Advertisement

Plant and Soil

, 317:93 | Cite as

Antimony accumulation and antioxidative responses in four fern plants

  • Renwei Feng
  • Chaoyang Wei
  • Shuxin Tu
  • Fengchang Wu
  • Linsheng Yang
Regular Article

Abstract

Antimony (Sb) toxicity and contamination has become a growing concern in recent years. Remediation of Sb contamination using plants may be an effective approach. This study aimed to investigate the potential of antimony (Sb) tolerance and accumulation by plants, as well as to understand the antioxidative responses to Sb. One set of hydroponic trials was set up using four species of fern plants, including Pteris cretica (PCA), Microlepia hancei (MH), Cyrtomium fortunei (CYF) and Cyclosorus dentatus (CYD). Ferns were grown for 2 weeks in nutrient solution containing a medium (5 mg L−1) and a high (20 mg L−1) rate of Sb, with no Sb added as the control. The biomass of fern PCA remained constant with Sb addition, whereas the biomass of ferns CYF, MH and CYD at the high Sb rate exposure decreased by 12.5%, 35.0% and 38.3%, respectively as compared with their controls. This suggests a high to low Sb tolerance order for these four fern plants. For all of these fern plants, more Sb was accumulated in the roots than in the fronds. Antimony concentration in the roots at the high rate of Sb addition was recorded, on average, as 358 mg kg−1 for fern PCA, 224 mg kg−1 for fern CYF, 124 mg kg−1 for fern CYD and 123 mg kg−1 for fern MH. A high rate of addition of Sb increased the contents of malondialdehyde (MDA) by 41.3% and 171.6% for ferns MH and CYD, respectively, as compared with their controls. No changes for MDA contents were observed in ferns PCA and CYF with Sb addition, indicating no lipid peroxidation reaction in these two plants. At a medium rate of Sb addition, the activities of peroxidase, catalase and ascorbate peroxidase in fern PCA were much higher than those in ferns CYF, CYD and MH, demonstrating the important role of these three enzymes in resisting Sb toxicity. The consistency in unchanged biomass, high accumulation of Sb in roots, lower MDA contents, as well as high enzyme production in fronds, indicated that fern PCA was more tolerant to Sb than the other three fern plants. Antioxidative enzymes (peroxidase, catalase and ascorbate peroxidase) might be involved in Sb toxicity resistance of fern PCA.

Keywords

Arsenic hyperaccumulator Antimony Antioxidants Tolerance Phytoremediation 

Abbreviations

PCA

Pteris cretica

CYF

Cyrtomium fortunei

CYD

Cyclosorus dentatus

MH

Microlepia hancei

MDA

malondialdehyde

SOD

superoxide dismutase

POD

peroxidase

CAT

catalase

APX

ascorbate peroxidase

GR

glutathione reductase

Notes

Acknowledgements

This research was supported by the National Science Foundation of China (40632011, 20477045), the National Key Technologies R&D Program of China during the 11th Five-Year Plan Period (2006BAJ05A08), and the Renovation Project of the Institute of Geographical Sciences and Natural Resources Research, Chinese Academy of Sciences (CXIOG-C04-02). We thank Ms. Ling-Mei Wang for her assistance in chemical analysis. We also thank the two anonymous reviewers for their thoughtful comments, which help to greatly improve the quality of this manuscript.

References

  1. Ainsworth N, Cooke JA, Johnson MS (1990a) Distribution of antimony in contaminated grassland: I-Vegetation and soils. Environ Pollut 65:65–77 doi: 10.1016/0269-7491(90)90165-9 PubMedCrossRefGoogle Scholar
  2. Ainsworth N, Cooke JA, Johnson MS (1990b) Distribution of antimony in contaminated grassland: II-Small mammals and invertebrates. Environ Pollut 65:79–87 doi: 10.1016/0269-7491(90)90166-A PubMedCrossRefGoogle Scholar
  3. Ainsworth N, Cooke JA, Johnson MS (1991) Biological significance of antimony in contaminated grassland. Water Air Soil Pollut 57–58:193–199 doi: 10.1007/BF00282882 CrossRefGoogle Scholar
  4. Assche Van F, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13:195–206 doi: 10.1111/j.1365-3040.1990.tb01304.x CrossRefGoogle Scholar
  5. Baker AJM (1981) Accumulators and excluders—strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654CrossRefGoogle Scholar
  6. Baker CJ, Orlandi EW (1995) Active Oxygen in Plant Pathogenesis. Annu Rev Phytopathol 33:299–321 doi: 10.1146/annurev.py.33.090195.001503 PubMedCrossRefGoogle Scholar
  7. Baroni F, Boscagli A, Protano G, Riccobono F (2000) Antimony accumulation in Achillea ageratum, Plantago lanceolata and Silene vulgaris growing in an old Sb-mining area. Environ Pollut 109:347–352 doi: 10.1016/S0269-7491(99)00240-7 PubMedCrossRefGoogle Scholar
  8. Brennan T, Frenkel C (1977) Involvement of Hydrogen Peroxide in the Regulation of Senescence in Pear. Plant Physiol 59:411–416PubMedCrossRefGoogle Scholar
  9. Brun CB, Astrom ME, Peltola P, Johansson MB (2008) Trends in major and trace elements in decomposing needle litters during a long-term experiment in Swedish forests. Plant Soil 306:199–210 doi: 10.1007/s11104-008-9572-x CrossRefGoogle Scholar
  10. Cao X, Ma LQ, Tu C (2004) Antioxidative responses to arsenic in the arsenic-hyperaccumulator Chinese brake fern (Pteris vittata L.). Environ Pollut 128:317 doi: 10.1016/j.envpol.2003.09.018 PubMedCrossRefGoogle Scholar
  11. Chen TB, Wei CY, Huang ZC, Huang QF, Lu QG (2002) Arsenic hyperaccumulator Pteris vittata L. and its arsenic accumulation.. Chin Sci Bull 47:902–905 doi: 10.1360/02tb9202 Google Scholar
  12. Crommentuijn T, Sijm D, de Bruijn J, van den Hoop M, van Leeuwen K, van de Plassche E (2000) Maximum permissible and negligible concentrations for metals and metalloids in the Netherlands, taking into account background concentrations. J Environ Manage 60:121–143 doi: 10.1006/jema.2000.0354 CrossRefGoogle Scholar
  13. De Gregori I, Fuentes E, Rojas M, Pinochet H, Potin-Gautier M (2003) Monitoring of copper, arsenic and antimony levels in agricultural soils impacted and non-impacted by mining activities, from three regions in Chile. J Environ Monit 5:287–295 doi: 10.1039/b211469k PubMedCrossRefGoogle Scholar
  14. Donahue JL, Okpodu CM, Cramer CL, Grabau EA, Alscher RG (1997) Responses of antioxidants to paraquat in pea leaves (relationships to resistance). Plant Physiol 113:249–257PubMedGoogle Scholar
  15. Eikmann T, Kloke A (1993) Nutzungs- und schutzgutbezogene Orientierungswerte fur (Schad-) stoffe in Boden. In: Rosenkranz D, Bachmann G, Einsele G, Harress HM (eds) Bodenschutz. Ergänzbares Handbuch der Maßnahmen und Empfehlungen für Schutz, Pflege und Sanierung von Böden, Landschaft und Grundwasser-1, Band, 14 Lfg X/93. Erich Schmidt, Berlin, GermanyGoogle Scholar
  16. EU (1998) Council Directive 98/83/EC of 3 November 1998, Quality of Water Intended for Human consumption. Official J L 330, 05/12/1998, pp 32–54Google Scholar
  17. Filella M, Belzile N, Chen YW (2002) Antimony in the environment: a review focused on natural waters: I. Occurrence. Earth Sci Rev 57:125–176 doi: 10.1016/S0012-8252(01)00070-8 CrossRefGoogle Scholar
  18. Foyer CH, Noctor G (2000) Oxygen processing in photosynthesis: regulation and signalling. New Phytol 146:359–388 doi: 10.1046/j.1469-8137.2000.00667.x CrossRefGoogle Scholar
  19. Fu J, Huang B (2001) Involvement of antioxidants and lipid peroxidation in the adaptation of two cool-season grasses to localized drought stress. Environ Exp Bot 45:105–114 doi: 10.1016/S0098-8472(00)00084-8 PubMedCrossRefGoogle Scholar
  20. Gebel T (1998) Suppression of arsenic-induced chromosome mutagenicity by antimony. Mutat Res 412:213–218PubMedGoogle Scholar
  21. Giannopolitis CN, Ries SK (1977) Superoxide Dismutases: I. Occurrence in Higher Plants. Plant Physiol 59:309–314Google Scholar
  22. Gonzalez CM, Casanovas SS, Pignata ML (1996) Biomonitoring of air pollutants from traffic and industries employing Ramalina ecklonii (Spreng.) Mey. and Flot. in Cordoba, Argentina. Environ Pollut 91:269–277 doi: 10.1016/0269-7491(95)00076-3 CrossRefGoogle Scholar
  23. Hartikainen H, Xue T, Piironen V (2000) Selenium as an anti-oxidant and pro-oxidant in ryegrass. Plant Soil 225:193–200 doi: 10.1023/A:1026512921026 CrossRefGoogle Scholar
  24. He MC (2007) Distribution and phytoavailability of antimony at an antimony mining and smelting area, Hunan, China. Environ Geochem Health 29:209–219 doi: 10.1007/s10653-006-9066-9 PubMedCrossRefGoogle Scholar
  25. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Cal Agric Exp Sta Cir 347:1–32Google Scholar
  26. Kabata-Pendias A, Pendias H (2001) Trace elements in soils and plants., 3rd edn. CRC Press, Boca Raton, FL, USAGoogle Scholar
  27. Koricheva J, Roy S, vranjic JA, Haukioja E, Hughes PR, Hanninen O (1997) Antioxidant responses to simulated acid rain and heavy metal deposition in birch seedlings. Environ Pollut 95:249–258 doi: 10.1016/S0269-7491(96)00071-1 PubMedCrossRefGoogle Scholar
  28. Lagrimini LM (1991) Wound-Induced Deposition of Polyphenols in Transgenic Plants Overexpressing Peroxidase. Plant Physiol 96:577–583PubMedCrossRefGoogle Scholar
  29. Ma LQ, Komar KM, Tu C, Zhang WH, Cai Y, Kennelley ED (2001) A fern that hyperaccumulates arsenic. Nature 409:579 doi: 10.1038/35054664 PubMedCrossRefGoogle Scholar
  30. Milone MT, Sgherri C, Clijsters H, Navari-Izzo F (2003) Antioxidative responses of wheat treated with realistic concentration of cadmium. Environ Exp Bot 50:265–276 doi: 10.1016/S0098-8472(03)00037-6 CrossRefGoogle Scholar
  31. Patel MJ, Patel JN, Subramanian RB (2005) Effect of cadmium on growth and the activity of H2O2 scavenging enzymes in Colocassia esculentum. Plant Soil 273:183–188 doi: 10.1007/s11104-004-7402-3 CrossRefGoogle Scholar
  32. Pereira GJG, Molina SMG, Lea PJ, Azevedo RA (2002) Activity of antioxidant enzymes in response to cadmium in Crotalaria juncea. Plant Soil 239:123–132 doi: 10.1023/A:1014951524286 CrossRefGoogle Scholar
  33. Ragaini RC, Ralston HR, Roberts N (1977) Environmental trace metal contamination in Kellogg, Idaho, near a lead smelting complex. Environ Sci Technol 11:773–781 doi: 10.1021/es60131a004 CrossRefGoogle Scholar
  34. Reeves RD, Baker AJM (2000) Metal-accumulating plants. In: Raskin I (Ed), Phytoremediation of Toxic Metals: Using Plants to Clean Up the Environment. John Wiley & Sons, Inc, pp 193–229Google Scholar
  35. Smith IK, Vierheller TL, Thorne CA (1989) Properties and functions of glutathione reductase in plants. Physiol Plant 77:449–456 doi: 10.1111/j.1399-3054.1989.tb05666.x CrossRefGoogle Scholar
  36. Smith KS, Huyck HLO (1999) An overview of the abundance, relative mobility, bioavailability, and human toxicity of metals. In: Plumlee GS, Logsdon MJ (eds) The environmental geochemistry of mineral deposits, Part A: Society of Economic Geologists. Rev Econ Geol 6A, 29–70Google Scholar
  37. Srivastava A, Jaiswal V (1990) Biochemical changes in duck weed after cadmium treatment. Enhancement in senescence. Water Air Soil Pollut 50:163–170 doi: 10.1007/BF00284790 Google Scholar
  38. Srivastava M, Ma LQ, Singh N, Singh S (2005) Antioxidant responses of hyper-accumulator and sensitive fern species to arsenic. J Exp Bot 56:1335–1342 doi: 10.1093/jxb/eri134 PubMedCrossRefGoogle Scholar
  39. Stemmer KL (1976) Pharmacology and toxicology of heavy metals: antimony. Pharmacol Ther A 1:157–160Google Scholar
  40. Shotyk W, Krachler M, Chen B (2005) Antimony: global environmental contaminant. J Environ Monit 7:1135–1136 doi: 10.1039/b515468p PubMedCrossRefGoogle Scholar
  41. Thompson JE, Legge RL, Barber RF (1987) The Role Of Free Radicals In Senescence And Wounding. New Phytol 105:317–344 doi: 10.1111/j.1469-8137.1987.tb00871.x CrossRefGoogle Scholar
  42. Tirmenstein MA, Mathias PI, Snawder JE, Wey HE, Toraason M (1997) Antimony-induced alterations in thiol homeostasis and adenine nucleotide status in cultured cardiac myocytes. Toxicol 119:203–211 doi: 10.1016/S0300-483X(97)03628-7 CrossRefGoogle Scholar
  43. Tirmenstein MA, Plews PI, Walker CV, Woolery MD, Wey HE, Toraason MA (1995) Antimony-Induced Oxidative Stress and Toxicity in Cultured Cardiac Myocytes. Toxicol Appl Pharmacol 130:41–47 doi: 10.1006/taap.1995.1006 PubMedCrossRefGoogle Scholar
  44. USEPA (1979) Water related fate of the 129 priority pollutants, vol. 1. USEPA, Washington DC, USA EP-440/4-79-029AGoogle Scholar
  45. Wang HB, Wong MH, Lan CY, Baker AJM, Qin YR, Shu WS et al (2007) Uptake and accumulation of arsenic by 11 Pteris taxa from southern China. Environ Pollut 145:225–233 doi: 10.1016/j.envpol.2006.03.015 PubMedCrossRefGoogle Scholar
  46. Wei CY, Chen TB (2006) Arsenic accumulation by two brake ferns growing on an arsenic mine and their potential in phytoremediation. Chemosphere 63:1048–1053 doi: 10.1016/j.chemosphere.2005.09.061 PubMedCrossRefGoogle Scholar
  47. Wei CY, Sun X, Wang C, Wang WY (2006) Factors influencing arsenic accumulation by Pteris vittata: A comparative field study at two sites. Environ Pollut 141:488–493 doi: 10.1016/j.envpol.2005.08.060 PubMedCrossRefGoogle Scholar
  48. Wilson NJ, Craw D, Hunter K (2004) Antimony distribution and environmental mobility at an historic antimony smelter site, New Zealand. Environ Pollut 129:257–266 doi: 10.1016/j.envpol.2003.10.014 PubMedCrossRefGoogle Scholar
  49. Wyllie S, Fairlamb AH (2006) Differential toxicity of antimonial compounds and their effects on glutathione homeostasis in a human leukaemia monocyte cell line. Biochem Pharmacol 71:257–267 doi: 10.1016/j.bcp.2005.10.043 PubMedCrossRefGoogle Scholar
  50. Zhao FJ, Dunham SJ, McGrath SP (2002) Arsenic hyperaccumulation by different fern species. New Phytol 156:27–31 doi: 10.1046/j.1469-8137.2002.00493.x CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Renwei Feng
    • 1
    • 2
  • Chaoyang Wei
    • 1
  • Shuxin Tu
    • 2
  • Fengchang Wu
    • 3
  • Linsheng Yang
    • 1
  1. 1.Institute of Geographic Sciences and Natural Resources ResearchChinese Academy of SciencesBeijingChina
  2. 2.College of Resources and EnvironmentHuazhong Agricultural UniversityWuhanChina
  3. 3.Chinese Research Academy of Environmental SciencesBeijingChina

Personalised recommendations