Plant and Soil

, Volume 303, Issue 1–2, pp 35–47 | Cite as

Rock-eating mycorrhizas: their role in plant nutrition and biogeochemical cycles

  • Laura van Schöll
  • Thomas W. Kuyper
  • Mark M. Smits
  • Renske Landeweert
  • Ellis Hoffland
  • Nico van Breemen


A decade ago, tunnels inside mineral grains were found that were likely formed by hyphae of ectomycorrhizal (EcM) fungi. This observation implied that EcM fungi can dissolve mineral grains. The observation raised several questions on the ecology of these “rock-eating” fungi. This review addresses the roles of these rock-eating EcM associations in plant nutrition, biogeochemical cycles and pedogenesis. Research approaches ranged from molecular to ecosystem level scales. Nutrient deficiencies change EcM seedling exudation patterns of organic anions and thus their potential to mobilise base cations from minerals. This response was fungal species-specific. Some EcM fungi accelerated mineral weathering. While mineral weathering could also increase the concentrations of phytotoxic aluminium in the soil solution, some EcM fungi increase Al tolerance through an enhanced exudation of oxalate. Through their contribution to Al transport, EcM hyphae could be agents in pedogenesis, especially podzolisation. A modelling study indicated that mineral tunnelling is less important than surface weathering by EcM fungi. With both processes taken together, the contribution of EcM fungi to weathering may be significant. In the field vertical niche differentiation of EcM fungi was shown for EcM root tips and extraradical mycelium. In the field EcM fungi and tunnel densities were correlated. Our results support a role of rock-eating EcM fungi in plant nutrition and biogeochemical cycles. EcM fungal species-specific differences indicate the need for further research with regard to this variation in functional traits.


Aluminium Base cations Ectomycorrhiza Hyphae Organic anions Podzol Weathering 


  1. Ahonen JU, Van Hees PAW, Lundström 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
  2. Arocena JM, Göttlein A, Raidl S (2004) Spatial changes of soil solution and mineral composition in the rhizosphere of Norway-spruce seedlings colonized by Piloderma croceum. J Plant Nutr Soil Sci 167:479–486CrossRefGoogle Scholar
  3. Arvieu C, Leprince F, Plassard C (2003) Release of oxalate and protons by ectomycorrhizal fungi in response to P-deficiency and calcium carbonate in nutrient solution. Ann For Sci 60:815–821CrossRefGoogle Scholar
  4. 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 48:75–92CrossRefGoogle Scholar
  5. Bending GD, Read DJ (1995) The structure and function of the vegetative mycelium of ectomycorrhizal plants: V. Foraging behaviour and translocation of nutrients from exploited litter. New Phytol 130:401–409CrossRefGoogle Scholar
  6. Brandes B, Godbold DL, Kuhn AJ, Jentschke G (1998) Nitrogen and phosphorus acquisition by the mycelium of the ectomycorrhizal fungus Paxillus involutus and its effect on host nutrition. New Phytol 140:735–743CrossRefGoogle Scholar
  7. Casarin V, Plassard C, Souche G, Arvieu JC (2003) Quantification of oxalate ions and protons released by ectomycorrhizal fungi in rhizosphere soil. Agronomie 23:461–469CrossRefGoogle Scholar
  8. Cumming JR, Weinstein LH (1990a) Aluminum-mycorrhizal interactions in the physiology of pitch pine seedlings. Plant Soil 125:7–18CrossRefGoogle Scholar
  9. Cumming JR, Weinstein LH (1990b) Utilization of aluminum phosphate as a phosphorus source by ectomycorrhizal Pinus rigida Mill. seedlings. New Phytol 116:99–106CrossRefGoogle Scholar
  10. Dickie IA, Xu B, Koide RT (2002) Vertical niche differentiation of ectomycorrhizal hyphae in soil as shown by T-RFLP analysis. New Phytol 156:527–535CrossRefGoogle Scholar
  11. Ericsson T (1995) Growth and shoot–root ratio of seedlings in relation to nutrient availability. Plant Soil 168:205–214CrossRefGoogle Scholar
  12. Finlay RD (1995) Interactions between soil acidification, plant growth and nutrient uptake in ectomycorrhizal associations of forest trees. Ecol Bull 44:197–214Google Scholar
  13. Fox TR, Comerford NB, Mcfee WW (1990) Phosphorus and aluminum release from a spodic horizon mediated by organic acids. Soil Sci Soc Am J 54:1763–1767CrossRefGoogle Scholar
  14. Fransson AM, Valeur I, Wallander H (2004) The wood-decaying fungus Hygrophoropsis aurantiaca increases P availability in acid forest humus soil, while N addition hampers this effect. Soil Biol Biochem 36:1699–1705CrossRefGoogle Scholar
  15. Fries N (1980) Intersterility groups in Paxillus involutus. Mycotaxon 24:403–409Google Scholar
  16. Gadd GM (2007) Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol Res 111:3–49PubMedCrossRefGoogle Scholar
  17. Genney DR, Anderson IA, Alexander IJ (2006) Fine-scale distribution of pine ectomycorrhizas and their extramatrical mycelium. New Phytol 170:381–390PubMedCrossRefGoogle Scholar
  18. Gorbushina AA (2007) Life on the rocks. Environ Microbiol 9:1613–1631PubMedCrossRefGoogle Scholar
  19. Giesler R, Högberg M, Högberg P (1998) Soil chemistry and plants in Fennoscandian boreal forest as exemplified by a local gradient. Ecology 79:119–137CrossRefGoogle Scholar
  20. Giesler R, Ilvesniemi H, Nyberg L, Van Hees PAW, Starr M, Bishop K, Kareinen T, Lundström US (2000) Distribution and mobilization of Al, Fe and Si in three podzolic soil profiles in relation to the humus layer. Geoderma 94:249–263CrossRefGoogle Scholar
  21. Glowa KR, Arocena JM, Masssicotte HB (2003) Extraction of potassium and/or magnesium from selected soil minerals by Piloderma. Geomicrobiol J 20:99–111CrossRefGoogle Scholar
  22. 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 1:57–74CrossRefGoogle Scholar
  23. Griffiths RP, Baham JE, Caldwell BA (1994) Soil solution chemistry of ectomycorrhizal mats in forest soil. Soil Biol Biochem 26:331–337CrossRefGoogle Scholar
  24. Haselwandter K, Winkelmann G (2002) Ferricrocin: An ectomycorrhizal siderophore of Cenococcum geophilum. Biometals 15:73–77PubMedCrossRefGoogle Scholar
  25. 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 259:111–121CrossRefGoogle Scholar
  26. 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 12:379–390PubMedGoogle Scholar
  27. Hobbie EA (2006) Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. Ecology 87:563–569PubMedCrossRefGoogle Scholar
  28. Hoffland E, Giesler R, Jongmans T, Van Breemen N (2002) Increasing feldspar tunneling by fungi across a North Sweden podzol chronosequence. Ecosystems 5:11–22CrossRefGoogle Scholar
  29. Hoffland E, Giesler R, Jongmans AG, Van Breemen N (2003) Feldspar tunneling by fungi along natural productivity gradients. Ecosystems 6:739–746CrossRefGoogle Scholar
  30. Hoffland E, Kuyper TW, Wallander H, Plassard C, Gorbushina AA, Haselwandter 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 2:258–264CrossRefGoogle Scholar
  31. Hoffland E, Smits MM, Van Schöll L, Landeweert R (2005) Rock-eating mycorrhizas: 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 (eds) Plant nutrition for food security, human health and environmental protection, Beijing, pp 802–803.Google Scholar
  32. Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Löfvenius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792PubMedCrossRefGoogle Scholar
  33. Holmström SJM, Lundström US, Finlay RD, Van Hees PAW (2004) Siderophores in forest soil solution. Biogeochemistry 71:247–258CrossRefGoogle Scholar
  34. Jentschke G, Brandes B, Kuhn AJ, Schröder WH, Becker JS, Godbold DL (2000) The mycorrhizal fungus Paxillus involutus transports magnesium to Norway spruce seedlings. Evidence from stable isotope labeling. Plant Soil 220:243–246CrossRefGoogle Scholar
  35. 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 149:327–337CrossRefGoogle Scholar
  36. 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 389:682–683CrossRefGoogle Scholar
  37. Kinraide TB (1991) Identity of the rhizotoxic aluminum species. Plant Soil 134:167–178Google Scholar
  38. Kinraide TB (2003) Toxicity factors in acidic forest soils: attempts to evaluate separately the toxic effects of excessive Al3 + and H + and insufficient Ca2 + and Mg2 + upon root elongation. Eur J Soil Sci 54:323–333CrossRefGoogle Scholar
  39. Kjøller R (2006) Disproportionate abundance between ectomycorrhizal root tips and their associated mycelia. FEMS Microbiol Ecol 58:214–224PubMedCrossRefGoogle Scholar
  40. 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 55:459–493CrossRefGoogle Scholar
  41. Laiho O (1970) Paxillus involutus as a mycorrhizal symbiont of forest trees. Acta For Fenn 106:5–72Google Scholar
  42. 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
  43. Landeweert R, Leeflang P, Kuyper TW, Hoffland E, Rosling A, Wernars K, Smit E (2003a) Molecular identification of ectomycorrhizal mycelium in soil horizons. Appl Environ Microbiol 69:327–333PubMedCrossRefGoogle Scholar
  44. Landeweert R, Veenman C, Kuyper TW, Fritze H, Wernars K, Smit E (2003b) Quantification of ectomycorrhizal mycelium in soil by real-time PCR compared to conventional quantification techniques. FEMS Microbiol Ecol 45:283–292CrossRefPubMedGoogle Scholar
  45. 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 (eds) Magnesium deficiency in forest ecosystems. Kluwer, DordrechtGoogle Scholar
  46. 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 173:611–602PubMedCrossRefGoogle Scholar
  47. Lundström US, Van Breemen N, Bain D (2000) The podzolization process. A review. Geoderma 94:91–107CrossRefGoogle Scholar
  48. Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278PubMedCrossRefGoogle Scholar
  49. 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 194:241–246CrossRefGoogle Scholar
  50. 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
  51. Paris F, Botton B, Lapeyrie F (1996) In vitro weathering of phlogopite by ectomycorrhizal fungi 2. Effect of K+ and Mg2+ deficiency and N sources on accumulation of oxalate and H+. Plant Soil 179:141–50CrossRefGoogle Scholar
  52. Peintner U, Iotti M, Klotz P, Bonuso E, Zambonelli A (2007) Soil fungal communities in a Castanea sativa (chestnut forest producing large quantities of Boletus edulis sensu lato (porcini): where is the mycelium of porcini? Environ Microbiol 9:880–889PubMedCrossRefGoogle Scholar
  53. Read DJ, Leake JR, Perez-Moreno J (2004) Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes. Can J Bot 82:1243–1263CrossRefGoogle Scholar
  54. 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 159:775–783CrossRefGoogle Scholar
  55. Rosling A, Lindahl BD, Finlay RD (2004) Carbon allocation to ectomycorrhizal roots and mycelium colonising different mineral substrates. New Phytol 162:795–802CrossRefGoogle Scholar
  56. Rudawska M, Leski T (1998) Aluminium tolerance of different Paxillus involutus Fr. strains originating from polluted and nonpolluted sites. Acta Soc Bot Pol 67:115–122Google Scholar
  57. Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol 52:527–560PubMedCrossRefGoogle Scholar
  58. 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 25:1252–1262CrossRefGoogle Scholar
  59. Schier GA, McQuattie CJ (1996) Response of ectomycorrhizal and nonmycorrhizal pitch pine (Pinus rigida) seedlings to nutrient supply and aluminum: Growth and mineral nutrition. Can J For Res 26:2145–2152Google Scholar
  60. Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd ed. Academic, San DiegoGoogle Scholar
  61. Smits MM (2005) Ectomycorrhizal fungi and biogeochemical cycles of boreal forests. Ph.D. thesis, Wageningen University.
  62. Smits MM (2006) Mineral tunneling by fungi. In: Gadd GM (ed) Fungi in biogeochemical cycles. Cambridge University Press, Cambridge, UK, pp 311–327Google Scholar
  63. Smits MM, Hoffland E, Van Breemen N (2005) Contribution of mineral tunneling to total feldspar weathering. Geoderma 125:59–69CrossRefGoogle Scholar
  64. Sverdrup H, Hagen-Thorn A, Holmqvist J, Wallman P, Warfvinge P, Walse C, Alveteg M (2002) Biogeochemical processes and mechanisms. In: Sverdrup H, Stjernquist I (eds) Developing principles and models for sustainable forestry in Sweden. Kluwer, Dordrecht, pp 91–196Google Scholar
  65. Thelin G (2000) Nutrient imbalance in Norway spruce. Ph.D. thesis, Lund UniversityGoogle Scholar
  66. Toljander JF, Eberhardt U, Toljander YK, Paul LR, Taylor AFS (2006) Species composition of an ectomycorrhizal fungal community along a local nutrient gradient in a boreal forest. New Phytol 170:873–884PubMedCrossRefGoogle Scholar
  67. Übel E, Heinsdorf D (1997) Results of long-term K and Mg fertilizer experiments in afforestation. For Ecol Manag 91:47–52CrossRefGoogle Scholar
  68. Van Breemen N, Finlay RD, Lundström US, Jongmans AG, Giesler R, Melkerud PA (2000a) Mycorrhizal weathering: a true case of mineral plant nutrition? Biogeochemistry 49:53–67CrossRefGoogle Scholar
  69. Van Breemen N, Lundström US, Jongmans AG (2000b) Do plants drive podzolization via rock-eating mycorrhizal fungi? Geoderma 94:163–171CrossRefGoogle Scholar
  70. Van Hees PAW, Godbold DL, Jentschke G, Jones DL (2003) Impact of ectomycorhizas on the concentration and biodegradation of simple organic acids in a forest soil. Eur J Soil Sci 54:697–706CrossRefGoogle Scholar
  71. 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 55:101–111CrossRefGoogle Scholar
  72. Van Hees PAW, Jones DL, Nyberg L, Holmström SJM, Godbold DL, Lundström US (2005) Modelling low molecular weight organic acid dynamics in forest soils. Soil Biol Biochem 37:517–531CrossRefGoogle Scholar
  73. Van Hees PAW, Rosling A, Finlay RD (2006a) The impact of trees, ectomycorrhiza and potassium availability on simple organic compounds and dissolved organic carbon in soil. Soil Biol Biochem 38:1912–1923CrossRefGoogle Scholar
  74. Van Hees PAW, Rosling A, Lundström US, Finlay RD (2006b) The biogeochemical impact of ectomycorrhizal conifers on major soil elements (Al, Fe, K and Si). Geoderma 136:364–377CrossRefGoogle Scholar
  75. Van Hees PAW, Rosling A, Essen S, Godbold DL, Jones DL, Finlay RD (2006c) Oxalate and ferricrocin exudation by the extramatrical mycelium of an ectomycorrhizal fungus in symbiosis with Pinus sylvestris. New Phytol 169:367–377PubMedCrossRefGoogle Scholar
  76. Van Schöll L (2006) Ectomycorrhizal fungi and Pinus sylvestris: aluminium toxicity, base cation deficiencies and exudation of organic anions. Ph.D. thesis, Wageningen University.
  77. 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 215:352–360CrossRefGoogle Scholar
  78. 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 170:153–163PubMedCrossRefGoogle Scholar
  79. Van Schöll L, Smits MM, Hoffland E (2006b) Ectomycorrhizal weathering of the soil minerals muscovite and hornblende. New Phytol 171:805–814PubMedCrossRefGoogle Scholar
  80. Villarreal-Ruiz L, Anderson IC, Alexander IJ (2004) Interaction between an isolate from the Hymenoscyphus ericae aggregate and roots of Pinus and Vaccinium. New Phytol 164:183–192CrossRefGoogle Scholar
  81. Wallander H (2000) Uptake of P from apatite by Pinus sylvestris colonised by different ectomycorrhizal fungi. Plant Soil 218:249–256CrossRefGoogle Scholar
  82. Wallander H (2006) Mineral dissolution by ectomycorrhizal fungi. In: Gadd GM (ed) Fungi in biogeochemical cycles. Cambridge University Press, Cambridge, UK, pp 328–343Google Scholar
  83. Wallander H, Hagerberg D (2004) Do ectomycorrhizal fungi have a significant role in weathering of minerals in forest soil? Symbiosis 27:249–257Google Scholar
  84. Wright DP, Johansson T, Le Quéré A, Söderström B, Tunlid A (2005) Spatial patterns of gene expression in the extramatrical mycelium and mycorrhizal root tips formed by the ectomycorrhizal fungus Paxillus involutus in association with birch (Betula pendula) seedlings in soil microcosms. New Phytol 167:579–596PubMedCrossRefGoogle Scholar
  85. Yamaji K, Ishimoto H, Usui N, Mori S (2005) Organic acids and water-soluble phenolics produced by Paxillus sp 60/92 together show antifungal activity against Pythium vexans under acidic culture conditions. Mycorrhiza 15:17–23PubMedCrossRefGoogle Scholar
  86. Zhu Y, Cavagnaro TR, Smith SE, Dickson S (2001) Backseat driving? Accessing phosphate beyond the rhizosphere – depletion zone. Trends Pl Sci 6:194–195CrossRefGoogle Scholar

Copyright information

© The Author(s) 2007

Authors and Affiliations

  • Laura van Schöll
    • 1
    • 3
  • Thomas W. Kuyper
    • 1
  • Mark M. Smits
    • 1
    • 2
    • 4
  • Renske Landeweert
    • 1
    • 5
  • Ellis Hoffland
    • 1
  • Nico van Breemen
    • 2
  1. 1.Department of Soil QualityWageningen UniversityWageningenThe Netherlands
  2. 2.Laboratory of Soil Science and GeologyWageningen UniversityWageningenThe Netherlands
  3. 3.Nutrient Management InstituteWageningenThe Netherlands
  4. 4.Department of Animal and Plant SciencesUniversity of SheffieldSheffieldUK
  5. 5.Blgg, Mariendal 8OosterbeekThe Netherlands

Personalised recommendations