Abstract
Mycorrhizal fungi, obligate biotrophs, form mutualistic associations with plants and provide mainly phosphorus to plants. Mycorrhizal fungi colonize the roots of many plants growing on metal-contaminated soils and play an important role in metal tolerance and accumulation. Even though mycorrhizae are known to inhabit metal contaminated sites; the exact mechanism of colonization is unclear. For example, how mycorrhizal fungi tolerate and maintain homeostasis to toxic metals? Could metal tolerance be transferred to host plants? If so, how do mycorrhizal associations enhance metal accumulation in plants? Mycorrhiza possesses the same constitutive mechanisms as do the higher plants to circumvent metal toxicity. The adaptive tolerance is acquired by expressing genes that confer enhanced metal tolerance under stressed conditions. Various mechanisms adopted by mycorrhizal symbionts to overcome metal toxicity are highlighted. The metal detoxification mechanisms discussed here are likely to serve as a base for developing transgenic plants with abilities of increased metal tolerance and uptake, for decontamination and restoration of the metal polluted sites.
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References
Achard-Joris M, Moreau JL, Lucas M, Baudrimont M, Mesmer-Dudons N, Gonzalez P, Boudou A, Bourdineaud JP (2007) Role of metallothioneins in superoxide radical generation during copper redox cycling: defining the fundamental function of metallothioneins. Biochimie 89:1474–1488
Adriaensen K (2005) Adaptive heavy metal tolerance in the ectomycorrhizal fungi Suillus bovinus and Suillus luteus. Ph.D. thesis, Limburgs Universitair Centrum, Diepenbeek
Amor Y, Babiychuk E, Inze D, Levine A (1998) The involvement of poly(ADP-ribose) polymerase in the oxidative stress responses in plants. FEBS Lett 440:1–7
Arriagada CA, Herrera MA, Ocampo JA (2007) Beneficial effect of saprobe and arbuscular mycorrhizal fungi on growth of Eucalyptus globulus co-cultured with Glycine max in soil contaminated with heavy metals. J Environ Manage 84:93–99
Ashford AE, Peterson RL, Dwarte D, Chilvers GA (1986) Polyphosphate granules in eucalypt mycorrhizas: Determination by energy dispersive x-ray microanalysis. Can J Bot 64:677–687
Awotoye OO, Adewole MB, Salami AO, Ohiembor MO (2009) Arbuscular mycorrhiza contribution to the growth performance and heavy metal uptake of Helianthus annuus Linn in pot culture. Afr J Environ Sci Technol 3:157–163
Azcon R, Peralvarez MDC, Biro B, Roldan A, Lozano JMR (2009) Antioxidant activities and metal acquisition in mycorrhizal plants growing in a heavy-metal multi-contaminated soil amended with treated lignocellulosic agrowaste. Appl Soil Ecol 41:168–177
Benabdellah K, Merlos MA, Azcón-Aguilar C, Ferrol N (2009) GintGRX1, the first characterized glomeromycotan glutaredoxin, is a multifunctional enzyme that responds to oxidative stress. Fungal Genet Biol 46:94–103
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
Berta G, Sampo S, Gamalero E, Massa N, Lemanceau P (2005) Suppression of Rhizoctonia root-rot of tomato by Glomus mossae BEG12 and Pseudomonas fluorescens A6RI is associated with their effect on the pathogen growth and on the root morphogenesis. Eur J Plant Pathol 111:279–288
Blaudez D, Botton B, Chalot M (2000) Cadmium uptake and subcellular compartmentation in the ectomycorrhizal fungus Paxillus involutus. Microbiology 146:1109–1117
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
Chen BD, Thu YG, Duan J, Xiao XY, Smith SE (2007) Effects of the arbuscular mycorrhizal fungus Glomus mosseae on growth and metal uptake by four plant species in copper mine tailings. Environ Pollut 147:374–380
Citterio S, Prato N, Fumagalli P, Aina R, Massa N, Santagostino A, Sgorbati S, Berta G (2005) The arbuscular mycorrhizal fungus Glomus mosseae induces growth and metal accumulation changes in Cannabis sativa L. Chemosphere 59:21–29
Clemens S, Schroeder JI, Degenkolb T (2001) Caenorhabditis elegans express a functional phytochelatin synthase. Eur J Biochem 268:3640–3643
Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182
Courbot M, Diez L, Ruotolo R, Chalot M, Leroy P (2004) Cadmium-responsive thiols in the ectomycorrhizal fungus Paxillus involutus. Appl Environ Microbiol 70:7413–7417
Dalton DA (1995) Antioxidant defenses of plants and fungi. In: Ahmad S (ed) Oxidative stress and antioxidant defenses in biology. Chapman & Hall, New York, pp 298–355
Diatchenko L, Lau YF, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, Siebert PD (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93:6025–6030
Drager DB, Desbrosses-Fonrouge AG, Krach C, Chardonnens AN, Meyer RC, Saumitou-Laprade P, Krämer U (2004) Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels. Plant J 39:425–439
Driver JD, Holben WE, Rilling MC (2005) Characterization of glomalin as a hyphal wall component of arbuscular mycorrhizal fungi. Soil Biol Biochem 37:101–106
Eide DJ (2003) Multiple regulatory mechanisms maintain zinc homeostasis in Saccharomyces cerevisiae. J Nutr 133:1532–1535
Ferrol N, González-Guerrero M, Valderas A, Benabdellah K, Azcón-Aguilar C (2009) Survival strategies of arbuscular mycorrhizal fungi in Cu-polluted environments. Phytochem Rev 8:551–559
Fomina M, Alexander IJ, Colpaert JV, Gadd GM (2005) Solubilization of toxic metal minerals and metal tolerance of mycorrhizal fungi. Soil Biol Biochem 37:851–866
Fowler BA, Hildebrand CE, Kojima Y, Webb M (1987) Nomenclature of metallothionein. Experientia Suppl 52:19–22
Frey B, Zierold K, Brunner I (2000) Extracellular complexation of Cd in the Hartig net and cytosolic Zn sequestration in the fungal mantle of Picea abies-Hebeloma crustuliniforme ectomycorrhizas. Plant Cell Environ 23:1257–1265
Gadd GM (1993) Interactions of fungi with toxic metals. New Phytol 124:25–60
Gaither IA, Eide DJ (2001) Eukaryotic zinc transporters and their regulation. Biometals 14: 251–270
Gamalero E, Trotta A, Massa N, Copetta A, Martinotti MG, Berta G (2004) Impact of two fluorescent pseudomonads and an arbuscular mycorrhizal fungus on tomato plant growth, root architecture, and P acquisition. Mycorrhiza 14:185–192
Gaur A, Adholeya A (2004) Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Curr Sci 86:528–534
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
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
Gonzalez-Guerrero M, Azcon-Aguilar C, Ferrol N (2006) GintABC1 and GintMT1 are involved in Cu and Cd homeostasis in Glomus intraradices. In: Abstracts of the 5th international conference on Mycorrhiza, Granada
González-Guerrero M, Cano C, Azcón-Aguilar C, Ferrrol N (2007) GintMT1 encodes a functional metallothionein in Glomus intraradices that responds to oxidative stress. Mycorrhiza 17:327–335
González-Guerrero M, Benabdellah K, Valderas A, Azcón-Aguilar C, Ferrol N (2010) GintABC1 encodes a putative ABC transporter of the MRP subfamily induced by Cu, Cd, and oxidative stress in Glomus intraradices. Mycorrhiza 20:137–146
Gueldry O, Lazard M, Delort F, Dauplais M, Grigoras I, Blanquet S, Plateau P (2003) Ycf1p-dependent Hg(II) detoxification in Saccharomyces cerevisiae. Eur J Biochem 270:2486–2496
Ha SB, Smith AP, Howden R, Dietrich WM, Bugg S, O’Connell MJ, Goldsbrough PB, Cobbett CS (1999) Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. Plant Cell 11:1153–1164
Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11
Hartley J, Cairney JWG, Meharg AA (1997) Do ectomycorrhizal fungi exhibit adaptive tolerance to potentially toxic metals in the environment? Plant Soil 189:303–319
Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68:139–146
Jacob C, Courbot M, Martin F, Brun A, Chalot M (2004) Transcriptomic response to cadmium in the ectomycorrhizal fungus Paxillus involutus. FEBS Lett 576:423–427
Jentschke G, Fritz E, Godbold DL (1991) Distribution of lead in mycorrhizal and non-mycorrhizal Norway spruce seedlings. Physiol Plant 81:417–422
Joner EJ, Leyval C (1997) Uptake of 109Cd by roots and hyphae of a Glomus mosseae/Trifolium subterraneum mycorrhiza from soil amended with high and low concentrations of cadmium. New Phytol 135:353–360
Joner EJ, Leyval C, Briones R (2000) Metal binding capacity of arbuscular mycorrhizal mycelium. Biol Fertil Soil 226:227–234
Jones DL (1998) Organic acids in the rhizosphere – a critical review. Plant Soil 205:25–44
Kojima Y (1991) Definitions and nomenclature of metallothioneins. Meth Enzymol 205:8–10
Landeweert R, Hoffland E, Finlay RD, Kuyper TW, Van Breemen N (2001) Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals. Trends Ecol Evol 16:248–254
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
Lanfranco L, Novero M, Bonfante P (2005) The mycorrhizal fungus Gigaspora margarita possesses a Cu/Zn superoxide dismutase that is up-regulated during symbiosis with legume hosts. Plant Physiol 137:1319–1330
Leyval C, Turnau K, Haselwandter K (1997) Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza 7:139–153
Li XL, Christie P (2000) Changes in soil solution Zn and pH and uptake of Zn by arbuscular mycorrhizal red clover in Zn-contaminated soil. Chemosphere 42:201–207
Li ZS, Lu YP, Zhen RG, Szczypka M, Thiele DJ, Rea PA (1997) A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis(glutathionato)cadmium. Proc Natl Acad Sci USA 94:42–47
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
Maret W (2003) Cellular zinc and redox states converge in the metallothionein/thionein pair. J Nutr 133:1460–1462
Martin F, Rubini P, Côté R, Kottke I (1994) Aluminium polyphosphate complexes in the mycorrhizal basidiomycete Laccaria bicolor: A 27Al-nuclear magnetic resonance study. Planta 194: 241–246
Martino E, Perottoa S, Parsons R, Gadd GM (2003) Solubilization of insoluble inorganic zinc compounds by ericoid mycorrhizal fungi derived from heavy metal polluted sites. Soil Biol Biochem 35:133–141
Meharg AA (2003) The mechanistic basis of interactions between mycorrhizal associations and toxic metal cations. Mycol Res 107:1253–1265
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
Mehra RK, Tarbet EB, Gray WR, Winge DR (1988) Metal-specific synthesis of two metallothioneins and γ-glutamil peptides in Candida glabrata. Proc Natl Acad Sci USA 85:8815–8819
Mehra RK, Garey JR, Butt TR, Gray WR, Winge DR (1989) Candida glabrata metallothioneins: cloning and sequence of the genes and characterization of proteins. J Biol Chem 264:19747–19753
Moons A (2003) Osgstu3 and osgstu4, encoding tau class glutathione S-transferases, are heavy metal- and hypoxic stress-induced and differentially salt stress-responsive in rice roots. FEBS Lett 553:427–432
Nies DH, Silver S (1995) Ion efflux systems involved in bacterial metal resistances. J Indust Microbiol 14:186–199
Ortiz DF, Ruscitti T, McCue KF, Ow DW (1995) Transport of metal binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. J Biol Chem 270:4721–4728
Ott T, Fritz E, Polle A, Schutzendubel A (2002) Characterisation of antioxidative stress systems in the ectomycorhiza-building basidiomycete Paxillus involutus (Bartsch) Fr. and its reaction to cadmium. FEMS Microbiol Ecol 42:359–366
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
Pocsi I, Prade RA, Penninckx MJ (2004) Glutathione, altruistic metabolite in fungi. Adv Microbiol Physiol 49:1–76
Purin S, Rillig MC (2008) Immuno-cytolocalization of glomalin in the mycelium of the arbuscular mycorrhizal fungus Glomus intraradices. Soil Biol Biochem 40:1000–1003
Ramesh G, Podila GK, Gay G, Marmeisse R, Reddy MS (2009) Copper and cadmium metallothioneins of the ectomycorrhizal fungus Hebeloma cylindrosporum have different patterns of regulation. Appl Environ Microbiol 75:2266–2274
Redon PO, Beguiristain T, Leyval C (2008) Influence of Glomus intraradices on Cd partitioning in a pot experiment with Medicago truncatula in four contaminated soils. Soil Biol Biochem 40:2710–2712
Rhody D (2002) Erste Schritte zur Etablierung und Verbesserung von Transformations systemen fu r wurzelbesiedelnde Pflanzen. Ph.D. thesis, The University of Marburg, Marburg
Rivera-Becerril F, Calantzis C, Turnau K, Caussanel JP, 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
Rouch DA, Lee BTD, Morby AP (1995) Understanding cellular responses to toxic agents: a model for mechanism choice in bacterial metal resistance. J Ind Microbiol 14:132–141
Sanita` L, Prasad MNV, Ottonello S (2002) Metal chelating peptides and proteins in plants. In: Prasad MNV, Strzalka K (eds) Physiology and biochemistry of metal toxicity and tolerance in plants. Kluwer, Dordrecht, pp 59–94
Schmoger MEV, Oven M, Grill E (2000) Detoxification of arsenic by phytochelatins in plants. Plant Physiol 122:793–802
Silver S, Walderhaug M (1992) Gene regulation of plasmid and chromosome determined inorganic ion transport in bacteria. Microbiol Rev 56:195–228
Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation (Tansley Review No. 52). New Phytol 125:27–58
Smith AP, DeRidder BP, Guo WJ, Seeley EH, Regnier FE, Goldsbrough PB (2004) Proteomic analysis of Arabidopsis glutathione S-transferases from benoxacor- and copper-treated seedlings. J Biol Chem 279:26098–26104
Stommel M, Mann P, Franken P (2001) EST-library construction using spore RNA of the arbuscular mycorrhizal fungus Gigaspora rosea. Mycorrhiza 10:281–285
Sudová R, Doubková P, Vosátka M (2008) Mycorrhizal association of Agrostis capillaris and Glomus intraradices under heavy metal stress: combination of plant clones and fungal isolates from contaminated and uncontaminated substrates. Appl Soil Ecol 40:19–29
Tamai KT, Gralla EB, Ellerby LM, Valentine JS, Thiele DJ (1993) Yeast and mammalian metallothioneins functionally substitute for yeast copper-zinc superoxide dismutase. Proc Natl Acad Sci USA 90:8013–8017
Tomsett AB (1993) Genetics and molecular biology of metal tolerance in fungi. In: Jennings DH (ed.) Stress tolerance of fungi., pp 69–95
Turnau K, Ryszka P, Gianinazzi-Pearson V, van Tuinen D (2001) Identification of arbuscular mycorrhizal fungi in soils and roots of plants colonizing zinc wastes in southern Poland. Mycorrhiza 10:169–174
Vare H (1990) Aluminium polyphosphate in the ectomycorrhizal fungus Suillus variegatus (Fr.) O. Kunze as revealed by energy dispersive spectrometry. New Phytol 116:663–668
Vatamaniuk OK, Bucher EA, Ward JT, Rea PA (2001) A new pathway for heavy metal detoxification in animals: phytochelatins synthase is required for cadmium tolerance in Caenorhabditis elegans. J Boil Chem 276:20817–20820
Waalkes MP, Goering PL (1990) Metallothionein and other cadmium-binding proteins: recent developments. Chem Res Toxicol 3:281–288
Waschke A, Sieh D, Tamasloukht M, Fischer K, Mann P, Franken P (2006) Identification of heavy metal-induced genes encoding glutathione S-transferases in the arbuscular mycorrhizal fungus Glomus intraradices. Mycorrhiza 17:1–10
Williams LE, Pittman JK, Hall JL (2000) Emerging mechanisms for heavy metal transport in plants. BBA Biomembr 1465:104–126
Zhu YG, Christie P, Laidlaw AS (2001) Uptake of Zn by arbuscular mycorrhizal white clover from Zn-contaminated soil. Chemosphere 42:193–199
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Saraswat, S., Rai, J.P.N. (2011). Mechanism of Metal Tolerance and Detoxification in Mycorrhizal Fungi. In: Khan, M., Zaidi, A., Goel, R., Musarrat, J. (eds) Biomanagement of Metal-Contaminated Soils. Environmental Pollution, vol 20. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-1914-9_9
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