Mineral transformations by mycorrhizal fungi

Geomicrobiology Journal

Volumn 27, Issue 6-7, 2010, Pages 609-623

  Martino, Elena ^a   Perotto, Silvia ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

Metal toxicity; Mineral weathering; Mycorrhizal fungi

Indexed keywords

FUNGUS; MINERAL; MYCORRHIZA; SOLUBILIZATION; TOXICITY; WEATHERING;

FUNGI;

EID: 77956711151     PISSN: 01490451     EISSN: 15210529     Source Type: Journal    
DOI: 10.1080/01490451003702958     Document Type: Review

References (171)

1. Adeyemi AO, Gadd GM. 2005. Fungal degradation of calcium-, lead and silicon-bearing minerals. Biometals 18:269-281.
2. Adriaensen K, Van Der Lelie D, Van Laere A, Vangrosveld J, Colpaert JV. 2003. A zinc-adapted fungus protects pines from zinc stress. New Phytol 161:549-555.
3. Ahonen Jonnarth U, Göransson A, Finlay RD. 2003. Growth and nutrient uptake of ectomycorrhizal Pinus sylvestris seedlings in a natural substrate treated with elevated Al concentrations. Tree Physiol 23:157-167.
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 146:557-567.
5. Altomare C, Norvell WA, Bjorkman T, Harman GE. 1999. Solubilization of phosphates and micronutrients by the plant-growth-promoting and biocon-trol fungus Trichoderma harzianum rifai 1295-22. Appl Environ Microbiol 65:2926-2933.
6. Anderson IC, Cairney JWG. 2007. Ectomycorrhizal fungi: exploring the mycelial frontier. FEMS Microbiol Rev 31:388-406.
7. Arocena JM, Glowa KR, Massicotte HB, Lavkulich L. 1999. Chemical and mineral composition of ectomycorrhizosphere soils of subalpine fir (Abies lasiocarpa (Hook.) Nutt.) in the AE horizon of a Luvisol. Can J Soil Sci 79:25-35.
8. Arocena JM, Glowa KR. 2000. Mineral weathering in ectomycorrhizosphere of subalpine fir (Abies lasiocarpa (Hook.) Nutt.) as revealed by soil solution composition. Forest Ecol Manage 133:61-70.
9. Atwell BJ, Newsome JC. 1990. Turgor Pressure in Mechanically Impeded Lupin Roots. Aust J Plant Physiol 17:49-56.
10. Bakker MR, George E, Turpault MP, Zhang JL, Zeller B. 2004. Impact of Douglas-fir and Scots pine seedlings on plagioclase weathering under acidic conditions. Plant Soil 266:247-259.
11. Balogh-Brunstad Z, Keller CK, Gill RA, Bormann BT, Li CY. 2008. The effect of bacteria and fungi on chemical weathering and chemical denudation fluxes in pine growth experiments. Biogeochemistry 88:153-167.
12. Barcelo J, Poschenrieder C. 2002. Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: a review. Env Exp Bot 48:75-92.
13. Barea JM, Azcon R, Azcon-Aguilar C. 2002. Mycorrhizosphere interactions to improve plant fitness and soil quality. Anton van Leeuw 81:343-351.
14. Barker WW, Welch SA, Chu S, Banfield JF. 1998. Experimental observations of the effects of bacteria on aluminosilicate weathering. Am Mineral 83:1551-1563.
15. Bastmeyer M, Deising HB, Bechinger C. 2002. Force exertion in fungal infection. Ann Rev Bioph Biom Struct 31:321-341.
16. Bechinger C, Giebel K-F, Schnell M, Leiderer P, Deising HB, Bastmeyer M. 1999. Optical measurements of invasive forces exerted by appressoria of a plant pathogenic fungus. Science 285:1896-1899.
17. Bertaux J, Schmid M, Hutzler P, Hartmann A, Garbaye J, Frey-Klett P. 2005. Occurrence and distribution of endobacteria in the plant-associated mycelium of the ectomycorrhizal fungus Laccaria bicolor S238N. Environ Microbiol 7:1786-1795.
18. Bidartondo MI, Redecker D, Hijri I, Wiemken A, Bruns TD, Domínguez L, Sérsic A, Leake JR, Read DJ. 2002. Epiparasitic plants specialized on arbuscular mycorrhizal fungi. Nature 419:389-392.
19. Bidartondo MI. 2005. The evolutionary ecology of myco-heterotrophy. New Phytol 167:335-352.
20. Blum JD, Klaue A, Nezat CA, Driscoll CT, Johnson CE, Siccama TG, Eagar C, Fahey TJ, Likens GE. 2002. Mycorrhizal weathering of apatite as important calcium source in base-poor forest ecosystems. Nature 417:729-731.
21. Bonneville S, Smits MM, Brown A, Harrington J, Leake JR, Brydson R, Benning LG. 2009. Plant-driven fungal weathering: Early stages of mineral alteration at the nanometer scale. Geology 37:615-618.
22. Bradley R, Burt AJ, Read DJ. 1981. Mycorrhizal infection and resistance to heavy metal toxicity in Calluna vulgaris. Nature 292:335-337.
23. Brown MT, Wilkins DA. 1985a. Zinc tolerance of Amanita and Paxillus. Trans Brit Mycol Soc 84:367-369.
24. Brown MT, Wilkins DA. 1985b. Zinc tolerance of mycorrhizal Betula. New Phytol 99:101-106.
25. Buée M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, Martin F. 2009. 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol, doi: 10.1111/j.1469-8137.2009.03003.x.
26. Burford EP, Fomina M, Gadd GM. 2003. Fungal involvement in bioweathering and biotransformation of rocks and minerals. Mineral Mag 67:1127-1155.
27. Callot G, Mousain D, Plassard C. 1985. Concentration of calcium carbonate on the walls of fungal hyphae. Agronomie 5:143-150.
28. Calvaruso C, Turpault MP, Frey-Klett P. 2006. Root-associated bacteria contribute to mineral weathering and to mineral nutrition in trees: a budgeting analysis. Appl Environ Microbiol 72:1258-1266.
29. Calvaruso C, Turpault MP, Leclerc E, Frey-Klett P. 2007. Impact of ectomycor-rhizosphere on the functional diversity of soil bacterial and fungal communities from a forest stand in relation to nutrient mobilization processes. Microb Ecol 54:567-577.
30. Casarin V, Plassard C, Hinsinger P, Arvieu JC. 2004. Quantification of ecto-mycorrhizal fungal effects on the bioavailability and mobilization of soil P in the rhizosphere of Pinus pinaster. New Phytol 163:177-185.
31. Clark LJ, Whalley WR, Barraclough BP. 2001. Partial mechanical impedance can increase the turgor of seedling pea roots. J Exp Bot 52:167-171.
32. Colpaert JV, Muller LAH, Lambaerts M, Andriaensen K, Vangronsveld J. 2004. Evolutionary adaptation to Zn toxicity in populations of Suilloid fungi. New Phytol 162:549-559.
33. Cumming JR, Ning J. 2003. Arbuscular mycorrhizal fungi enhance aluminium resistance of broomsedge (Andropogon virginicus L.). J Exp Bot 54:1447-1459.
34. Cumming JR, Weinstein LH. 1990a. Aluminum-mycorrhizal interactions in the physiology of pitch pine seedlings. Plant Soil 125:7-18.
35. Cumming JR, Weinstein LH. 1990b. Utilization of aluminum phosphate as a phosphorus source by ectomycorrhizal Pinus rigida Mill. seedlings. New Phytol 116:99-106.
36. 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 10:2294-2301.
37. De Boer W, Folman LB, Summerbell RC, Boddy L. 2005. Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795-811.
38. Denny HJ, Wilkins DA. 1987a. Zinc tolerance in Betula spp. III. Variation in response to zinc among ectomycorrhizal associates. New Phytol 106:535-544.
39. Denny HJ, Wilkins DA. 1987b. Zinc tolerance in Betula ssp. IV. The mechanism of ectomycorrhizal amelioration of zinc toxicity. New Phytol 106:545-553.
40. Devevre O, Garbaye J, Botton B. 1996. Release of complexing organic acids by rhizosphere fungi as a factor in Norway Spruce yellowing in acidic soils. Mycol Res 100:1367-1374.
41. Duponnois R, Colombet A, Hien V, Thioulouse J. 2005. The mycorrhizal fungus Glomus intraradices and rock phosphate amendment influence plant growth and microbial activity in the rhizosphere of Acacia holosericea. Soil Biol Biochem 37:1460-1468.
42. Dutton MV, Evans CS. 1996. Oxalate productionbyfungi: Its roleinpathogenic-ity and ecology in the soil environment. Can J Microbio. 42:881-895.
43. Ek H. 1997. The influence of nitrogen fertilization on the carbon economy of Paxillus involutus in ectomycorrhizal association with Betula pendula. New Phytol 135:133-142.
44. Entry JA, Rose CL, Cromack K. 1992. Microbial biomass and nutrient concentrations in hyphal mats of the ectomycorrhizal fungus Hysterangium setchellii in a coniferous forest soil. Soil Biol Biochem 24:447-453.
45. Finlay RD. 1995. Interactions between soil acidification, plant growth and nutrient uptake in ectomycorrhizal associations of forest trees. Ecol Bull 44:197-214.
46. Finlay RD. 2004. Mycorrhizal fungi and their multifunctional roles. Mycologist 18:91-96.
47. Finlay RD. 2005. Action and interaction in the mycorrhizal hyphosphere: a re-evaluation of the role of mycorrhizal symbiosis in nutrient acquisition and plant ecology. In: BassiriRad H, editor. Nutrient acquisition by plants: an ecological perspective. Heidelberg: Springer-Verlag. P 221-276.
48. Finlay RD. 2008. Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot 59:1115-1126.
49. Finlay RD, Rosling A. 2006. Integrated nutrient cycles in forest ecosystems, the role of ectomycorrhizal fungi. In: Gadd GM, editor. Fungi in biogeochemical cycles. Cambridge: Cambridge University Press. P 28-50.
50. Fomina M, Alexander IJ, Colpaert JV, Gadd GM. 2005. Solubilization of toxic metal minerals and metal tolerance of mycorrhizal fungi. Soil Biol Biochem 37:857-866.
51. Fomina M, Alexander IJ, Hillier S, Gadd GM. 2004. Zinc phosphate and pyromorphite solubilization by soil plant-symbiotic fungi. Geomicrobiol J 21:351-366.
52. Fomina M, Charnock JM, Hillier S, Alexander IJ, Gadd GM. 2006. Zinc phosphate transformations by the Paxillus involutus/pine ectomycorrhizal association. Microb Ecol 52:322-333.
53. Frey P, Frey-Klett P, Garbaye J, Berge O, Heulin T. 1997. Metabolic and genotypic fingerprinting of fluorescent pseudomonads associated with the Douglas fir-Laccaria bicolor mycorrhizosphere. Appl Environ Microbiol 63:1852-1860.
54. Frey-Klett J, Garbaye J, Tarkka M. 2007. The mycorrhiza helper bacteria revisited. New Phytol 176:22-36.
55. Frey-Klett P, Chavatte M, Clausse ML, Courrier S, Le Roux C, Raaijmakers J, Martinotti MG, Pierrat JC, Garbaye J. 2005. Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonads. New Phytol 165:317-328.
56. Gadd GM. 1986. Fungal responses towards heavy metals. In: Herbert RA, Codd GA, editors. Microbes in Extreme Environments. London: Academic Press. P 83-110.
57. Gadd GM. 1993. Interactionsof fungi with toxic metals. New Phytol 124:25-60.
58. Gadd GM. 2001. Metal transformations. In: Gadd GM, editor. Fungi in Biore-mediation. Cambridge: Cambridge University Press. P 359-382.
59. Gadd GM. 2007. Geomycology: Biogeochemical transformations ofrocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol Res 111:3-49.
60. 2O) and the formation of calcium oxalate by different oxalic and citric acid-producing fungi. Mycol Res 103:473-481.
61. Giesler R, Högberg M, Högberg P. 1998. Soil chemistry and plants in Fennoscandian boreal forest as exemplified by a local gradient. Ecology 79:119-137.
62. Giesler R, Ilvesniemi H, Nyberg L, Van Hees PAW, Starr M, Bishop K, Kareinen T, Lundström US. 2000. Distribution and mobilizationof Al,Fe andSi in three podzolic soil profiles in relation to the humus layer. Geoderma 94:249-263.
63. Gildon A, Tinker PB. 1983. Interactions of vesicular arbuscular mycorrhizal infection and heavy metals on the development of vesicular-arbuscular mic-orrhizas. New Phytol 95:247-261.
64. Glowa KR, Arocena JM, Masssicotte HB. 2003. Extraction of potassium and/or magnesium from selected soil minerals by Piloderma. Geomicrobiol J 20:99-111.
65. Göransson A, Eldhuset T. 2001. Is the Ca + K + Mg/Al ratio in the soil solution a predictive tool for estimating forest damage? Water Air Soil Pollut Focus 1:57-74.
66. Harold FM. 2002. Force and compliance: Rethinking morphogenesis in walled cells. Fungal Gen Biol 37:271-282.
67. Haselwandter K. 2008. Structure and function of siderophores produced by mycorrhizal fungi. Mineral Mag 72:61-64.
68. Heggo A, Angle JS. 1990. Effects of vesicular-arbuscular mycorrhizal fungi on heavy metal uptake by soybeans. Soil Biol Biochem 22:856-869.
69. Heinonsalo J, Hurme KR, Sen R. 2004. Recent C-14-labelled assimilate allocation to Scots pine seedling root and mycorrhizosphere compartments developed on reconstructed podzol humus, E-and B-mineral horizons. Plant Soil 259:111-121.
70. Hendricks JJ, Mitchell RJ, Kuehn KA, Pecot SD, Sims SE. 2006. Measuring external mycelia production of ectomycorrhizal fungi in the field: the soil matrix matters. New Phytol 171:179-186.
71. Hentschel E, Godbold DL, Marschner P, Schlegel H, Jentschke G. 1993. The effect of Paxillus involutus Fr. on aluminum sensitivity of Norway spruce seedlings. Tree Physiol 12:379-390.
72. Hobbie EA. 2006. Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. Ecology 87:563-569.
73. Hoffland E, Giesler R, Jongmans T, Van Breemen N. 2002. Increasing feldspar tunneling by fungi across a North Sweden podzol chronosequence. Ecosystems 5:11-22.
74. Hoffland E, Kuyper TW, Wallander H, Plassard C, Gorbushina AA, Hasel-wandter K, Holmström S, Landeweert R, Lundström U, Rosling A, Sen R, Smits M, van Hees P, Van Breemen N. 2004. The role of fungi in weathering. Front Ecol Environ 2:258-264.
75. Hoffland E, Smits MM, Van Schöll L, Landeweert R. 2005. Rock-eating mycor-rhizas: mobilizing nutrients from minerals? In: Li CJ, Zhang FS, Doberman A, Hinsinger P, Lambers H, Li XL, Marschner P, Maene L, McGrath S, Oenema O, Peng SB, Rengel Z, Shen QR, Welch R, Von Wirén N, Yan XL, Zhu YG, editors. Plant nutrition for food security, human health and environmental protection. Beijing. P 802-803.
76. Högberg MN, Högberg P. 2002. Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phytol 154:791-795.
77. Howard DH. 2004. Iron gathering by zoopathogenic fungi. FEMS Immunol Med Microbiol 40:95-100.
78. Huntington TG. 2000. The potential for calcium depletion in forest ecosystems of southeastern United States: Review and analysis. Glob Biogeochem Cycles 14:623-638.
79. Jackson RB, Canadell J, Ehleringer JR, Mooney HA, Sala OE, Schulze ED. 1996. A global analysis of root distributions for terrestrial biomes. Oecologia 108:389-411.
80. Jentschke G, Brandes B, Kuhn AJ, Schröder WH, Godbold DL. 2001. Interdependence of phosphorus, nitrogen, potassium and magnesium translocation by the ectomycorrhizal fungus Paxillus involutus. New Phytol 149:327-337.
81. Johansson JF, Paul LR, Finlay RD. 2004. Microbial interactions in the mycorrhi-zosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 48:1-13.
82. 13CO2 pulse-labelling of upland grassland demonstrates thata rapid pathway of carbonflux from arbuscular mycorrhizal mycelia to the soil. New Phytol 153:327-334.
83. Jongmans AG, van Breemen N, Lundström US, van Hees PAW, Finlay RD, Srinivasan M, Unestam T, Giesler R, Melkerud P-A, Olsson M. 1997. Rock-eating fungi. Nature 389:682-683.
84. Jönsson U, Rosengren U, Thelin G, Nihlgard B. 2003. Acidification-induced chemical changes in coniferous forest soils in southern Sweden 1988-99. Environ Poll 123:75-83.
85. Kennedy M, Droser M, Mayer LM, Pevear D, Mrofka D. 2006. Late Precambrian oxygenation: Inception of the clay mineral factory. Science 311:1446-1449.
86. Kinraide TB. 1991. Identity of the rhizotoxic aluminum species. Plant Soil 134:167-178.
87. 2+ upon root elongation. Eur J Soil Sci 54:323-333.
88. Knox AS, Seaman JC, Mench MJ, Vangronsveld J. 2000. Remediation of metaland radionuclide-contaminated soils by in situ stabilization techniques. In: Iskandar IK, editor. Environmental Restoration of Metals-Contaminated Soil. BocaRaton, FL: Lewis Publishers. P 21-61.
89. Kochian LV, Hoekenga OA, Pinerosa MA. 2004. How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Ann Rev Plant Biol 55:459-493.
90. Kraemer SM. 2004. Iron oxide dissolution and solubility in the presence of siderophores. Aquatic Sci 66:3-18.
91. Laiho O. 1970. Paxillus involutus as a mycorrhizal symbiont of forest trees. Acta For Fenn 106:5-72.
92. Lambers H, Raven JA, Shaver GR, Smith SE. 2008. Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95-103.
93. 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.
94. Landeweert R, Leeflang P, Kuyper TW, Hoffland E, Rosling A, Wernars K, Smit E. 2003. Molecular identification of ectomycorrhizal mycelium in soil horizons. Appl Environ Microbiol 69:327-333.
95. Landmann G, Hunter IR, Hendershot W. 1997. Temporal and spatial development of magnesium deficiency in forest stands in Europe, North America and New Zealand. In: Hüttl RF, Schaaf W, editors. Magnesium deficiency in forest ecosystems. Dordrecht: Kluwer.
96. Lapeyrie F, Chilvers GA, Bhem CA. 1987. Oxalic acid synthesis by the mycor-rhizal fungus Paxillus involutus (Batsch. ex Fr.) Fr. New Phytol 106:139-146.
97. Lapeyrie F, Ranger J, Vairelles D. 1991. Phosphate-solubilizing activity of ectomycorrhizal fungi in vitro. Can J Bot 69:342-346.
98. Leake JR. 2004. Myco-heterotroph/epiparasitic plant interactions with ectomy-corrhizal and arbuscular mycorrhizal fungi. Curr Op Pl Biol 7:422-428.
99. Leyval C, Berthelin J. 1986. Comparison between the utilization of phosphorus from insoluble mineral phosphates by ectomycorrhizal fungi and rhizobac-teria. In: Gianinazzi Pearson V, Gianinazzi S, editors. Physiological and ge-netical aspects of mycorrhizae: Proceedings of the 1st European Symposium on Mycorrhizae. Dijon. Paris, France: INRA. P 345-349.
100. Leyval C, Berthelin J. 1989. Interactions between Laccaria laccata, Agrobac-terium radiobacter and beech roots: influence on P, K, Mg, and Fe mobilization from minerals and plant growth. Plant Soil 117:103-110.
101. Leyval C, Berthelin J. 1993. Rhizodeposition and net release of soluble organic compounds by pine and beech seedlings inoculated with rhizobacteria and ectomycorrhizal fungi. Biol Fertil Soils 15:259-267.
102. Lian B, Wang B, Pan M, Liu C, Teng, HH. 2007. Microbial release of potassium from K-bearing minerals by thermophilic fungus Aspergillus fumigatus. Geoch Cosmoch Acta 72:87-98.
103. Likens GE, Driscoll CT, Buso DC. 1996. Long-term effects of acid rain: Response and recovery of a forest ecosystem. Science 272:244-246.
104. López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L. 2003. The role of nutrient availability in regulating root architecture. Current Op Pl Biol, 6:280-287.
105. Lundström US, Van Breemen N, Bain D. 2000. The podzolization process. A review. Geoderma 94:91-107.
106. Ma JF, Ryan PR, Delhaize E. 2001. Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273-278.
107. 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, Secq MPO, 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 452:88-92.
108. Martino E, Cerminara S, Prandi L, Fubini B, Perotto S. 2004. Physical and biochemical interactions of soil fungi with asbestos fibers. Environ Toxicol Chem 23:938-944.
109. Martino E, Perotto S, Parsons R, Gadd GM. 2003a. Solubilization of insoluble inorganic zinc compounds by ericoid mycorrhizal fungi derived from heavy metal polluted sites. Soil Biol Biochem 35:133-141.
110. Martino E, Prandi L, Fenoglio I, Bonfante P, Perotto S, Fubini B. 2003b. Soil fungal hyphae bind and attack asbestos fibres. Angewandte ChemieInternational Edition 42:219-222.
111. Meharg AA. 2003. The mechanistic basis of interactions between mycorrhizal associations and toxic metal cations. Mycol Res 107:1253-1265.
112. Meharg AA, Cairney JWG. 2000. Co-evolution of mycorrhizal symbionts and their hosts to metal-contaminated environments. Adv Ecol Res 30:69-112.
113. Money PN. 1999. Fungus punches its way in. Science 201:332-333.
114. Moulton KL, West J, Berner RA. 2000. Solute flux and mineral mass balance approaches to the quantification of plant effects on silicate weathering. Am J Sci 300:539-570.
115. Murakami T, Utsunomiya S, Yokoyama T, Kasama T. 2003. Biotite dissolution processes and mechanisms in the laboratory and in nature: Early stage weathering environment and vermiculitization. Am Mineral 88:377-386.
116. Neilands JB. 1995. Siderophores. Structure and function of microbial iron transport compounds. J Biol Chem 270:26723-26726.
117. Newsham KK, Fitter AH, Watkinson AR. 1995. Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol Evol 10:407-411.
118. Ochs M. 1996. Influence of humified and non-humified natural organic compounds on mineral dissolution. Chem Geol 132:119-124.
119. Olsson PA, Wallander H. 1998. Interactions between ectomycorrhizal fungi and the bacterial community in soil amended with various primary minerals. FEMS Microbiol Ecol 27:195-205.
120. Palta JA, Wyn-Jones RG, Deri Tomos A. 1987. Leaf Diffusive Conductance and Tap Root Cell Turgor Pressure of Sugarbeet. Plant Cell Environm 10:735-740.
121. 2+ deficiency on phyllosilicate evolution. Plant Soil 177:191-201.
122. Paris F, Bonnaud P, Ranger J, Robert M, Lapeyrie F. 1995b. Weathering of ammonium-or calcium-saturated 2:1 phyllosilicates by ectomycorrhizal fungi in vitro. Soil Biol Biochem 27:1237-1244.
123. +. Plant Soil 179:141-50.
124. Rambelli A. 1973. The rhizosphere of mycorrhizae, p. 299-349. In: Marks GC, Kozlowski TT, editors. Ectomycorrhizae, their ecology and physiology. New York, NY: Academic Press.
125. Read DJ, Perez-Moreno J. 2003. Mycorrhizas and nutrient cycling in ecosystems-A journey towards relevance? New Phytol 157:475-492.
126. Redecker D, Kodner R, Graham LE. 2000. Glomalean fungi from the Ordovi-cian. Science 289:1920-1921.
127. 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 40:2460-2463.
128. Robert M, Berthelin J. 1986. Role of biological and biochemical factors in soil mineral weathering. In: Huang PM, Schnitzer M. editors. Interactions of Soil Minerals with Natural Organics and Microbes. SSSA special publication. 17, P 453-495.
129. Rosling A, Landeweert R, Lindahl B, Larsson KH, Kuyper TW, Taylor AFS, Finlay R. 2003. Vertical distribution of ectomycorrhizal root tips in a podzol soil profile. New Phytol 159:775-783.
130. Rosling A, Lindahl BD, Finlay RD. 2004. Carbon allocation to ectomycor-rhizal roots and mycelium colonising different mineral substrates. New Phytol 162:795-802.
131. Ryan PR, Delhaize E, Jones DL. 2001. Function and mechanism of organic anion exudation from plant roots. Ann Rev Plant Physiol Plant Mol Biol 52:527-560.
132. Sayer JA, Gadd GM. 1997. Solubilisation and transformation of insoluble metal compounds to insoluble metal oxalates by Aspergillus niger. Mycol Res 101:653-661.
133. Schier GA, McQuattie CJ. 1995. Effect of aluminum on the growth, anatomy, and nutrient content of ectomycorrhizal and nonmycorrhizal eastern white pine seedlings. Can J For Res 25:1252-1262.
134. Schier GA, McQuattie CJ. 1996. Response of ectomycorrhizal and nonmycor-rhizal pitch pine (Pinus rigida) seedlings to nutrient supply and aluminum: Growth and mineral nutrition. Can J For Res 26:2145-2152.
135. Selosse M-A, Setaro S, Glatard F, Richard F, Urcelay C, Weiss M. 2007. Sebacinales are common mycorrhizal associates of Ericaceae. New Phytol 174:864-878.
136. Smith SE, Read DJ. 2008. Mycorrhizal symbiosis. 3rd edn. Academic Press.
137. Smits MM, Bonneville S, Haward S, Leake JR. 2008. Ectomycorrhizal weathering, a matter of scale? Mineral Magaz 72:131-134.
138. Smits MM, Hoffland E, Van Breemen N.2005. Contribution of mineral tunneling to total feldspar weathering. Geoderma 125:59-69.
139. Tagu D, Marmeisse R, Baillet Y, Riviere S, Palin B, Bernardini F, Mereau A, Gay G, Balestrini R, Bonfante P, Martin F. 2002. Hydrophobins in ectomy-corrhizas: heterologous transcription of the Pisolithus HydPt-1 gene in yeast and Hebeloma cylindrosporum. Europ J Histochem 46:23-29.
140. Tamm CO, Aronsson A, Popovic B, Flower Ellis J. 1999. Optimum nutrition and nitrogen saturation in Scots pine stands. Studia Forest Sue 1999:1-126.
141. Taylor AFS, Alexander I. 2005. The ectomycorrhizal symbiosis: life in the real world. Mycologist 19:102-112.
142. Taylor LL, Leake JR, Quirk J, Hardy K, Banwart SA, Beerling DJ. 2009. Biological weathering and the long-term carbon cycle: integrating mycorrhizal evolution and function into the current paradigm. Geobiology 7:171-191.
143. Thelin G. 2000. Nutrient imbalance in Norway spruce. Ph.D. thesis, Lund University.
144. Toro M, Azcon R, Barea J. 1997. Improvement of arbuscular mycorrhizal development by inoculation of soil with phosphate-solubilizing rhizobacteria to improve rock phosphate bioavailability (32P) and nutrient cycling. Appl Environ Microbiol 63:4408-4412.
145. Übel E, Heinsdorf D.1997. Resultsof long-termKandMg fertilizer experiments in afforestation. For Ecol Manag 91:47-52.
146. Uroz S, Calvaruso C, Turpault MP, Frey-Klett P. 2009. Mineral weathering by bacteria: ecology, actors and mechanisms. Trends Microbiol 17:378-387.
147. Uroz S, Calvaruso C, Turpault MP, Pierrat JC, Mustin C, Frey-Klett P. 2007. Effect of the mycorrhizosphere on the genotypic and metabolic diversity of the bacterial communities involved in mineral weathering in a forest soil. Appl Environ Microbiol 73:3019-3027.
148. Van Breemen N, Finlay RD, Lundström U, Jongmans AG, Giesler R, Olsson M. 2000a. Mycorrhizal weathering: a true case of mineral nutrition? Biogeo-chemistry 49:53-67.
149. Van Breemen N, Lundström US, Jongmans AG. 2000b. Do plants drive pod-zolization via rock-eating mycorrhizal fungi? Geoderma 94:163-171.
150. Van Der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69-72.
151. Van Hees PAW, Godbold DL, Jentschke G, Jones DL. 2003. Impact of ectomy-corhizas on the concentration and biodegradation of simple organic acids in a forest soil. Eur J Soil Sci 54:697-706.
152. Van Hees PAW, Jones DL, Jentschke G, Godbold DL. 2004. Mobilization of aluminium, iron and silicon by Picea abies and ectomycorrhizas in a forest soil. Eur J Soil Sci 55:101-111.
153. Van Hees PAW, Rosling A, Lundström US, Finlay RD. 2006. The biogeochem-ical impact of ectomycorrhizal conifers on major soil elements (Al, Fe, K and Si). Geoderma 136:364-377.
154. Van Leerdam DM, Williams PA, Cairney JWG. 2001. Phosphate-solubilising abilities of ericoid mycorrhizal endophytes of Woolsia pungens (Epacridaceae). Austr J Bot 49:75-80.
155. Van Schöll L, Hoffland E, Van Breemen N. 2006a. Organic anion exudation by ectomycorrhizal fungi and Pinus sylvestris in response to nutrient deficiencies. New Phytol 170:153-163.
156. Van Schöll L, Keltjens WG, Hoffland E, Van Breemen N. 2005. Effect of ectomycorrhizal colonization on the uptake of Ca, Mg and Al by Pinus sylvestris under aluminium toxicity. For Ecol Manag 215:352-360.
157. Van Schöll L, Smits MM, Hoffland E. 2006b. Ectomycorrhizal weathering of the soil minerals muscovite and hornblende. New Phytol 171:805-814.
158. Van Schöll L, Kuyper TW, Smits MM, Landeweert R, Hoffland E, van Breemen N. 2008. Rock-eating mycorrhizas: their role in plant nutrition and biogeo-chemical cycles. Plant Soil 303:35-47.
159. Van Tichelen KK, Colpaert JV, Vangronsveld J. 2001. Ectomycorrhizal protection of Pinus sylvestris against copper toxicity. New Phytol 150:203-213.
160. Walker EL, Connolly EL. 2008. Time to pump iron: iron-deficiency-signaling mechanisms of higher plants. Current Op Pl Biol 11:530-535.
161. Wallander H. 2000a. Uptake of P from apatite by Pinus sylvestris seedlings colonised by different ectomycorrhizal fungi. Plant Soil 218:249-256.
162. Wallander H. 2000b. Use of strontium isotopes and foliar K content to estimate weathering of biotite induced by pine seedlings colonised by ectomycorrhizal fungi from two different soils. Plant Soil 222:215-229.
163. Wallander H. 2006. Mineral dissolution by ectomycorrhiza. In: Gadd GM, editor. Fungi in biogeochemical cycles. Cambridge: Cambridge University Press. P 681-717.
164. Wallander H, Hagerberg D. 2004. Do ectomycorrhizal fungi have a significant role in weathering of minerals in forest soil? Symbiosis 27:249-257.
165. Wallander H, Nilsson LO, Hagerberg D, Bååth E. 2001. Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field. New Phytol 151:752-760.
166. Wallander H, Wickman T, Jacks G. 1997. Apatite as a P source in mycorrhizal and non-mycorrhizal Pinus sylvestris seedlings. Plant Soil 196:123-131.
167. Wallander H, Wickman T. 1999. Biotite and microcline as potassium sources in ectomycorrhizal and non-mycorrhizal Pinus sylvestris seedlings. Mycorrhiza 9:25-32.
168. Welch SA, Ullman WJ. 1993. The effect of organic acids on plagioclase dissolution rates and stoichiometry. Geoch Cosmoch Acta 57:2725-2736.
169. Whitelaw MA. 2000. Growth promotion of plants inoculated with phosphate-solubilizing fungi. Adv Agron 69:99-151.
170. Whitelaw MA, Harden TJ, Helyar KR. 1999. Phosphate solubilization in solution culture by the soil fungus Penicillium radicum. Soil Biol Bioch 31:655-665.
171. Wosten HAB, De Vries OMH, Wessels JGH. 1993. Interfacial self-assembly of a fungal hydrophobin into a hydrophobic rodlet layer. The Plant Cell 5:1567-1574.