Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation

Abstract

High concentrations of heavy metals (HM) in the soil have detrimental effects on ecosystems and are a risk to human health as they can enter the food chain via agricultural products or contaminated drinking water. Phytoremediation, a sustainable and inexpensive technology based on the removal of pollutants from the environment by plants, is becoming an increasingly important objective in plant research. However, as phytoremediation is a slow process, improvement of efficiency and thus increased stabilization or removal of HMs from soils is an important goal. Arbuscular mycorrhizal (AM) fungi provide an attractive system to advance plant-based environmental clean-up. During symbiotic interaction the hyphal network functionally extends the root system of their hosts. Thus, plants in symbiosis with AM fungi have the potential to take up HM from an enlarged soil volume. In this review, we summarize current knowledge about the contribution of the AM symbiosis to phytoremediation of heavy metals.

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Abbreviations

AM:

Arbuscular mycorrhizal

HM:

Heavy metals

EC50 :

Effective concentration reducing germination or hyphal growth to 50%

References

  1. Benedetto A, Magurno F, Bonfante P, Lanfranco L (2005) Expression profiles of a phosphate transporter gene (GmosPT) from the endomycorrhizal fungus Glomus mosseae. Mycorrhiza 15:1–8

    Article  CAS  Google Scholar 

  2. Briat J-F, Lobreaux S (1997) Iron transport and storage in plants. Trends Plant Sci 2:187–193

    Article  Google Scholar 

  3. Burleigh SH, Kristensen BK, Bechmann IE (2003) A plasma membrane zinc transporter from Medicago truncatula is up-regulated in roots by Zn fertilization, yet down-regulated by arbuscular mycorrhizal colonization. Plant Mol Biol 52:1077–1088

    PubMed  Article  CAS  Google Scholar 

  4. Chen B, Christie P, Li X (2001) A modified glass bead compartment cultivation system for studies on nutrient and trace metal uptake by arbuscular mycorrhiza. Chemosphere 42:185–192

    PubMed  Article  CAS  Google Scholar 

  5. Chen BD, Li XL, Tao HQ, Christie P, Wong MH (2003) The role of arbuscular mycorrhiza in zinc uptake by red clover growing in a calcareous soil spiked with various quantities of zinc. Chemosphere 50:839–846

    PubMed  Article  CAS  Google Scholar 

  6. Chen X, Wu C, Tang J, Hu S (2005) Arbuscular mycorrhizae enhance metal lead uptake and growth of host plants under a sand culture experiment. Chemosphere 60:665–671

    PubMed  Article  CAS  Google Scholar 

  7. Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486

    PubMed  Article  CAS  Google Scholar 

  8. Clemens S, Bloss T, Vess C, Neumann D, Nies DH, zur Nieden U (2002) A transporter in the endoplasmic reticulum of schizosaccharomyces pombe cells mediates zinc storage and differentially affects transition metal tolerance. J Biol Chem 277:18215–18221

    PubMed  Article  CAS  Google Scholar 

  9. Del Val C, Barea JM, Azcon-Aguilar C (1999) Diversity of arbuscular mycorrhizal fungus populations in heavy-metal-contaminated soils. Appl Environ Microbiol 65:718–723

    PubMed  CAS  Google Scholar 

  10. Dhankher OP, Li Y, Rosen BP, Shi J, Salt D, Senecoff JF, Sashti NA, Meagher RB (2002) Engineering tolerance and hyperaccumulation of arsenic in plants by combining arsenate reductase and gamma-glutamylcysteine synthetase expression. Nat Biotechnol 20:1140–1145

    PubMed  Article  CAS  Google Scholar 

  11. Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97–112

    PubMed  Article  CAS  Google Scholar 

  12. Gaur A, Adholeya A (2004) Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Current Sci 86:528–534

    CAS  Google Scholar 

  13. Glassop D, Smith SE, Smith FW (2005) Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222(4):688–698

    PubMed  Article  CAS  Google Scholar 

  14. Gonzalez-Chavez MC, Carrillo-Gonzalez R, Wright SF, Nichols KA (2004) The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environ Pollut 130:317–323

    PubMed  Article  CAS  Google Scholar 

  15. Gonzalez-Guerrero M, Azcon-Aguilar C, Mooney M, Valderas A, MacDiarmid CW, Eide DJ, Ferrol N (2005) Characterization of a Glomus intraradices gene encoding a putative Zn transporter of the cation diffusion facilitator family. Fungal Genet Biol 42:130–140

    PubMed  Article  CAS  Google Scholar 

  16. Gravot A, Lieutaud A, Verret F, Auroy P, Vavasseur A, Richaud P (2004) AtHMA3, a plant P1B- ATPase, functions as a Cd/Pb transporter in yeast. FEBS Lett 561:22–28

    PubMed  Article  CAS  Google Scholar 

  17. Grcman H, Vodnik D, Velikonja-Bolta S, Lestan D (2003) Ethylenediaminedissuccinate as a new chelate for environmentally safe enhanced lead phytoextraction. J Environ Qual 32:500–506

    PubMed  CAS  Article  Google Scholar 

  18. Guerinot ML (2000) The ZIP family of metal transporters. Biochim Biophys Acta 1465:190–198

    PubMed  Article  CAS  Google Scholar 

  19. Guo Y, George E, Marschner H (1996) Contribution of an arbuscular mycorrhizal fungus to the uptake of cadmium and nickel in bean and maize plants. Plant Soil 184:195–205

    Article  CAS  Google Scholar 

  20. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    PubMed  Article  CAS  Google Scholar 

  21. Hall JL, Williams LE (2003) Transition metal transporters in plants. J Exp Bot 54:2601–2613

    PubMed  Article  CAS  Google Scholar 

  22. Harrison MJ (1999) Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annu Rev Plant Physiol Plant Mol Biol 50:361–389

    PubMed  Article  CAS  Google Scholar 

  23. Harrison MJ, van Buuren ML (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626–629

    PubMed  Article  CAS  Google Scholar 

  24. Harrison MJ, Dewbre GR, Liu J (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:2413–2429

    PubMed  Article  CAS  Google Scholar 

  25. Hildebrandt U, Kaldorf M, Bothe H (1999) The zinc violet and its colonization by arbuscular mycorrhizal fungi. J Plant Physiol 154:709–717

    CAS  Google Scholar 

  26. Himelblau E, Amasino RM (2000) Delivering copper within plant cells. Curr Opin Plant Biol 3:205–210

    PubMed  CAS  Google Scholar 

  27. Hirayama T, Kieber JJ, Hirayama N, Kogan M, Guzman P, Nourizadeh S, Alonso JM, Dailey WP, Dancis A, Ecker JR (1999) Responsive-to-antagonist1, a Menkes/Wilson disease- related copper transporter, is required for ethylene signaling in Arabidopsis. Cell 97:383–393

    PubMed  Article  CAS  Google Scholar 

  28. Holleman A, Wiberg E (1985) Lehrbuch der Anorganischen Chemie. Berlin

  29. Hutchinson JJ, Young SD, Black CR, West HM (2004) Determining uptake of radio-labile soil cadmium by arbuscular mycorrhizal hyphae using isotopic dilution in a compartmented-pot system. New Phytol 164:477–484

    Article  CAS  Google Scholar 

  30. Jacquot-Plumey E, van Tuinen D, Chatagnier O, Gianinazzi S, Gianinazzi-Pearson V (2001) 25S rDNA-based molecular monitoring of glomalean fungi in sewage sludge-treated field plots. Environ Microbiol 3:525–531

    PubMed  Article  CAS  Google Scholar 

  31. Janouskova M, Pavlikova D, Macek T, Vosatka M (2005) Arbuscular mycorrhiza decreases cadmium phytoextraction by transgenic tobacco with inserted metallothionein. Plant Soil 272:29–40

    Article  CAS  Google Scholar 

  32. Jarup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182

    PubMed  Article  Google Scholar 

  33. Joner EJ, Briones R, Leyval C (2000) Metal-binding capacity of arbuscular mycorrhizal mycelium. Plant Soil 226:227–234

    Article  CAS  Google Scholar 

  34. Kaldorf M, Kuhn AJ, Schröder WH, Hildebrandt U, Bothe H (1999) Selective element deposits in maize colonized by a heavy metal tolerance conferring arbuscular mycorrhizal fungus. J Plant Physiol 154:718–728

    CAS  Google Scholar 

  35. Khan AG (2005) Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. J Trace Elem Med Biol 18:355–364

    PubMed  Article  CAS  Google Scholar 

  36. Krämer U (2005) Phytoremediation: novel approaches to cleaning up polluted soils. Curr Opin Biotechnol 16:133–141

    PubMed  Article  CAS  Google Scholar 

  37. Lanfranco L, Bolchi A, Ros EC, Ottonello S, Bonfante P (2002) Differential expression of a metallothionein gene during the presymbiotic versus the symbiotic phase of an arbuscular mycorrhizal fungus. Plant Physiol 130:58–67

    PubMed  Article  CAS  Google Scholar 

  38. Lanfranco L, Novero M, Bonfante P (2005) The mycorrhizal fungus Gigaspora margarita possesses a CuZn superoxide dismutase that is up-regulated during symbiosis with legume hosts. Plant Physiol 137:1319–1330

    PubMed  Article  CAS  Google Scholar 

  39. Leung HM, Ye ZH, Wong MH (2006) Interactions of mycorrhizal fungi with Pteris vittata (as hyperaccumulator) in as-contaminated soils. Environ Pollut 139:1–8

    PubMed  Article  CAS  Google Scholar 

  40. Liu Y, Zhu YG, Chen BD, Christie P, Li XL (2005) Yield and arsenate uptake of arbuscular mycorrhizal tomato colonized by Glomus mosseae BEG167 in as spiked soil under glasshouse conditions. Environ Int 31:867–873

    PubMed  Article  CAS  Google Scholar 

  41. Maldonado-Mendoza IE, Dewbre GR, Harrison MJ (2001) A phosphate transporter gene from the extra-radical mycelium of an arbuscular mycorrhizal fungus Glomus intraradices is regulated in response to phosphate in the environment. Mol Plant Microbe Interact 14:1140–1148

    PubMed  Article  CAS  Google Scholar 

  42. McGrath SP, Zhao FJ (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opin Biotechnol 14:277–282

    PubMed  Article  CAS  Google Scholar 

  43. Medina A, Vassilev N, Barea JM, Azcon R (2005) Application of Aspergillus niger-treated agrowaste residue and Glomus mosseae for improving growth and nutrition of Trifolium repens in a Cd- contaminated soil. J Biotechnol 116:369–378

    PubMed  Article  CAS  Google Scholar 

  44. Meharg A, Macnair M (1994) Relationship between plant phosphorus status and the kinetics of arsenate influx in clones of Deschamsia caespitosa (L.) Beauv. that differ in their tolerance of arsenate. Plant Soil 162:99–106

    Article  CAS  Google Scholar 

  45. Mertz W (1981) The essential trace elements. Science 213:1332–1338

    PubMed  Article  CAS  Google Scholar 

  46. Nagy R, Karandashov V, Chague V, Kalinkevich K, Tamasloukht M, Xu G, Jakobsen I, Levy AA, Amrhein N, Bucher M (2005) The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant J 42:236–250

    PubMed  Article  CAS  Google Scholar 

  47. Natvig D, Sylvester K, Dvorachek W, Baldwin J (1996) Superoxide dismutases and catalases. In: Marzluf G (ed) The micota III biochemistry and molecular biology. Springer, Berlin Heidelberg New York, pp 191–209

    Google Scholar 

  48. Ouziad F, Hildebrandt U, Schmelzer E, Bothe H (2005) Differential gene expressions in arbuscular mycorrhizal-colonized tomato grown under heavy metal stress. J Plant Physiol 162:634–649

    PubMed  Article  CAS  Google Scholar 

  49. Parádi I, Berecz B, Halász K, Bratek Z (2003) Influence of arbuscular mycorrhiza and cadmium on the polyamine contents of Ri T-DNA transformed Daucus carota L. root cultures. Acta Biologica Szegediensis 47:31–36

    Google Scholar 

  50. Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 99:13324–13329

    PubMed  Article  CAS  Google Scholar 

  51. Pawlowska TE, Charvat I (2004) Heavy-metal stress and developmental patterns of arbuscular mycorrhizal fungi. Appl Environ Microbiol 70:6643–6649

    PubMed  Article  CAS  Google Scholar 

  52. Peuke AD, Rennenberg H (2005) Phytoremediation. EMBO Rep 6:497–501

    PubMed  Article  CAS  Google Scholar 

  53. Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414:462–470

    PubMed  Article  CAS  Google Scholar 

  54. Rivera-Becerril F, Calantzis C, Turnau K, Caussanel J-P, Belimov AA, Gianinazzi S, Strasser RJ, Gianinazzi-Pearson V (2002) Cadmium accumulation and buffering of cadmium-induced stress by arbuscular mycorrhiza in three Pisum sativum L. genotypes. J Exp Bot 53:1177–1185

    PubMed  Article  CAS  Google Scholar 

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Acknowledgements

We apologize to all those researchers whose work we overlooked or could not include because of page limitations. We are grateful to Patrick King for critical reading of the manuscript.

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Correspondence to Uta Paszkowski.

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Göhre, V., Paszkowski, U. Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223, 1115–1122 (2006). https://doi.org/10.1007/s00425-006-0225-0

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Keywords

  • Arbuscular mycorrhizal symbiosis
  • Glomus
  • Heavy metal
  • Phytoremediation