Diversity and Biotechnology of Ectomycorrhizae pp 231-254 | Cite as
Metal Elements and the Diversity and Function of Ectomycorrhizal Communities
Abstract
This chapter focuses on the mutual relations between metal elements and the population biology, community composition and biodiversity of ectomycorrhizal fungi (ECMF) and on the contribution of ECMF to metal transfers in food webs. The ectomycorrhizal (ECM) association of trees and fungi is successful in recycling scarce essential metal elements and in colonizing soils with high levels of metal toxicity. Uptake and translocation of metal elements by ECMF may account for major deviations from simple models of soil metal budgets. Accumulation of certain essential and non-essential metals and metalloids (e.g. K, Rb, Cs, As, Se, Zn, Cd, Hg, Ag) is common in ECMF, while other elements tend to be excluded (e.g. Al, Pb). Bioconcentration factors (BCFs) are species, strain and metal specific. A negative correlation between environmental metal concentrations and BCFs appears to be the rule. The role of ECMF as a nutrient source of rare elements (e.g. Se) and as an important gateway of toxic metals to vertebrate foodwebs in polluted areas merits further study.
ECM communities in metalliferous soils can be surprisingly diverse. The potential to colonize metalliferous soils is widespread in various phylogenetic groups of ECMF. The microevolution of metal tolerance does not require populational differentiation.
Keywords
Litter Decomposition Host Tree Metal Tolerance Serpentine Soil Saprotrophic FungusReferences
- Adle DJ, Sinani D, Kim H, Lee J (2006) A Cadmium-transporting P1B-type ATPase in Yeast Saccharomyces cerevisiae. J Biol Chem 282:947–955PubMedCrossRefGoogle Scholar
- Adriaensen K, van der Lelie D, Van Laere A, Vangronsveld J, Colpaert JV (2004) A zinc-adapted fungus protects pines from zinc stress. New Phytol 161:549–555CrossRefGoogle Scholar
- Adriaensen K, Vralstad T, Noben JP, Vangronsveld J, Colpaert JV (2005) Copper-adapted Suillus luteus, a symbiotic solution for pines colonizing Cu mine spoils. Appl Environ Microbiol 71:7279PubMedCrossRefGoogle Scholar
- Adriaensen K, Vangronsveld J, Colpaert JV (2006) Zinc-tolerant Suillus bovinus improves growth of Zn-exposed Pinus sylvestris seedlings. Mycorrhiza 16:553–558PubMedCrossRefGoogle Scholar
- Åhman B, Wright SM, Howard BJ (2004) Radiocaesium in lynx in relation to ground deposition and diet. Radiat Environ Biophys 43:119–126PubMedCrossRefGoogle Scholar
- Ahonen-Jonnarth U, Finlay RD (2001) Effects of elevated nickel and cadmium concentrations on growth and nutrient uptake of mycorrhizal and non-mycorrhizal Pinus sylvestris seedlings. Plant Soil 236:129–138CrossRefGoogle Scholar
- Amir H, Pineau R (1998) Effects of metals on the germination and growth of fungal isolates from New Caledonian ultramafic soils. Soil Biol Biochem 30:2043–2054CrossRefGoogle Scholar
- Arnolds E (1991) Decline of ectomycorrhizal fungi in Europe. Agric Ecosyst Environ 35:209–244CrossRefGoogle Scholar
- Bellion M, Courbot M, Jacob C, Blaudez D, Chalot M (2006) Extracellular and cellular mechanisms sustaining metal tolerance in ectomycorrhizal fungi. FEMS Microbiol Lett 254:173–181PubMedCrossRefGoogle Scholar
- Bellion M, Courbot M, Jacob C, Guinet F, Blaudez D, Chalot M (2007) Metal induction of a Paxillus involutus metallothionein and its heterologous expression in Hebeloma cylindrosporum. New Phytol 174:151–158PubMedCrossRefGoogle Scholar
- Berthelsen BO, Olsen RA, Steinnes E (1995) Ectomycorrhizal heavy metal accumulation as a contributing factor to heavy metal levels in organic surface soils. Sci Total Environ 170:141–149CrossRefGoogle Scholar
- Blum JD, Klaue A, Nezat CA, Driscoll CT, Johnson CE, Siccama TG, Eagar C, Fahey TJ, Likens GE (2002) Mycorrhizal weathering of apatite as an important calcium source in base-poor forest ecosystems. Nature 417:729–731PubMedCrossRefGoogle Scholar
- Borovička J, Řanda Z (2007) Distribution of iron, cobalt, zinc and selenium in macrofungi. Mycol Prog 6:249–259CrossRefGoogle Scholar
- Borovička J, Řanda Z, Jelínek E, Kotrba P, Dunn CE (2007) Hyperaccumulation of silver by Amanita strobiliformis and related species of the section Lepidella. Mycol Res 111:1339–1344PubMedCrossRefGoogle Scholar
- Brearley FQ (2006) Differences in the growth and ectomycorrhizal community of Dryobalanops lanceolata (Dipterocarpaceae) seedlings grown in ultramafic and non-ultramafic soils. Soil Biol Biochem 38:3407–3410CrossRefGoogle Scholar
- Brown MT, Wilkins DA (1985) Zinc tolerance of mycorrhizal Betula. New Phytol 99:101–106CrossRefGoogle Scholar
- Brun CB, Åström ME, Peltola P, Johansson M (2008) Trends in major and trace elements in decomposing needle litters during a long-term experiment in Swedish forests. Plant Soil 306:199–210CrossRefGoogle Scholar
- Burgstaller W, Schinner F (1993) Leaching of metals with fungi. J Biotechnol 27:91–116CrossRefGoogle Scholar
- Chudzynski K, Falandysz J (2008) Multivariate analysis of elements content of Larch Bolete (Suillus grevillei) mushroom. Chemosphere 73:1230–1239PubMedCrossRefGoogle Scholar
- Colpaert JV (2008) Heavy metal pollution and genetic adaptations in ectomycorrhizal fungi. In: Simon V Avery, Malcolm Stratford, Pieter Van West (eds) Stress in Yeasts and Ilamentous Fungi (eds) British Mycological Symposia Series. Academic Press, Elsevier Ltd., LondonGoogle Scholar
- Colpaert JV, van Assche JA (1992) Zinc toxicity in ectomycorrhizal Pinus sylvestris. Plant Soil 143:201–211CrossRefGoogle Scholar
- Colpaert JV, van Assche JA (1993) The effects of cadmium on ectomycorrhizal Pinus sylvestris L. New Phytol 123:325–333CrossRefGoogle Scholar
- Colpaert JV, Adriaensen K, Muller LAH, Lambaerts M, Faes C, Carleer R, Vangronsveld J (2005) Element profiles and growth in Zn-sensitive and Zn-resistant Suilloid fungi. Mycorrhiza 15:628–634PubMedCrossRefGoogle Scholar
- Dighton J, Tugay T, Zhdanova N (2008) Fungi and ionizing radiation from radionuclides. FEMS Microbiol Lett 281:109–120PubMedCrossRefGoogle Scholar
- Douhan GW, Huryn KL, Douhan LI (2007) Significant diversity and potential problems associated with inferring population structure within the Cenococcum geophilum species complex. Mycologia 99:812–819PubMedCrossRefGoogle Scholar
- Ernst WH (2000) Evolution of metal hyperaccumulation and phytoremediation hype. New Phytol 146:357–358CrossRefGoogle Scholar
- Finlay RD (2008) Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot 59:1115PubMedCrossRefGoogle Scholar
- 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
- Fomina MA, Charnock J, Bowen AD, Gadd GM (2007) X-ray absorption spectroscopy (XAS) of toxic metal mineral transformations by fungi. Environ Microbiol 9:308–321PubMedCrossRefGoogle Scholar
- Gadd GM (1993) Interactions of fungi with toxic metals. New Phytol 124:25–60CrossRefGoogle Scholar
- Gadd GM (2007) Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol Res 111:3–49PubMedCrossRefGoogle Scholar
- Gadgil RL, Gadgil PD (1971) Mycorrhiza and litter decomposition. Nature 233:133PubMedCrossRefGoogle Scholar
- Gast CH, Jansen E, Bierling J, Haanstra L (1988) Heavy metals in mushrooms and their relationship with soil characteristics. Chemosphere 17:789–799CrossRefGoogle Scholar
- Gibson BR, Mitchell DT (2004) Nutritional influences on the solubilization of metal phosphate by ericoid mycorrhizal fungi. Mycol Res 108:947–954PubMedCrossRefGoogle Scholar
- Godbold DL, Jentschke G, Winter S, Marschner P (1998) Ectomycorrhizas and amelioration of metal stress in forest trees. Chemosphere 36:757–762CrossRefGoogle Scholar
- Gonçalves SC, Portugal A, Gonçalves MT, Vieira R, Martins-Loução MA, Freitas H (2007) Genetic diversity and differential in vitro responses to Ni in Cenococcum geophilum isolates from serpentine soils in Portugal. Mycorrhiza 17:677–686PubMedCrossRefGoogle Scholar
- Gonçalves SC, Martins-Loução MA, Freitas H (2009) Evidence of adaptive tolerance to nickel in isolates of Cenococcum geophilum from serpentine soils. Mycorrhiza 19:221–230PubMedCrossRefGoogle Scholar
- Hagerberg D, Pallon J, Wallander H (2005) The elemental content in the mycelium of the ectomycorrhizal fungus Piloderma sp. during the colonization of hardened wood ash. Mycorrhiza 15:387–392PubMedCrossRefGoogle Scholar
- Hartley J, Cairney JW, Meharg AA (1997) Do ectomycorrhizal fungi exhibit adaptive tolerance to potentially toxic metals in the environment? Plant Soil 189:303–319CrossRefGoogle Scholar
- Hohmann U, Huckschlag D (2005) Investigations on the radiocaesium contamination of wild boar (Sus scrofa) meat in Rhineland-Palatinate: a stomach content analysis. Eur J Wildl Res 51:263–270CrossRefGoogle Scholar
- Hrynkiewicz K, Haug I, Baum C (2007) Ectomycorrhizal community structure under willows at former ore mining sites. Eur J Soil Biol 44:37–44CrossRefGoogle Scholar
- Huang PM (2008) Impacts of physicochemical-biological interactions on metal and metalloid transformations in soils: an overview. In: Violante A, Huang PM, Gadd GM (eds) Biophysico-chemical processes of heavy metals and metalloids in soil environments. Wiley, Hoboken, NJ, pp 3–52Google Scholar
- Jamnická G, Bučinová K, Havranová I, Urban A (2007) Current state of mineral nutrition and risk elements in a beech ecosystem situated near the aluminium smelter in Žiar nad Hronom, Central Slovakia. For Ecol Manage 248:26–35CrossRefGoogle Scholar
- Jentschke G, Godbold DL (2000) Metal toxicity and ectomycorrhizas. Physiol Plant 109:107–116CrossRefGoogle Scholar
- 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
- Jongmans AG, van Breemen N, Lundstrom U, van Hees PAW, Finlay RD, Srinivasan M, Unestam T, Giesler R, Melkerud P, Olsson M (1997) Rock-eating fungi. Nature 389:682–683CrossRefGoogle Scholar
- Kalač P, Svoboda L (2000) A review of trace element concentrations in edible mushrooms. Food Chem 69:273–281CrossRefGoogle Scholar
- Kapoor A, Viraraghavan T (1997) Heavy metal biosorption sites in Aspergillus niger. Bioresour Technol 61:221–227CrossRefGoogle Scholar
- Kayama M, Choi D, Tobita H, Utsugi H, Kitao M, Maruyama Y, Nomura M, Koike T (2006) Comparison of growth characteristics and tolerance to serpentine soil of three ectomycorrhizal spruce seedlings in northern Japan. Trees 20:430–440CrossRefGoogle Scholar
- Kennedy PJ, Vashisht AA, Hoe K, Kim D, Park H, Hayles J, Russell P (2008) A genome-wide screen of genes involved in cadmium tolerance in Schizosaccharomyces pombe. Toxicol Sci 106:124–139PubMedCrossRefGoogle Scholar
- Kiefer P, Pröhl G, Müller H, Lindner G, Drissner J, Zibold G (1996) Factors affecting the transfer of radiocaesium from soil to roe deer in forest ecosystems of Southern Germany. Sci Total Environ 192:49–61PubMedCrossRefGoogle Scholar
- Koide RT, Wu T (2003) Ectomycorrhizas and retarded decomposition in a Pinus resinosa plantation. New Phytol 158:401–407CrossRefGoogle Scholar
- Kozdroj J, Piotrowska-Seget Z, Krupa P (2007) Mycorrhizal fungi and ectomycorrhiza associated bacteria isolated from an industrial desert soil protect pine seedlings against Cd (II) impact. Ecotoxicology 16:449–456PubMedCrossRefGoogle Scholar
- Krpata D, Peintner U, Langer I, Fitz WJ, Schweiger P (2008) Ectomycorrhizal communities associated with Populus tremula growing on a heavy metal contaminated site. Mycol Res 112:1069–1079PubMedCrossRefGoogle Scholar
- Krpata D, Fitz W, Peintner U, Langer I, Schweiger P (2009) Bioconcentration of zinc and cadmium in ectomycorrhizal fungi and associated aspen trees as affected by level of pollution. Environ Pollut 157:280–286PubMedCrossRefGoogle Scholar
- Krznaric E, Verbruggen N, Wevers JH, Carleer R, Vangronsveld J, Colpaert JV (2009) Cd-tolerant Suillus luteus: a fungal insurance for pines exposed to Cd. Environ Pollut 157:1581–1588PubMedCrossRefGoogle Scholar
- 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
- Langer I, Krpata D, Fitz WJ, Wenzel WW, Schweiger PF (2009) Zinc accumulation potential and toxicity threshold determined for a metal-accumulating Populus canescens clone in a dose-response study. Environ Pollut 157:2871–2877PubMedCrossRefGoogle Scholar
- Leyval C, Turnau K, Haselwandter K (1997) Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza 7:139–153CrossRefGoogle Scholar
- Lin H, Kumanovics A, Nelson JM, Warner DE, Ward DM, Kaplan J (2008) A single amino acid change in the yeast vacuolar metal transporters Zrc1 and Cot1 alters their substrate specificity. J Biol Chem 283:33865–33873PubMedCrossRefGoogle Scholar
- Lindahl BD, Stenlid J, Finlay R (2001) Effects of resource availability on mycelial interactions and 32P transfer between a saprotrophic and an ectomycorrhizal fungus in soil microcosms. FEMS Microbiol Ecol 38:43–52CrossRefGoogle Scholar
- Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Högberg P, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173:611–620PubMedCrossRefGoogle Scholar
- Markkola AM, Ahonen-Jonnarth U, Roitto M, Strömmer R, Hyvärinen M (2002) Shift in ectomycorrhizal community composition in Scots pine (Pinus sylvestris L.) seedling roots as a response to nickel deposition and removal of lichen cover. Environ Pollut 120:797–803PubMedGoogle Scholar
- Martino E, Perotto 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 35:133–141CrossRefGoogle Scholar
- Meharg A (2003) The mechanistic basis of interactions between mycorrhizal associations and toxic metal cations. Mycol Res 107:1253–1265PubMedCrossRefGoogle Scholar
- Melgar MJ, Alonso J, Garcia MA (2009) Mercury in edible mushrooms and underlying soil: bioconcentration factors and toxicological risk. Sci Total Environ 407:5328–5334PubMedCrossRefGoogle Scholar
- Mleczko P (2004) Mycorrhizal and saprobic macrofungi of two zinc wastes in southern Poland. Acta Biol Crac Ser Bot 46:25–38Google Scholar
- Moser AM, Frank JL, D’Allura JA, Southworth D (2008) Ectomycorrhizal communities of Quercus garryana are similar on serpentine and nonserpentine soils. Plant Soil 315:185–194CrossRefGoogle Scholar
- Muller LAH, Lambaerts M, Vangronsveld J, Colpaert JV (2004) AFLP-based assessment of the effects of environmental heavy metal pollution on the genetic structure of pioneer populations of Suillus luteus. New Phytol 164:297–303CrossRefGoogle Scholar
- Muller LAH, Vangronsveld J, Colpaert JV (2007) Genetic structure of Suillus luteus populations in heavy metal polluted and nonpolluted habitats. Mol Ecol 16:4728–4737PubMedCrossRefGoogle Scholar
- Mutanen M (1986) Bioavailability of selenium in mushrooms, Boletus edulis, to young women. Int J Vitam Nutr Res 56:297–301PubMedGoogle Scholar
- Oline DK, Mitton JB, Grant MC (2000) Population and subspecific genetic differentiation in the Foxtail pine (Pinus balfouriana). Evolution 54:1813–1819PubMedGoogle Scholar
- Ott T, Fritz E, Polle A, Schützendübel A (2002) Characterisation of antioxidative systems in the ectomycorrhiza-building basidiomycete Paxillus involutus (Bartsch) Fr. and its reaction to cadmium. FEMS Microbiol Ecol 42:359–366PubMedCrossRefGoogle Scholar
- Pacyna JM, Pacyna EG (2001) An assessment of global and regional emissions of trace metals to the atmosphere from anthropogenic sources worldwide. Environ Rev 9:269–298CrossRefGoogle Scholar
- Panaccione DG, Sheets NL, Miller SP, Cumming JR (2001) Diversity of Cenococcum geophilum isolates from serpentine and non-serpentine soils. Mycologia 93:645–652CrossRefGoogle Scholar
- Pokorny B, Al Sayegh-Petkovšek S, Ribarič-Lasnik C, Vrtačnik J, Doganoc DZ, Adamič M (2004) Fungi ingestion as an important factor influencing heavy metal intake in roe deer: evidence from faeces. Sci Total Environ 324:223–234PubMedCrossRefGoogle Scholar
- Ramesh G, Podila GK, Gay G, Marmeisse R, Reddy MS (2009) Different patterns of regulation for the copper and cadmium metallothioneins of the ectomycorrhizal fungus Hebeloma cylindrosporum. Appl Environ Microbiol 75:2266–2274PubMedCrossRefGoogle Scholar
- Rosling A, Roose T, Herrmann AM, Davidson FA, Finlay RD, Gadd GM (2009) Approaches to modelling mineral weathering by fungi. Fungal Biol Rev 23:138–144. Available at: http://linkinghub.elsevier.com/retrieve/pii/S1749461309000207.Google Scholar
- Rühling Å, 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
- Rühling Å, Bååth E, Nordgren A, Söderström B (1984) Fungi in metal-contaminated soil near the Gusum Brass Mill, Sweden. Ambio 13:34–36Google Scholar
- Scheid S, Günthardt-Georg MS, Schulin R, Nowack B (2009) Accumulation and solubility of metals during leaf litter decomposition in non-polluted and polluted soil. Eur J Soil Sci 60:613–621CrossRefGoogle Scholar
- Schramm JR (1966) Plant Colonization Studies on Black Wastes from Anthracite Mining in Pennsylvania. American Philosophical Society. Available at: http://www.jstor.org/stable/1006024. Accessed 3 Dec 2009
- Serafín Muñoz AH, Kubachka K, Wrobel K, Gutierrez Corona JF, Yathavakilla SKV, Caruso JA, Wrobel K (2006) Se-enriched mycelia of Pleurotus ostreatus: distribution of selenium in cell walls and cell membranes/cytosol. J Agric Food Chem 54:3440–3444PubMedCrossRefGoogle Scholar
- Serafín Muñoz AH, Wrobel K, Gutierrez Corona JF, Wrobel K (2007) The protective effect of selenium inorganic forms against cadmium and silver toxicity in mycelia of Pleurotus ostreatus. Mycol Res 111:626–632PubMedCrossRefGoogle Scholar
- Slejkovec Z, Byrne AR, Stijve T, Goessler W, Irgolic KJ (1997) Arsenic compounds in higher fungi. Appl Organomet Chem 11:673–682CrossRefGoogle Scholar
- Smits MM, Hoffland E (2009) Possible role of ectomycorrhizal fungi in cycling of aluminium in podzols. Soil Biol Biochem 41:491–497CrossRefGoogle Scholar
- Smits MM, Hoffland E, Jongmans AG, van Breemen N (2005) Contribution of mineral tunneling to total feldspar weathering. Geoderma 125:59–69CrossRefGoogle Scholar
- 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
- Stijve T, Vellinga E, Herrmann A (1990) Arsenic accumulation in some higher fungi. Persoonia 14:161–166Google Scholar
- Svoboda L, Havlícková B, Kalac P (2006) Contents of cadmium, mercury and lead in edible mushrooms growing in a historical silver-mining area. Food Chem 96:580–585CrossRefGoogle Scholar
- Tahara K, Norisada M, Tange T, Yagi H, Kojima K (2005) Ectomycorrhizal association enhances Al tolerance by inducing citrate secretion in Pinus densiflora. Soil Sci Plant Nutr 51:397–403CrossRefGoogle Scholar
- Turnau K, Kottke I, Dexheimer J (1996) Toxic element filtering in Rhizopogon roseolus/Pinus sylvestris mycorrhizas collected from calamine dumps. Mycol Res 100:16–22CrossRefGoogle Scholar
- Turnau K, Przybylowicz WJ, Mesjasz-Przybylowicz J (2001) Heavy metal distribution in Suillus luteus mycorrhizas – as revealed by micro-PIXE analysis. Nucl Instrum Methods Phys Res Sect B 181:649–658CrossRefGoogle Scholar
- Urban A, Puschenreiter M, Strauss J, Gorfer M (2008) Diversity and structure of ectomycorrhizal and co-associated fungal communities in a serpentine soil. Mycorrhiza 18:339–354PubMedCrossRefGoogle Scholar
- van Breemen N, Finlay R, Lundström U, Jongmans AG, Giesler R, Olsson M (2000) Mycorrhizal weathering: a true case of mineral plant nutrition? Biogeochemistry 49:53–67CrossRefGoogle Scholar
- van Hees PA, Jones DL, Finlay R, Godbold DL, Lundström US (2005) The carbon we do not see – the impact of low molecular weight compounds on carbon dynamics and respiration in forest soils: a review. Soil Biol Biochem 37:1–13CrossRefGoogle Scholar
- van Schöll LV, Smits MM, Hoffland E (2006) Ectomycorrhizal weathering of the soil minerals muscovite and hornblende. New Phytol 171:805–814PubMedCrossRefGoogle Scholar
- van Schöll LV, Kuyper T, Smits M, Landeweert R, Hoffland E, Breemen N (2008) Rock-eating mycorrhizas: their role in plant nutrition and biogeochemical cycles. Plant Soil 303:35–47CrossRefGoogle Scholar
- Vralstad 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
- Wallander H, Mahmood S, Hagerberg D, Johansson L, Pallon J (2003) Elemental composition of ectomycorrhizal mycelia identified by PCR-RFLP analysis and grown in contact with apatite or wood ash in forest soil. FEMS Microbiol Ecol 44:57–65PubMedGoogle Scholar
- Wedepohl H (1995) The composition of the continental crust. Geochim Cosmochim Acta 59:1217–1232CrossRefGoogle Scholar
- Wilkinson DM, Dickinson NM (1995) Metal resistance in trees: the role of mycorrhizae. Oikos 72:298–300CrossRefGoogle Scholar
- Wright J (2007) Local adaptation to serpentine soils in Pinus ponderosa. Plant Soil 293:209–217CrossRefGoogle Scholar