1887

Abstract

Cadmium uptake and subcellular compartmentation in the ectomycorrhizal fungus were investigated using radiotracer flux analyses. Concentration-dependent Cd-uptake kinetics were characterized by a smooth, non-saturating curve that could be dissected into linear and saturable components. The linear-uptake kinetic component was interpreted as representing binding of Cd to apoplastic components, whereas the remaining saturable component was the result of carrier-mediated transport across the plasma membrane. Cell-wall-bound Cd was almost completely removed during desorption from cell-wall preparations. Cd desorption from intact mycelium was found to be a function of time involving three compartments corresponding in series to cell wall (50%), cytoplasm (30%) and vacuole (20%), when mycelia were exposed to a 005 μM Cd concentration. At 4 °C, most of the Cd recovered was due to the cell-wall-bound fraction, suggesting that transport across the plasma membrane is a metabolically mediated process. Carbonyl cyanide chlorophenylhydrazone (CCCP) inhibited Cd accumulation in mycelia by up to 28%, which indicates that transport of Cd was partially dependent on the membrane potential. Cd uptake into symplasm is linked to Ca transport, as revealed by the inhibition of Cd accumulation by the Ca ionophore A23187. The present work demonstrates the ability of the ectomycorrhizal fungus to take up and further accumulate Cd in different compartments. Binding of Cd onto cell walls and accumulation of Cd in the vacuolar compartment may be regarded as two essential metal-detoxification mechanisms. These data represent a first step towards the understanding of metal-tolerance mechanisms in mycorrhizal fungi.

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2000-05-01
2020-09-30
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References

  1. Borst-Pauwels G. W. F. H.. 1981; Ion transport in yeast. Biochim Biophys Acta650:88–127[CrossRef]
    [Google Scholar]
  2. Brady D., Duncan J. R.. 1994; Binding of heavy metals by the cell walls of Saccharomyces cerevisiae. Enzyme Microb Technol16:633–638[CrossRef]
    [Google Scholar]
  3. Burgstaller W.. 1997; Transport of small ions and molecules through the plasma membrane of filamentous fungi. Crit Rev Microbiol23:1–46[CrossRef]
    [Google Scholar]
  4. Cataldo D. A., Garland T. R., Wildung R. E.. 1983; Cadmium uptake kinetics in intact soybean plants. Plant Physiol73:844–848[CrossRef]
    [Google Scholar]
  5. Chalot M., Brun A., Botton B., Söderström B.. 1996; Kinetics, energetics and specificity of a general amino acid transporter from the ectomycorrhizal fungus Paxillus involutus. Microbiology142:1749–1756[CrossRef]
    [Google Scholar]
  6. Clemens S., Antosiewicz D. M., Ward J. M., Schachtman D. P., Schroeder J. I.. 1998; The plant cDNA LCT1 mediates the uptake of calcium and cadmium in yeast. Proc Natl Acad Sci USA95:12043–12048[CrossRef]
    [Google Scholar]
  7. Colpaert J. V., Van Assche J. A.. 1993; The effects of cadmium on ectomycorrhizal Pinus sylvestris L. New Phytol123:325–333[CrossRef]
    [Google Scholar]
  8. Costa G., Morel J. L.. 1993; Cadmium uptake by Lupinus albus (L.): cadmium excretion, a possible mechanism of cadmium tolerance. J Plant Nutr16:1921–1929[CrossRef]
    [Google Scholar]
  9. Cutler J. M., Rains D. W.. 1974; Characterization of cadmium uptake by plant tissue. Plant Physiol54:67–71[CrossRef]
    [Google Scholar]
  10. Dixon R. K., Buschena C. A.. 1988; Response of ectomycorrhizal Pinus banksiana and Picea glauca to heavy metals in soil. Plant Soil105:265–271[CrossRef]
    [Google Scholar]
  11. Fuhrmann R., Rothstein A.. 1968; The transport of Zn2+, Co2+ and Ni2+ into yeast cells. Biochim Biophys Acta163:325–330[CrossRef]
    [Google Scholar]
  12. Gadd G. M.. 1993; Tansley review no. 47: interactions of fungi with toxic metals. New Phytol124:25–60[CrossRef]
    [Google Scholar]
  13. Gadd G. M., White C.. 1989; Heavy metal and radionuclide accumulation and toxicity in fungi and yeasts. In Metal–Microbe Interactions pp.19–38Edited by Poole R. K., Gadd G. M.. Oxford: IRL Press;
    [Google Scholar]
  14. Galli U., Schuepp H., Brunold C.. 1994; Heavy metal binding by mycorrhizal fungi. Physiol Plant92:364–368[CrossRef]
    [Google Scholar]
  15. Godbold D. L.. 1991; Cadmium uptake in Norway spruce (Picea abies [L.] Karst.) seedlings. Tree Physiol9:349–357[CrossRef]
    [Google Scholar]
  16. Gruhn C. M., Miller O. K.. 1991; Effect of copper on tyrosinase activity and polyamine content of some ectomycorrhizal fungi. Mycol Res95:268–272[CrossRef]
    [Google Scholar]
  17. Hardiman R. T., Jacoby B.. 1984; Absorption and translocation of Cd in bush beans (Phaseolus vulgaris). Physiol Plant61:670–674[CrossRef]
    [Google Scholar]
  18. Hart J. J., Welch R. M., Norvell W. A., Sullivan L. A., Kochian L. V.. 1998; Characterization of cadmium binding, uptake, and translocation in intact seedlings of bread and durum wheat cultivars. Plant Physiol116:1413–1420[CrossRef]
    [Google Scholar]
  19. Homma Y., Hirata H.. 1984; Kinetics of cadmium and zinc absorption by rice seedling roots. Soil Sci Plant Nutr30:527–532[CrossRef]
    [Google Scholar]
  20. Jones M. D., Hutchinson T. C.. 1986; The effect of mycorrhizal infection on the response of Betula papyrifera to nickel and copper. New Phytol102:429–442[CrossRef]
    [Google Scholar]
  21. Kochian L. V., Lucas W. J.. 1982; Potassium transport in corn roots. I. Resolution of kinetics into a saturable and linear component. Plant Physiol70:1723–1731[CrossRef]
    [Google Scholar]
  22. Kwan K. H. M., Smith S.. 1991; Some aspects of the kinetics of cadmium and thallium uptake by fronds of Lemna minor L. New Phytol117:91–102[CrossRef]
    [Google Scholar]
  23. Lagerwerff J. V.. 1971; Uptake of cadmium, lead and zinc by radish from soil and air. Soil Sci111:129–133[CrossRef]
    [Google Scholar]
  24. Lasat M. M., Baker A. J. M., Kochian L. V.. 1998; Altered Zn compartmentation in the root symplasm and stimulated Zn absorption into the leaf as mechanisms involved in Zn hyperaccumulation in Thlaspi caerulescens. Plant Physiol118:875–883[CrossRef]
    [Google Scholar]
  25. Leyval C., Turnau K., Haselwandter K.. 1997; Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza7:139–153[CrossRef]
    [Google Scholar]
  26. Macklon A. E. S., Sim A.. 1987; Cellular cobalt fluxes in roots and transport to the shoots of wheat seedlings. J Exp Bot38:1663–1677[CrossRef]
    [Google Scholar]
  27. Macklon A. E. S., Lumsdon D. G., Sim A., McHardy W. J.. 1996; Phosphate fluxes, compartmentation and vacuolar speciation in root cortex cells of intact Agrostis capillaris seedlings: effects of non-toxic levels of aluminium. J Exp Bot47:793–803[CrossRef]
    [Google Scholar]
  28. Marschner H.. 1995; Mineral Nutrition of Higher Plants, 2nd edn. Boston, MA: Academic Press;
    [Google Scholar]
  29. Miller J. E., Hasset J. J., Koeppe D. E.. 1976; Uptake of cadmium by soybean as influenced by soil cation exchange capacity, pH and available phosphorus. J Environ Qual5:157–160
    [Google Scholar]
  30. Mullins G. L., Sommers L. E.. 1986; Cadmium and zinc influx characteristics by intact corn (Zea mays L.) seedlings. Plant Soil96:153–164[CrossRef]
    [Google Scholar]
  31. Norris P. R., Kelly D. P.. 1977; Accumulation of cadmium and cobalt by Saccharomyces cerevisiae. J Gen Microbiol99:317–324[CrossRef]
    [Google Scholar]
  32. Okorokov L. A.. 1985; Main mechanisms of ion transport and regulation of ion concentrations in the yeast cytoplasm. In Environmental Regulation of Microbial Metabolism pp.339–349Edited by Kulaev I. S., Dawes E. A., Tempest D. W.. London: Academic Press;
    [Google Scholar]
  33. Ortiz D. F., Kreppel L., Speiser D. M., McDonald G., Ow D. W.. 1992; Heavy metal tolerance in the fission yeast requires an ATP-binding cassette-type vacuolar membrane transporter. EMBO J11:3491–3499
    [Google Scholar]
  34. Ortiz D. F., Ruscitti T., McCue K. F., Ow D. W.. 1995; Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. J Biol Chem270:4721–4728[CrossRef]
    [Google Scholar]
  35. Rauser W. E.. 1987; Compartmental efflux analysis and removal of extracellular cadmium from roots. Plant Physiol85:62–65[CrossRef]
    [Google Scholar]
  36. Rauser W. E.. 1995; Phytochelatins and related peptides: structure, biosynthesis, and function. Plant Physiol109:1141–1149[CrossRef]
    [Google Scholar]
  37. Thornton B.. 1991; Indirect compartmental analysis of copper in live ryegrass roots: comparison with model systems. J Exp Bot42:183–188[CrossRef]
    [Google Scholar]
  38. Ting Y. P., Teo W. K.. 1994; Uptake of cadmium and zinc by yeast: effects of co-metal ion and physical-chemical treatments. Bioresour Technol50:113–117[CrossRef]
    [Google Scholar]
  39. Tripathi R. D., Rai U. N., Gupta M., Yunus M., Chandra P.. 1995; Cadmium transport in submerged macrophyte Ceratophyllum demersum L. in presence of various metabolic inhibitors and calcium channel blockers. Chemosphere31:3783–3791[CrossRef]
    [Google Scholar]
  40. Turnau K., Kottke I., Dexheimer J., Botton B.. 1994; Element distribution in mycelium of Pisolithus arrhizus treated with cadmium dust. Ann Bot74:137–142[CrossRef]
    [Google Scholar]
  41. White C., Gadd G. M.. 1987; The uptake and cellular distribution of zinc in Saccharomyces cerevisiae. J Gen Microbiol133:727–737
    [Google Scholar]
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