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Role of Arbuscular Mycorrhizal (AM) Fungi in Phytoremediation of Soils Contaminated: A Review
Document Type : Original Article
Author
Department of Plant Ecophysiology, Faculty of Agriculture, University of Tabriz, Iran
Abstract
Pollution of the soil environment with toxic materials from fossil burning, mining and smelting of metalliferous ores, disposal of sewage, fertilizers and pesticides, etc. has increased dramatically since the onset of industrial revolution. Application of plants with ability of absorbing heavy metals is a low-cost alternative for eliminating soils from heavy metals. Phytoremediation uses plants to remove pollutants from the environment. Arbuscular mycorrhizal Fungi provide an attractive system to advance plant based environmental clean-up. AM associations are integral functioning parts of plant roots and are widely recognized as enhancing plant growth on severely disturbed sites, including those contaminated with heavy metals. This review highlights the potential of AM fungi for enhancing phytoremediation of heavy metal contaminated soils.
Keywords
Ahiabor, B.D., & Hirata, H. (1995). Influence of growth stage on the association between some tropical legumes and two variant species of Glomus in an Andosol. Soil Science and Plant Nutrition. 41: 481-496.
Alloway, B.J. (1990). Heavy metal in soils. New York: John Wiley and Sons, Inc. Babula, P., Adam, V., Apatrilova, R., Zehnalek, J., Havel, L., & Kizek, R. (2008). Uncommon heavy metals, metalloids and their plant toxicity. Environmental Chemistry Letters. 6: 189-213.
Chandreshekara, C.P., Patil, V.C., & Sreenivasa, M.N. (1995). VA-mycorrhiza mediated P effect on growth and yield of sunflower (Helianthus annus L.) at different P levels. Plant and Soil. 176:325-328.
Chaudhry, T.M., Hayes, W.J., Khan, A.G., & Khoo, C.S. (1998). Phytoremediation - focusing on accumulator plants that remediate metal contaminated soils. Australasian Journal of Ecotoxicology. 4: 37-51.
Chen, B., Shen, H., Li, X., Feng, G., & Christie, P. (2004). Effects of EDTA application and arbuscular mycorrhizal colonization on growth and zinc uptake by maize (Zea mays L.) in soil experimentally contaminated with zinc. Plant and Soil. 261: 219-229.
Chen, B., Jakobsen, I., Roos, P., Borggaard, O.K., & Zhu, Y.G. (2005). Mycorrhiza and root hairs enhance acquisition of phosphorus and uranium from phosphate rock but mycorrhiza decreases root to shoot uranium transfer. New Phytologist. 165: 591-598.
Christie, P., Li, X., & Chen, B. (2004). Arbuscular mycorrhiza can depress translocation of zinc to shoots of host plants in soils moderately polluted with zinc. Plant and Soil. 261: 209-217.
Clark, R.B., & Zeto, S.K. (2000). Mineral Acquisition by Arbuscular Mycorrhizal Plants. Journal of Plant Nutrition. 23: 867-902.
Cui, M., & Nobel, P.S. (2006). Nutrient status, water uptake and gas exchange for three desert succulents infected with mycorrhizal fungi. New Phytologist. 122: 643-649.
Del Val, C., Barea, J.M., & Azcon-Aguilar, C. (1999). Assessing the Tolerance of Heavy Metals of Arbuscular Mycorrhizal Fungi isolated Sewage Sludge Contaminated Soils. Applied Soil Ecology. 11: 261-269.
EPA. (2000). Introduction to phytoremediation, US Environmental Protection Agency, Cincinnati, 72 p.
Flathman, P.E., & Lanza, G.R. (1998). Phytoremediation: Current views on an emerging green technology. Journal of Soil Contamination. 7(4): 415-432.
Gadd, G.M. (1993). Interactions of fungi with toxic metals. New Phytologist. 124: 25-60.
Galli, U., Schuepp, H., & Brunold, C. (1994). Heavy metal binding by mycorrhizal fungi. Physiologia Plantarum. 92: 364-368.
Gao, Y., Cheng, Z., Ling, W., & Huang, J. (2010). Arbuscular mycorrhizal fungal hyphae contribute to the uptake of polycyclic aromatic hydrocarbons by plant roots. Bioresource Technology. 101:6895-6901.
George, E., Häussler, K.U., Vetterlein, D., Gorgus, E., & Marschner, H. (1992). Water and nutrient translocation by hyphae of Glomus mosseae. Canadian Journal of Botany. 70: 2130-2137.
Gildon, A., & Tinker, P.B. (1983). Interactions of vesicular-arbuscular mycorrhizal infection and heavy metals in plants. I. The effects of heavy metals on the development of vesicular-arbuscular mycorrhizas. New Phytologist. 95: 247-261.
Gonzalez-Chavez, C., D’Haen, J., Vangronsveld, J., & Dodd, J.C. (2002). Copper soprtion and accumulation by the extraradical mycelium of different Glomus spp (Arbuscular mycorrhizal fungi) isolated from the same polluted soil. Plant and Soil. 240(2): 287-297.
Guo, Y., George, E., & Marschner, H. (1996). Contribution of an arbuscular mycorrhizal fungus to uptake of Cadmnium and Nickel in bean by maize plants. Plant and Soil. 184: 195-205.
Harley, J.L., & Smith, S.E. (1983). Mycorrhizal symbiosis. Academic Press, London UK, 483 p.
Hildebrandt, U., Kaldorf, M., & Bothe, H. (1999). The zinc violet and its colonization by arbuscular mycorrhizal fungi. Journal of Plant Physiology. 154: 709-717. Jamal, A., Ayub, N., Usman, M., & Khan, A.G. (2002). Arbuscular Mycorrhizal Fungi Enhance Zinc and Nickel Uptake from Contaminated Soil by Soybean and Lentil. International Journal of
Phytoremediation. 4(3): 205-221.
Jasper, D.A., Abbott, L.K., & Robson, A.D. (1989). Hyphae of a vesicular-arbuscular mycorrhizal fungus maintain infectivity in dry soil, except when the soil is disturbed. New Phytologist. 112:101-107.
Khan, A.G., Kuek, C., Chaudhry, T.M., Khoo, C.S., & Hayes, W.J. (2000). Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere. 41(1): 197-207.
Kling, J. (1997). Phytoremediation of organics moving rapidly into field trials. Environmental Science and Technology. 31(3): 129A.
Kumar, P.B.A.N., Dushenkov, V., Motto, H., & Raskin, I. (1995). Phytoextraction - the use of plants to remove heavy metals from soils. Environmental Science and Technology. 29: 1232-1238.
Leyval, C., Tumau, K., & Haselwandter, K. (1997). Interactions between Heavy Metals and Mycorrhizal Fungi in Polluted Soils: Physiological, Ecological and Applied Aspects. Mycorrhiza. 7: 139-153.
Leyval, C., Joner, E.J., del Val, C., & Haselwandter, K. (2002). Potential of arbuscular mycorrhizal fungi for bioremediation. Mycorrhizal technology in agriculture. Pp: 175-186.
Liu, A., Hamel, C., Elmi, A., Costa, C., Ma, B., & Smith, D.L. (2002). Concentrations of K, Ca and Mg in maize colonised by arbuscular mycorrhizal fungi under field conditions. Canadian Journal of Soil Science. 82(3): 271-278.
Marschner, H. (1995). Mineral Nutrition of Higher Plants (2nd Edn). Academic Press, London. 889 p.
Memon, A.R., Aktoprakligil, D., Ozdemir, A., & Vertill, A. (2001) Heavy metal accumulation and detoxification mechanisms in plants. Turkish Journal of Botany. 25: 111-121.
Michelsen, A., Schmidt, I.K., Jonasson, S., Quarmby, C., & Sleep, D. (1996). Leaf 15N abundance of subarctic plants provides field evidence that ericoid, ectomycorrhizal and non- and arbuscular
mycorrhizal species access different sources of soil nitrogen. Oecologia. 105: 53-63.
Michelsen, A., Quarmby, C., Sleep, D., & Jonasson, S. (1998). Vascular plant N-15 natural abundance in heath and forest tundra ecosystems is closely correlated with presence and type of mycorrhizal fungi in roots. Oecologia. 115: 406-418.
Nadian, H., Smith, S.E., Alston, A.M., & Murray, R.S. (1997). Effects of soil compaction on plant growth, phosphorus uptake and morphological characteristics of vesiculararbuscular mycorrhizal colonization of Trifolium subterraneum. New Phytologist. 135(2): 303-311.
Noyd, R.K., Pfleger, F.L., & Norland, M.R. (1996). Field responses to added organic matter, arbuscular mycorrhizal fungi, and fertilizer in reclamation of torbonite iron ore tailing. Plant and Soil. 179: 89-97.
Nriagu, J.O. (1979). Global inventory of natural and anthropogenic emissions of trace metals to the atmosphere. Nature. 279: 409-411.
Raskin Ilya, & Ensley Burt, D. (2000). Phytoremediation of toxic metals: using plants to clean up the environment, New York: John Wiley. 304 p.
Rosén, K., Weiliang, Z., & Mårtensson, A. (2005). Arbuscular mycorrhizal fungi mediated uptake of Cs in leek and ryegrass. Science of the Total Environment. 338: 283-290.
Rufyikiri, G., Thiry, Y., Wang, L., Delvaux, B., & Declerck, S. (2002). Uranium uptake and translocation by the arbuscular fungus, Glomus intraradices, under root-organ culture conditions. New Phytologist. 156(2): 275-281.
Rufyikiri, G., Declerck, S., & Thiry, Y. (2004). Comparison of 233U and 33P uptake and translocation by the arbuscular mycorrhizal fungus Glomus intraradices in root organ culture conditions. Mycorrhiza. 14:203-207.
Sanjay Kumar, J.H.A., & Kumar, N. (2011). Potential of mycorrhizal fungi in ecosystem: A Review. International Journal of Research in Botany. 1(1): 1-7.
Shetty, K.G., Banks, M.K., Hetrick, B.A., & Schwab, A.P. (1995). Effects of mycorrhizae and fertilizer amendments on zinc tolerance of plants. Environmental Pollution. 88: 307-314.
Singh, O.V., Labana, S., Pandey, G., Budhiraja, R., & Jain, R.K. (2003). Phytoremediation: An overview of metallic ion decontamination from soil. Applied Microbiology and Biotechnology. 61: 405-412.
Smith, S.E., & Read, D.J. (1997). Mycorrhizal symbiosis, Academic Press, San Diego. 605 p. Smith, M.R., Charvat, I., & Jacobson, R.L. (1998). Arbuscular mycorrhizae promote establishment of prairie species in a tallgrass prairie restoration. Canadian Journal of Botany. 76: 1947-1954.
Söderström, B.E. (1979). Seasonal fluctuations of active fungal biomass in horizons of a podzolized pine-forest soil in central Sweden. Soil Biology and Biochemistry. 11:149-154.
Turnau, K. (1998). Heavy metal content and localization in mycorrhizal Euphorbia cyparissias from zinc wastes in Southern Poland. Acta Societatis Botanicorum Poloniae. 67: 105-113.
Weissenhorn, I., & Leyval, C. (1995). Root Colonization of Maize by a Cd-sensitive and a Cdtolerant Glomus mosseae and Cadmium Uptake in Sand Culture. Plant and Soil. 175: 233-238.
Xavier, I.J., Boyetchko, S.M. (2002). Arbuscular Mycorrhizal Fungi as Biostimulants and Bioprotectants of Crops. Applied Mycology and Biotechnology. 2: 311-340.
Yu, Y., Zhanh, S., & Huang, H. (2010). Behaivor of mercury in a soil-plant system as affected by inoculation with the arbuscular mycorrhizal fungus Glomus mosseae. Mycorrhiza. 20: 407-414
Alloway, B.J. (1990). Heavy metal in soils. New York: John Wiley and Sons, Inc. Babula, P., Adam, V., Apatrilova, R., Zehnalek, J., Havel, L., & Kizek, R. (2008). Uncommon heavy metals, metalloids and their plant toxicity. Environmental Chemistry Letters. 6: 189-213.
Chandreshekara, C.P., Patil, V.C., & Sreenivasa, M.N. (1995). VA-mycorrhiza mediated P effect on growth and yield of sunflower (Helianthus annus L.) at different P levels. Plant and Soil. 176:325-328.
Chaudhry, T.M., Hayes, W.J., Khan, A.G., & Khoo, C.S. (1998). Phytoremediation - focusing on accumulator plants that remediate metal contaminated soils. Australasian Journal of Ecotoxicology. 4: 37-51.
Chen, B., Shen, H., Li, X., Feng, G., & Christie, P. (2004). Effects of EDTA application and arbuscular mycorrhizal colonization on growth and zinc uptake by maize (Zea mays L.) in soil experimentally contaminated with zinc. Plant and Soil. 261: 219-229.
Chen, B., Jakobsen, I., Roos, P., Borggaard, O.K., & Zhu, Y.G. (2005). Mycorrhiza and root hairs enhance acquisition of phosphorus and uranium from phosphate rock but mycorrhiza decreases root to shoot uranium transfer. New Phytologist. 165: 591-598.
Christie, P., Li, X., & Chen, B. (2004). Arbuscular mycorrhiza can depress translocation of zinc to shoots of host plants in soils moderately polluted with zinc. Plant and Soil. 261: 209-217.
Clark, R.B., & Zeto, S.K. (2000). Mineral Acquisition by Arbuscular Mycorrhizal Plants. Journal of Plant Nutrition. 23: 867-902.
Cui, M., & Nobel, P.S. (2006). Nutrient status, water uptake and gas exchange for three desert succulents infected with mycorrhizal fungi. New Phytologist. 122: 643-649.
Del Val, C., Barea, J.M., & Azcon-Aguilar, C. (1999). Assessing the Tolerance of Heavy Metals of Arbuscular Mycorrhizal Fungi isolated Sewage Sludge Contaminated Soils. Applied Soil Ecology. 11: 261-269.
EPA. (2000). Introduction to phytoremediation, US Environmental Protection Agency, Cincinnati, 72 p.
Flathman, P.E., & Lanza, G.R. (1998). Phytoremediation: Current views on an emerging green technology. Journal of Soil Contamination. 7(4): 415-432.
Gadd, G.M. (1993). Interactions of fungi with toxic metals. New Phytologist. 124: 25-60.
Galli, U., Schuepp, H., & Brunold, C. (1994). Heavy metal binding by mycorrhizal fungi. Physiologia Plantarum. 92: 364-368.
Gao, Y., Cheng, Z., Ling, W., & Huang, J. (2010). Arbuscular mycorrhizal fungal hyphae contribute to the uptake of polycyclic aromatic hydrocarbons by plant roots. Bioresource Technology. 101:6895-6901.
George, E., Häussler, K.U., Vetterlein, D., Gorgus, E., & Marschner, H. (1992). Water and nutrient translocation by hyphae of Glomus mosseae. Canadian Journal of Botany. 70: 2130-2137.
Gildon, A., & Tinker, P.B. (1983). Interactions of vesicular-arbuscular mycorrhizal infection and heavy metals in plants. I. The effects of heavy metals on the development of vesicular-arbuscular mycorrhizas. New Phytologist. 95: 247-261.
Gonzalez-Chavez, C., D’Haen, J., Vangronsveld, J., & Dodd, J.C. (2002). Copper soprtion and accumulation by the extraradical mycelium of different Glomus spp (Arbuscular mycorrhizal fungi) isolated from the same polluted soil. Plant and Soil. 240(2): 287-297.
Guo, Y., George, E., & Marschner, H. (1996). Contribution of an arbuscular mycorrhizal fungus to uptake of Cadmnium and Nickel in bean by maize plants. Plant and Soil. 184: 195-205.
Harley, J.L., & Smith, S.E. (1983). Mycorrhizal symbiosis. Academic Press, London UK, 483 p.
Hildebrandt, U., Kaldorf, M., & Bothe, H. (1999). The zinc violet and its colonization by arbuscular mycorrhizal fungi. Journal of Plant Physiology. 154: 709-717. Jamal, A., Ayub, N., Usman, M., & Khan, A.G. (2002). Arbuscular Mycorrhizal Fungi Enhance Zinc and Nickel Uptake from Contaminated Soil by Soybean and Lentil. International Journal of
Phytoremediation. 4(3): 205-221.
Jasper, D.A., Abbott, L.K., & Robson, A.D. (1989). Hyphae of a vesicular-arbuscular mycorrhizal fungus maintain infectivity in dry soil, except when the soil is disturbed. New Phytologist. 112:101-107.
Khan, A.G., Kuek, C., Chaudhry, T.M., Khoo, C.S., & Hayes, W.J. (2000). Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere. 41(1): 197-207.
Kling, J. (1997). Phytoremediation of organics moving rapidly into field trials. Environmental Science and Technology. 31(3): 129A.
Kumar, P.B.A.N., Dushenkov, V., Motto, H., & Raskin, I. (1995). Phytoextraction - the use of plants to remove heavy metals from soils. Environmental Science and Technology. 29: 1232-1238.
Leyval, C., Tumau, K., & Haselwandter, K. (1997). Interactions between Heavy Metals and Mycorrhizal Fungi in Polluted Soils: Physiological, Ecological and Applied Aspects. Mycorrhiza. 7: 139-153.
Leyval, C., Joner, E.J., del Val, C., & Haselwandter, K. (2002). Potential of arbuscular mycorrhizal fungi for bioremediation. Mycorrhizal technology in agriculture. Pp: 175-186.
Liu, A., Hamel, C., Elmi, A., Costa, C., Ma, B., & Smith, D.L. (2002). Concentrations of K, Ca and Mg in maize colonised by arbuscular mycorrhizal fungi under field conditions. Canadian Journal of Soil Science. 82(3): 271-278.
Marschner, H. (1995). Mineral Nutrition of Higher Plants (2nd Edn). Academic Press, London. 889 p.
Memon, A.R., Aktoprakligil, D., Ozdemir, A., & Vertill, A. (2001) Heavy metal accumulation and detoxification mechanisms in plants. Turkish Journal of Botany. 25: 111-121.
Michelsen, A., Schmidt, I.K., Jonasson, S., Quarmby, C., & Sleep, D. (1996). Leaf 15N abundance of subarctic plants provides field evidence that ericoid, ectomycorrhizal and non- and arbuscular
mycorrhizal species access different sources of soil nitrogen. Oecologia. 105: 53-63.
Michelsen, A., Quarmby, C., Sleep, D., & Jonasson, S. (1998). Vascular plant N-15 natural abundance in heath and forest tundra ecosystems is closely correlated with presence and type of mycorrhizal fungi in roots. Oecologia. 115: 406-418.
Nadian, H., Smith, S.E., Alston, A.M., & Murray, R.S. (1997). Effects of soil compaction on plant growth, phosphorus uptake and morphological characteristics of vesiculararbuscular mycorrhizal colonization of Trifolium subterraneum. New Phytologist. 135(2): 303-311.
Noyd, R.K., Pfleger, F.L., & Norland, M.R. (1996). Field responses to added organic matter, arbuscular mycorrhizal fungi, and fertilizer in reclamation of torbonite iron ore tailing. Plant and Soil. 179: 89-97.
Nriagu, J.O. (1979). Global inventory of natural and anthropogenic emissions of trace metals to the atmosphere. Nature. 279: 409-411.
Raskin Ilya, & Ensley Burt, D. (2000). Phytoremediation of toxic metals: using plants to clean up the environment, New York: John Wiley. 304 p.
Rosén, K., Weiliang, Z., & Mårtensson, A. (2005). Arbuscular mycorrhizal fungi mediated uptake of Cs in leek and ryegrass. Science of the Total Environment. 338: 283-290.
Rufyikiri, G., Thiry, Y., Wang, L., Delvaux, B., & Declerck, S. (2002). Uranium uptake and translocation by the arbuscular fungus, Glomus intraradices, under root-organ culture conditions. New Phytologist. 156(2): 275-281.
Rufyikiri, G., Declerck, S., & Thiry, Y. (2004). Comparison of 233U and 33P uptake and translocation by the arbuscular mycorrhizal fungus Glomus intraradices in root organ culture conditions. Mycorrhiza. 14:203-207.
Sanjay Kumar, J.H.A., & Kumar, N. (2011). Potential of mycorrhizal fungi in ecosystem: A Review. International Journal of Research in Botany. 1(1): 1-7.
Shetty, K.G., Banks, M.K., Hetrick, B.A., & Schwab, A.P. (1995). Effects of mycorrhizae and fertilizer amendments on zinc tolerance of plants. Environmental Pollution. 88: 307-314.
Singh, O.V., Labana, S., Pandey, G., Budhiraja, R., & Jain, R.K. (2003). Phytoremediation: An overview of metallic ion decontamination from soil. Applied Microbiology and Biotechnology. 61: 405-412.
Smith, S.E., & Read, D.J. (1997). Mycorrhizal symbiosis, Academic Press, San Diego. 605 p. Smith, M.R., Charvat, I., & Jacobson, R.L. (1998). Arbuscular mycorrhizae promote establishment of prairie species in a tallgrass prairie restoration. Canadian Journal of Botany. 76: 1947-1954.
Söderström, B.E. (1979). Seasonal fluctuations of active fungal biomass in horizons of a podzolized pine-forest soil in central Sweden. Soil Biology and Biochemistry. 11:149-154.
Turnau, K. (1998). Heavy metal content and localization in mycorrhizal Euphorbia cyparissias from zinc wastes in Southern Poland. Acta Societatis Botanicorum Poloniae. 67: 105-113.
Weissenhorn, I., & Leyval, C. (1995). Root Colonization of Maize by a Cd-sensitive and a Cdtolerant Glomus mosseae and Cadmium Uptake in Sand Culture. Plant and Soil. 175: 233-238.
Xavier, I.J., Boyetchko, S.M. (2002). Arbuscular Mycorrhizal Fungi as Biostimulants and Bioprotectants of Crops. Applied Mycology and Biotechnology. 2: 311-340.
Yu, Y., Zhanh, S., & Huang, H. (2010). Behaivor of mercury in a soil-plant system as affected by inoculation with the arbuscular mycorrhizal fungus Glomus mosseae. Mycorrhiza. 20: 407-414
Volume 2, Issue 5 - Serial Number 5
May and June 2014Pages 1854-1864
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