Role of Mycorrhiza in Re-forestation at Heavy Metal-Contaminated Sites

Chapter
Part of the Soil Biology book series (SOILBIOL, volume 31)

Abstract

Re-forestation of mining areas is essential to limit soil erosion by wind and water, including runoff of metallic sediments. Here, we will focus on ectomycorrhizal (ECM) fungi, the predominant group of root symbionts of pioneer trees that are essential in afforestation and re-forestation practices. We review the literature dealing with the diversity and functional strategies of ECM communities and population on metal-contaminated forest sites in trees established on heavy metal-contaminated areas in different stages of succession. New knowledge gained from investigation of the ECM community in a former uranium mining area and an undisturbed site is included. In addition, molecular biological investigation of the ECM fungus Tricholoma vaccinum demonstrates changed gene expression profiles after contact with heavy metals.

Keywords

Mycorrhizal Fungus Fruiting Body Fungal Community Arbuscular Mycorrhiza Paxillus Involutus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Adriaensen K, Vangronsveld J, Colpaert JV (2006) Zinc-tolerant Suillus bovinus improves growth of Zn-exposed Pinus sylvestris seedlings. Mycorrhiza 16:553–558PubMedCrossRefGoogle Scholar
  2. Agerer R (2001) Exploration types of ectomycorrhizae – a proposal to classify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11:107–114CrossRefGoogle Scholar
  3. Agerer R (2006) Colour atlas of ectomycorrhizae. Einhorn-Verlag, Schwäbisch Gmünd, GermanyGoogle Scholar
  4. Ahonen-Jonnarth U, van Hees PAW, Lundstrom US, Finlay RD (2000) Organic acids produced by mycorrhizal Pinus sylvestris exposed to elevated aluminium and heavy metal concentrations. New Phytol 146:557–567CrossRefGoogle Scholar
  5. Ashkannejhad S, Horton TR (2006) Ectomycorrhizal ecology under primary succession on coastal sand dunes: interactions involving Pinus contorta, suilloid fungi and deer. New Phytol 169:345–354PubMedCrossRefGoogle Scholar
  6. Baar J, Horton TR, Kretzer AM, Bruns TD (1999) Mycorrhizal colonization of Pinus muricata from resistant propagules after a stand-replacing wildfire. New Phytol 143:409–418CrossRefGoogle Scholar
  7. Baum C, Hrynkiewicz K, Leinweber P, Meißner R (2006) Heavy-metal mobilization and uptake by mycorrhizal and nonmycorrhizal willows (Salix x dasyclados). J Plant Nutr Soil Sci 169:516–522CrossRefGoogle Scholar
  8. Bellion M, Courbot M, Jacob C, Blaudez D, Chalot M (2006) Extracellular and cellular mechanisms sustaining metal tolerance in ectomycorrhizal fungi. FEMS Microbiol Lett 254(2):173–181PubMedCrossRefGoogle Scholar
  9. Bissonnette L, St-Arnaud M, Labrecque M (2010) Phytoextraction of heavy metals by two Salicaceae clones in symbiosis with arbuscular mycorrhizal fungi during the second year of a field trial. Plant Soil 332:55–67CrossRefGoogle Scholar
  10. Boult S, Hand VL, Vaughan DJ (2006) Microbial controls on metal mobility under the low nutrient fluxes found throughout the subsurface. Sci Total Environ 372(1):299–305Google Scholar
  11. Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understnding global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77CrossRefGoogle Scholar
  12. Colpaert JV (2008) Heavy metal pollution and genetic adaptations in ectomycorrhizal fungi. In: Avery S, Stratford M, van West P (eds) Stress in yeasts and filamentous fungi. Elsevier, Amsterdam, pp 157–173CrossRefGoogle Scholar
  13. Colpaert JV, Muller LAH, Lambaerts M, Adriaensen K, Vangronsveld J (2004) Evolutionary adaptation to Zn toxicity in populations of Suilloid fungi. New Phytol 162:549–559CrossRefGoogle Scholar
  14. Courty PE, Pritsch K, Schloter M, Hartmann A, Garbaye J (2005) Activity profiling of ectomycorrhiza communities in two forest soils using multiple enzymatic tests. New Phytol 167:309–319PubMedCrossRefGoogle Scholar
  15. Cripps CL (2004) Ectomycorrhizal fungi above and below ground in a small, isolated aspen stand: a simple system reveals fungal fruiting strategies and an edge effect. In: Cripps (ed) Fungi in Forest Ecosystems: systematics, diversity and ecology, New York Botanical Garden Press, New York, pp 249–265Google Scholar
  16. Cromack K; Sollins P; Graustein WC; Speidel, K, Todd, AW, Spycher, G, Li CY, Todd RL (1979) Calcium-oxalate accumulation and soil weathering in mats of the hypogeous fungus Hysterangium-crassum. Soil Biol Biochem 11(5):463–468Google Scholar
  17. Dancis A, Klausner RD, Hinnesbuch AG, Barriocanal JG (1990) Genetic evidence that ferric reductase is required for iron uptake in Saccharomyces cerevisiae. Mol Cell Biol 10:2294–2301PubMedGoogle Scholar
  18. Dimkpa CO, Svatoš A, Dabrowska P, Schmidt A, Boland W, Kothe E (2008) Involvement of siderophores in the reduction of metal-induced inhibition of auxin synthesis in Streptomyces spp. Chemosphere 74:19–25PubMedCrossRefGoogle Scholar
  19. Finlay RD (2008) Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot 59(5):1115–1126PubMedCrossRefGoogle Scholar
  20. Fiore-Donno AM, Martin F (2001) Populations of ectomycorrhizal Laccaria amethystina and Xerocomus spp. show contrasting colonization patterns in a mixed forest. New Phytol 152(3):533–542Google Scholar
  21. Fomina MA, Alexander IJ, Colpaert JV, Gadd GM (2005) Solubilization of toxic metal minerals and metal tolerance of mycorrhizal fungi. Soil Biol Biochem 37:851–866CrossRefGoogle Scholar
  22. Fomina M, Charnock JM, Hillier S, Alvarez R, Livens F, Gadd GM (2008) Role of fungi in the biogeochemical fate of depleted uranium. Curr Biol 18(9):R357–R377CrossRefGoogle Scholar
  23. 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 abiesHebeloma crustuliniforme ectomycorrhizas. Plant Cell Environ 23:1257–1266CrossRefGoogle Scholar
  24. Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176(1):22–36PubMedCrossRefGoogle Scholar
  25. Gadd GM (1993) Interactions of fungi with toxic metals. New Phytol 124:25–60CrossRefGoogle Scholar
  26. Gadd GM (2010) Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156:609–643PubMedCrossRefGoogle Scholar
  27. Galli U, Schüepp H, Brunold C (1994) Heavy metal binding by mycorrhizal fungi. Physiol Plant 92:364–368CrossRefGoogle Scholar
  28. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes: application to the identificcation of mycorrhizae and rusts. Mol Ecol 2:113–118PubMedCrossRefGoogle Scholar
  29. Gardes M, Bruns TD (1996) Community structure of ectomycorrhizal fungi in a Pinus muricata forest: Above- and below-ground views. Can J Bot 74:1572–1583Google Scholar
  30. Gebhardt S, Neubert K, Wöllecke J, Münzenberger B, Hüttl RF (2007) Ectomycorrhiza communities of red oak (Quercus rubra L.) of different age in the Lusatian lignite mining district, East Germany. Mycorrhiza 17:279–290PubMedCrossRefGoogle Scholar
  31. Godbold DL (1994) Aluminium and heavy metal stress: from the rhizosphere to the whole plant. In: Gobold DL, Hüttermann A (eds) Effects of acid rain on forest processes. Wiley-Liss, New York, pp 231–264Google Scholar
  32. Gorfer M, Persak H, Berger H, Brynda S, Bandian D, Strauss J (2009) Identification of heavy metal regulated genes from the root associated ascomycete Cadophora finlandica using a genomic microarray. Mycol Res 113:1377–1388PubMedCrossRefGoogle Scholar
  33. Gryta H, Debaud JC, Marmeisse R (2001) Population dynamics of the symbiotic mushroom Hebeloma cylindrosporum: mycelial persistence and inbreeding. Heredity 84:294–302CrossRefGoogle Scholar
  34. Gryta H, Debaud JC, Effosse A, Gay G, Marmeisse R (1997) Fine-scale structure of populations of the ectomycorrhizal fungus Hebeloma cylindrosporum in coastal sand dune forest ecosystems. Mol Ecol 6(4):353–364Google Scholar
  35. Hartley J, Cairney JWG, Meharg AA (1997) Do ectomycorrhizal fungi exhibit adaptive tolerance to potentially toxic metals in the environment? Plant Soil 189:303–319CrossRefGoogle Scholar
  36. Hogberg N, Guidot A, Jonsson M, Dahlberg A (2009) Microsatellite markers for the ectomycorrhizal basidiomycete Lactarius mammosus. Mol Ecol Resour 9(3):1008–1010Google Scholar
  37. Horton TR, Bruns TD (1998) Multiple host fungi are the most frequent and abundant ectomycorrhizal types in a mixed stand of Douglas fir (Pseudotsuga menziesii) and bishop pine (Pinus muricata). New Phytol 139:331–339CrossRefGoogle Scholar
  38. Iordache V, Gherghel F, Kothe E (2009) Assessing the effect of disturbances on ectomycorrhiza diversity. Int J Environ Res Public Health 6:416–422CrossRefGoogle Scholar
  39. Iordache V, Kothe E, Neagoe A, Gherghel F (2011) A conceptual framework for up-scaling ecological processes and application to ectomycorrhizal fungi. In: Rai M, Varma A (eds) Diversity and biotechnology of ectomycorrhizae. Springer, Berlin, pp 255–300Google Scholar
  40. Izzo A, Agbowo J, Bruns TD (2005) Detection of plot-level changes in ectomycorrhizal communities across years in an old-growth mixed-conifer forest. New Phytol 166:619–630PubMedCrossRefGoogle Scholar
  41. Jacob C, Courbot ML, Martin F, Brun A, Chalot M (2004) Transcriptomic responses to cadmium in the ectomycorrhizal fungus Paxillus involutus. FEBS Lett 576(3):423–427PubMedCrossRefGoogle Scholar
  42. Jentschke G, Godbold DL (2000) Metal toxicity and ectomycorrhizas. Physiol Plant 109:107–116CrossRefGoogle Scholar
  43. Joner EJ, Leyval C (1997) Uptake of 109Cd by roots and hyphae of a Glomus mossae/Trifolium subterraneum mycorrhiza from soil amended with high and low concentrations of cadmium. New Phytol 135:353–360CrossRefGoogle Scholar
  44. Joner EJ, Leyval C (2001) Time-course of heavy metal uptake in maize and clover as affected by root density and different mycorrhizal inoculation regimes. Biol Fertil Soils 33(5):351–357CrossRefGoogle Scholar
  45. Jones MD, Hutchinson TC (1986) The effect of mycorrhizal infection on the response of Betula papyrifera to nickel and copper. New Phytol 102:429–442CrossRefGoogle Scholar
  46. Jumpponen A, Jones KL (2010) Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere. New Phytol 184:438–448CrossRefGoogle Scholar
  47. Kalač P, Burda J, Staskova I (1991) Concentrations of lead, cadmium, mercury and copper in mushrooms in the vicinity of a lead smelter. Sci Total Environ 105:109–119PubMedCrossRefGoogle Scholar
  48. Kõljalg U, Larsson KH, Abarenkov K, Nilsson RH, Alexander I, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Vrålstad T, Ursing BM (2005) UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. New Phytol 166:1063–1068PubMedCrossRefGoogle Scholar
  49. Kothe E, Bergmann H, Buchel G (2005) Molecular mechanisms in bio-geo-interactions: from a case study to general mechanisms. Chem Erde 65(S1):7–27CrossRefGoogle Scholar
  50. Krause K, Kothe E (2006) Use of RNA fingerprinting to identify fungal genes specifically expressed during ectomycorrhizal interaction. J Basic Microbiol 46(5):387–399PubMedCrossRefGoogle Scholar
  51. Kretzer AM, Dunham S, Molina R, Spatafora JW (2003) Microsatellite markers reveal the below ground distribution of genets in two species of Rhizopogon forming tuberculate ectomycorrhizas on Douglas fir. New Phytol 161:313–320CrossRefGoogle Scholar
  52. Krpata D, Peintner U, Langer I, Fitz JW, Schweiger P (2008) Ectomycorrhizal communities associated with Populus tremula growing on a heavy metal contaminated site. Mycol Res 112:106–1079CrossRefGoogle Scholar
  53. 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 16:248–254PubMedCrossRefGoogle Scholar
  54. Mankel A, Krause K, Kothe E (2002) Identification of a hydrophobin gene that is developmentally regulated in the ectomycorrhizal fungus Tricholoma terreum. Appl Environ Microbiol 68(3):1408–1413PubMedCrossRefGoogle Scholar
  55. Margulies M, Egholm M, Altaian WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer ML, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu P, Begley RF, Rothberg JM (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380PubMedGoogle Scholar
  56. Marschner P, Godbold DL, Jentschke G (1996) Dynamics of lead accumulation in mycorrhizal and non-mycorrhizal Norway spruce (Picea abies (L) Karst). Plant Soil 178(2):239–245CrossRefGoogle Scholar
  57. Martin F, Aerts A, Ahren D, Brun A, Danchin EGJ, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V, Salamov A, Shapiro HJ, Wuyts J, Blaudez D, Buee M, Brokstein P, Canback B, Cohen D, Courty PE, Coutinho PM, Delaruelle C, Detter JC, Deveau A, DiFazio S, Duplessis S, Fraissinet-Tachet L, Lucic E, Frey-Klett P, Fourrey C, Feussner I, Gay G, Grimwood J, Hoegger PJ, Jain P, Kilaru S, Labbe J, Lin YC, Legue V, Le Tacon F, Marmeisse R, Melayah D, Montanini B, Muratet M, Nehls U, Niculita-Hirzel H, Oudot-Le Secq MP, Peter M, Quesneville H, Rajashekar B, Reich M, Rouhier N, Schmutz J, Yin T, Chalot M, Henrissat B, Kues U, Lucas S, Van de Peer Y, Podila GK, Polle A, Pukkila PJ, Richardson PM, Rouze P, Sanders IR, Stajich JE, Tunlid A, Tuskan G, Grigoriev IV (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452(7183):88–92PubMedCrossRefGoogle Scholar
  58. Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, Montanini B, Morin E, Noel B, Percudani R, Porcel B, Rubini A, Amicucci A, Amselem J, Anthouard V, Arcioni S, Artiguenave F, AuryJ-M BP, Bolchi A, Brenna A, Brun A, Buée M, Cantarel B, Chevalier G, Couloux A, Da Silva C, Denoeud F, Duplessis S, Ghignone S, Hilselberger B, Iotti M, Marçais B, Mello A, Miranda M, Pacioni G, Quesneville H, Riccioni C, Ruotolo R, Splivallo R, Stocchi V, Tisserant E, Viscomi AR, Zambonelli A, Zampieri E, Henrissat B, Lebrun M-H, Paolocci F, Bonfante P, Ottonello S, Wincker P (2010) Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464:1033–1038PubMedCrossRefGoogle Scholar
  59. Meharg AA (2003) The mechanistic basis of interactions between mycorrhizal associations and toxic metal cations. Mycol Res 107:1253–1265PubMedCrossRefGoogle Scholar
  60. Meharg AA, Cairney JWG (2000) Co-evolution of mycorrhizal symbionts and their hosts to metal-contaminated environments. Adv Ecol Res 30:69–112CrossRefGoogle Scholar
  61. Mleczko P (2004) Mycorrhizal and saprobic macrofungi of two zinc wastes in southern Poland. Acta Biol Cracov Ser Bot 46:25–38Google Scholar
  62. Muehlmann O, Bacher M, Peintner U (2008) Polygonum viviparum mycobionts on an alpine primary successional glacier forefront. Mycorrhiza 18:87–95CrossRefGoogle Scholar
  63. Nara K (2006a) Ectomycorrhizal networks and seedling establishment during early primary succession. New Phytol 169:169–178PubMedCrossRefGoogle Scholar
  64. Nara K (2006b) Pioneer dwarf willow may facilitate tree succession by providing late colonizers with compatible ectomycorrhizal fungi in a primary successional volcanic desert. New Phytol 171:187–198PubMedCrossRefGoogle Scholar
  65. Nara K, Nakaya H, Wu BY, Zhou ZH, Hogetsu T (2003) Underground primary succession of ectomycorrhizal fungi in a volcanic desert on Mount Fuji. New Phytol 159:743–756CrossRefGoogle Scholar
  66. Neilands JB (1995) Siderophores – structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726PubMedGoogle Scholar
  67. Perotto S, Martino E (2001) Molecular and cellular mechanisms of heavy metal tolerance in mycorrhizal fungi: what perspectives for bioremediation? Minerva Biotechnologica 13:55–63Google Scholar
  68. Plassard C, Fransson P (2009) Regulation of low molecular weight organic acid production in fungi. Fungal Biol Rev 23:30–39CrossRefGoogle Scholar
  69. Pritsch K, Munch JC, Buscot F (1997) Morphological and anatomical characterisation of black alder Alnus glutinosa (L.) Gaertn. Ectomycorrhizas. Mycorrhiza 7(4):201–216Google Scholar
  70. Pulford ID, Watson C (2003) Phytoremediation of heavy metal-contaminated land by trees – a review. Environ Int 29:529–540PubMedCrossRefGoogle Scholar
  71. Rajala T (2008) Responses of soil microbial communities to clonal variation of Norway spruce. Dissertation, University of Helsinki, FinlandGoogle Scholar
  72. Rineau F, Courty PE, Uroz S, Buée M, Garbaye J (2008) Simple microplate assays to measure iron mobilization and oxalate secretion by ectomycorrhizal tree roots. Soil Biol Biochem 40:2460–2463CrossRefGoogle Scholar
  73. Rosling A, Lindahl BD, Taylor AFS, Finlay RD (2004) Mycelial growth and substrate acidification of ectomycorrhizal fungi in response to different minerals. FEMS Microbiol Ecol 47(1):31–37Google Scholar
  74. Rudawska M, Leski T, Trocha LK, Gornowicz R (2006) Ectomycorrhizal status of Norway spruce seedlings from bare-root forest nurseries. Ecol Manag 236:375–384CrossRefGoogle Scholar
  75. Rühling A, Söderström B (1990) Changes in fruitbody production of mycorrhizal and litter decomposing macromycetes in heavy metal polluted coniferous forests in north Sweden. Water Air Soil Pollut 49:375–387CrossRefGoogle Scholar
  76. Rühling A, Bååth E, Nordgren A, Söderström B (1984) Fungi in metal-contaminated soil near the Gusum brass mill, Sweden. Ambio 13:34–36Google Scholar
  77. Schuster SC (2008) Next-generation sequencing transforms today’s biology. Nat Methods 5:16–18PubMedCrossRefGoogle Scholar
  78. Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365PubMedCrossRefGoogle Scholar
  79. Sell J, Kayser A, Schulin R, Brunner I (2005) Contribution of ectomacorrhizal fungi to cadmium uptake of poplars and willows from a heavily polluted soil. Plant Soil 277:245–253CrossRefGoogle Scholar
  80. Selosse MA, Richard F, He X, Simard SW (2006) Mycorrhizal networks: des liaisons dangereuses? Trends Ecol Evol 21:621–628PubMedCrossRefGoogle Scholar
  81. Simard SW, Durall DM (2004) Mycorrhizal networks: a review of their extent, function and importance. Can J Bot 82(8):1140–1165CrossRefGoogle Scholar
  82. Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, LondonGoogle Scholar
  83. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, LondonGoogle Scholar
  84. Staudenrausch S, Kaldorf M, Renker C, Luis P, Buscot F (2005) Diversity of the ectomycorrhiza community at a uranium mining heap. Biol Fertil Soils 41:439–446CrossRefGoogle Scholar
  85. Tedersoo L, Kõljalg U, Hallenberg N, Larsson KH (2003) Fine scale distribution of ectomycorrhizal fungi and roots across substrate layers including coarse woody debris in a mixed forest. New Phytol 159:153–165CrossRefGoogle Scholar
  86. Tedersoo L, Suvi T, Larsson E, Koljalg U (2006) Diversity and community structure of ectomycorrhizal fungi in a wooded meadow. Mycol Res 110:734–748PubMedCrossRefGoogle Scholar
  87. Tedersoo L, May TW, Smith ME (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20(4):217–263PubMedCrossRefGoogle Scholar
  88. Trowbridge J, Jumpponen A (2004) Fungal colonization of shrub willow roots at the forefront of a receding glacier. Mycorrhiza 14:283–293PubMedCrossRefGoogle Scholar
  89. Turnau K, Gucwa E, Mleczko P, Godzik B (1988) Metal content in fruit-bodies and mycorrhizas of Pisolithus arrhizus from zinc wastes in Poland. Acta Mycologica 33:59–67Google Scholar
  90. Turnau K, Mleczko P, Blaudez D, Chalot M, Botton B (2002) Heavy metal binding properties of Pinus sylvestris mycorrhizas from industrial wastes. Acta Societatis Botanicorum Poloniae 71:253–261Google Scholar
  91. van Hees PAW, Rosling A, Lundstrom US, Finlay RD (2006) The biogeochemical impact of ectomycorrhizal conifers on major soil elements (Al, Fe, K and Si). Geoderma 136(1–2):364–377CrossRefGoogle Scholar
  92. van Scholl L, Hoffland E, van Breemen N (2006) Organic anion exudation by ectomycorrhizal fungi and Pinus sylvestris in response to nutrient deficiencies. New Phytol 170(1):153–163Google Scholar
  93. van Scholl L, Kuyper TW, Smits MM, Landeweert R, Hoffland E, van Breemen N (2008) Rock-eating mycorrhizas: their role in plant nutrition and biogeochemical cycles. Plant Soil 303:35–47CrossRefGoogle Scholar
  94. Vrålstad T, Myhre E, Schumacher T (2002) Molecular diversity and phylogenetic affinities of symbiotic root-associated ascomycetes of the Helotiales in burnt and metal polluted habitats. New Phytol 155:131–148CrossRefGoogle Scholar
  95. Wilkins DA (1991) The influence of sheathing (ecto-) mycorrhizas of trees on the uptake and toxicity of metals. Agr Ecosyst Environ 35:245–260CrossRefGoogle Scholar
  96. Wilkinson DM, Dickinson NM (1995) Metal resistance in trees: the role of mycorrhizae. Oikos 72:298–300CrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Department of MycologyPhilipps-University of MarburgMarburgGermany
  2. 2.Institute of MicrobiologyFriedrich Schiller UniversityJenaGermany

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