic acid. J Environ Qual 29:214–220

    Article  CAS  Google Scholar 

  • Passardi F, Penel C, Dunand C (2004) Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci 9:534–540

    Article  CAS  Google Scholar 

  • Pennathur S, Maitra D, Byun J, Sliskovic I, Abdulhamid I, Saed GM, Diamond MP, Abu-Soud HM (2010) Potent antioxidative activity of lycopene: a potential role in scavenging hypochlorous acid. Free Radic Biol Med 49:205–213

    Article  CAS  Google Scholar 

  • Petroutsos D, Katapodis P, Samiotaki M, Panavotou G, Kekos D (2008) Detoxification of 2,4-dichlorophenol by the marine microalga Tetraselmis marina. Phytochemistry 69:707–714

    Article  CAS  Google Scholar 

  • Pierre JL, Fontecave M (1999) Iron and activated oxygen species in biology: the basic chemistry. Biometals 12:195–199

    Article  CAS  Google Scholar 

  • Popp P, Bruggemann L, Keil P, Thuss U, Weiss H (2000) Chlorobenzenes and hexachlorocyclohexanes (HCHs) in the atmosphere of Bitterfeld and Leipzig (Germany). Chemosphere 41:849–855

    Article  CAS  Google Scholar 

  • Ramel F, Sulmon C, Bogard M, Couee I, Gouesbet G (2009) Differential patterns of reactive oxygen species and antioxidative mechanisms during atrazine injury and sucrose-induced tolerance in Arabidopsis thaliana plantlets. BMC Plant Biol 9:28–46

    Article  Google Scholar 

  • Rouhier N, Koh CS, Gelhaye E, Corbier C, Favier F, Didierjean C, Jacquot JP (2008) Redox based anti-oxidant systems in plants: biochemical and structural analyses. Biochim Biophys Acta 1780:1249–1260

    Article  CAS  Google Scholar 

  • Schroll R, Scheunert I (1992) A laboratory system to determine separately the uptake of organic chemicals from soil by plant roots and by leaves after vaporization. Chemosphere 24:97–108

    Article  CAS  Google Scholar 

  • Sinha S (2002) Oxidative stress induced by HCH in Hydrilla verticillata (l.f.) Royle: modulation in uptake and toxicity due to Fe. Chemosphere 46:281–288

    Article  CAS  Google Scholar 

  • Sunohara Y, Matsumoto H (2008) Quinclorac-induced cell death is accompanied by generation of reactive oxygen species in maize root tissue. Phytochemistry 69:2312–2319

    Article  CAS  Google Scholar 

  • Talano MA, Frontera S, Gonzalez P, Medina MI, Agostini E (2010) Removal of 2,4-dichlorophenol from aqueous solutions using tobacco hairy root cultures. J Hazard Mater 176:784–791

    Article  CAS  Google Scholar 

  • Tam DD, Shiu WY, Qiang K, Mackay D (1996) Uptake of chlorobenzenes by tissues of the soybean plant: equilibria and kinetics. Environ Toxicol Chem 15:489–494

    Article  CAS  Google Scholar 

  • Wang MJ, Jones KC (1994a) Occurrence of chlorobenzenes in 9 United-Kingdom retail vegetables. J Agric Food Chem 42:2322–2328

    Article  CAS  Google Scholar 

  • Wang MJ, Jones KC (1994b) Behavior and fate of chlorobenzenes (CBs) introduced into soil–plant systems by sewage-sludge application—a review. Chemosphere 28:1325–1360

    Article  CAS  Google Scholar 

  • Wang MJ, Bokern M, Boehme C, Jones KC, Harms H (1996) Phytotoxicity, uptake and metabolism of 1,4-dichlorobenzene by plant cells. Environ Toxicol Chem 15:1109–1114

    Article  CAS  Google Scholar 

  • Wrona M, Wardman P (2006) Properties of the radical intermediate obtained on oxidation of 2′,7′-dichlorodihydrofluorescein, a probe for oxidative stress. Free Radic Biol Med 41:657–667

    Article  CAS  Google Scholar 

  • Zhang JY, Zhao W, Pan J, Qiu LM, Zhu YM (2005) Tissue-dependent distribution and accumulation of chlorobenzenes by vegetables in urban area. Environ Int 31:855–860

    Article  CAS  Google Scholar 

  • Zhou X, Deng SB, Huang J, Yu G, Lv HL (2009) Occurrence and distribution of chlorobenzenes in the Tonghui river of Beijing, China. Arch Environ Contam Toxicol 57:32–41

    Article  CAS  Google Scholar 

  • Zimmermann P, Zentgraf U (2005) The correlation between oxidative stress and leaf senescence during plant development. Cell Mol Biol Lett 10:515–534

    CAS  Google Scholar 

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Acknowledgments

This work is part of VALORSITE-PHYCO project funded by AXELERA. We are especially grateful to Agnès Pilas-Bégué for valuable suggestions. The authors wish to thank Version Originale for correcting the English text.

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Authors and Affiliations

  1. Laboratoire d’Ecologie Alpine, UMR CNRS no. 5553, Université Joseph Fourier, BP 53, 38041, Grenoble Cedex 09, France

    Angélique San Miguel, Mathieu Faure, Patrick Ravanel & Muriel Raveton

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  1. Angélique San Miguel
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  2. Mathieu Faure
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  3. Patrick Ravanel
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  4. Muriel Raveton
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Correspondence to Muriel Raveton.

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Miguel, A.S., Faure, M., Ravanel, P. et al. Biological responses of maize (Zea mays) plants exposed to chlorobenzenes. Case study of monochloro-, 1,4-dichloro- and 1,2,4-trichloro-benzenes. Ecotoxicology 21, 315–324 (2012). https://doi.org/10.1007/s10646-011-0792-0

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