Mycorrhizal symbioses

  • José-Miguel Barea
  • Nuria Ferrol
  • Concepción Azcón-Aguilar
  • Rosario Azcón
Part of the Plant Ecophysiology book series (KLEC, volume 7)

The aim of this Chapter is to review and integrate current knowledge of the impact of mycorrhizal symbioses on plant functioning and adaptation with specific emphasis on P acquisition at various levels of cellular organization, from the molecular, biochemical and physiological to the whole plant. Accordingly, the available information will be structured as follows: (i) mycorrhizas as a plant strategy for P acquisition; (ii) fungal-plant integration to establish functional arbuscular mycorrhizal (AM) symbiosis; (iii) functional biology of Pi uptake by AM plants; (iv) ecological impact of AM symbiosis on plant community structure and productivity; and (v) mycorrhizosphere interactions and ecosystem P cycling.


Arbuscular Mycorrhizal Fungus Arbuscular Mycorrhizal Arbuscular Mycorrhiza Mycorrhizal Symbiosis Extraradical Mycelium 
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  1. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824–827PubMedCrossRefGoogle Scholar
  2. Alexander T, Meier R, Toth R, Weber HC (1988) Dynamics of arbuscule development and degeneration in mycorrhizas of Triticum aestivum L. and Avena sativa L. with reference to Zea mays L. New Phytol 110: 363–370CrossRefGoogle Scholar
  3. Aono T, Maldonado-Mendoza IE, Dewbre GR, Harrison MJ, Saito M (2004) Expression of alkaline phosphatase genes in arbuscular mycorrhizas. New Phytol 162: 525–534CrossRefGoogle Scholar
  4. Aristizabal C, Rivera EL, Janos DP (2004) Arbuscular mycorrhizal fungi colonize decomposing leaves of Myrica parvifolia, M. pubescens and Paepalanthus sp. Mycorrhiza 14: 221–228PubMedCrossRefGoogle Scholar
  5. Artursson V, Finlay RD, Jansson JK (2005) Combined bromodeoxyuridine immunocapture and terminal-restriction fragment length polymorphism analysis highlights differences in the active soil bacterial metagenome due to Glomus mosseae inoculation or plant species. Environ Microbiol 7: 1952–1966PubMedCrossRefGoogle Scholar
  6. Avio L, Pellegrino E, Bonari E, Giovannetti M (2006) Functional diversity of arbuscular mycorrhizal fungal isolates in relation to extraradical mycelial networks. New Phytol 172: 347–357PubMedCrossRefGoogle Scholar
  7. Awramik SM (1981) The pre-Phanerozic biosphere: Three billion years of crises and opportunities. In: Nitecki MH (ed), Biotic Crises in Ecological and Evolutionary Time. Academic, New York, pp 83–102Google Scholar
  8. Bago B, Azcón-Aguilar C (1997) Changes in the rhizospheric pH induced by arbuscular mycorrhiza formation in onion (Allium cepa L). Z Pflanz Bodenkunde 160: 333–339CrossRefGoogle Scholar
  9. Barea JM (1991) Vesicular-arbuscular mycorrhizae as modifiers of soil fertility. In: Stewart BA (ed), Advances in Soil Science. Springer, New York, pp 1–40Google Scholar
  10. Barea JM, Azcón R, Azcón-Aguilar C (2002a) Mycorrhizosphere interactions to improve plant fitness and soil quality. Anton Van Leeuwenhoek 81: 343–351CrossRefGoogle Scholar
  11. Barea JM, Gryndler M, Lemanceau P, Schüepp H, Azcón R (2002b) The rhizosphere of mycorrhizal plants. In: Gianinazzi S, Schüepp H, Barea JM, Haselwandter K (eds), Mycorrhiza Technology in Agriculture: From Genes to Bioproducts. Birkhäuser, Basel, Switzerland, pp 1–18Google Scholar
  12. Barea JM, Toro M, Orozco MO, Campos E, Azcón R (2002c) The application of isotopic (32P and 15N) dilution techniques to evaluate the interactive effect of phosphate-solubilizing rhizobacteria, mycorrhizal fungi and Rhizobium to improve the agronomic efficiency of rock phosphate for legume crops. Nutr Cycl Agroecosyst 63: 35–42CrossRefGoogle Scholar
  13. Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56: 1761–1778PubMedCrossRefGoogle Scholar
  14. Barea JM, Toro M, Azcón R (2007) The use of 32P isotopic dilution techniques to evaluate the interactive effects of phosphate-solubilizing bacteria and mycorrhizal fungi at increasing plant P availability. Plant Soil 287: 1–8Google Scholar
  15. Barghoorn ES (1974) Two billion years of prokaryotes and the emergence of eukaryotes. Taxon 23: 259Google Scholar
  16. Bécard G, Kosuta S, Tamasloukht M, Séjalon-Delmas N, Roux C (2004) Partner communication in the arbuscular mycorrhizal interaction. Can J Bot 82: 1186–1197CrossRefGoogle Scholar
  17. Benedetto A, Magurno F, Bonfante P, Lanfranco L (2005) Expression profiles of a phosphate transporter gene (GmosPT) from the endomycorrhizal fungus Glomus mosseae. Mycorrhiza 15: 620–627PubMedCrossRefGoogle Scholar
  18. Besserer A, Puech-Pages V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais JC, Roux C, Becard G, Sejalon-Delmas N (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. Plos Biol 4: 1239–1247CrossRefGoogle Scholar
  19. Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Ann Rev Plant Physiol 24: 225–252CrossRefGoogle Scholar
  20. Bolan NS, Robson AD, Barrow NJ, Aylmore LAG (1984) Specific activity of phosphorus in mycorrhizal and non-mycorrhizal plants in relation to the availability of phosphorus to plants. Soil Biol Biochem 16: 299–304CrossRefGoogle Scholar
  21. Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154: 275–304CrossRefGoogle Scholar
  22. Cardoso IM, Boddington CL, Janssen BH, Oenema O, Kuyper TW (2006) Differential access to phosphorus pools of an oxisol by mycorrhizal and nonmycorrhizal maize. Commun Soil Sci Plant Anal 37: 1537–1551CrossRefGoogle Scholar
  23. Chiou TJ, Liu H, Harrison MJ (2001) The spatial expression patterns of a phosphate transporter (MtPT1) from Medicago truncatula indicate a role in phosphate transport at the root/soil interface. Plant J 25: 281–293PubMedCrossRefGoogle Scholar
  24. Cooper KM, Tinker PB (1981) Translocation and transfer of nutrients in vesicular-arbuscular mycorrhizas. 4. Effect of environmental variables on movement of phosphorus. New Phytol 88: 327–339CrossRefGoogle Scholar
  25. Cress WA, Throneberry GO, Lindsey DL (1979) Kinetics of phosphorus absorption by mycorrhizal and non-mycorrhizal tomato roots. Plant Physiol 64: 484–487PubMedCrossRefGoogle Scholar
  26. Evans RD, Johansen JR (1999) Microbiotic crusts and ecosystem processes. Crit Rev Plant Sci 18: 183–225CrossRefGoogle Scholar
  27. Ezawa T, Saito M, Yoshida T (1995) Comparison of phosphatase localization in the intraradical hyphae of arbuscular mycorrhizal fungi, Glomus spp and Gigaspora spp. Plant Soil 176: 57–63CrossRefGoogle Scholar
  28. Ezawa T, Kuwahara S, Sakamoto K, Yoshida T, Saito M (1999) Specific inhibitor and substrate specificity of alkaline phosphatase expressed in the symbiotic phase of the arbuscular mycorrhizal fungus, Glomus etunicatum. Mycologia 91: 636–641CrossRefGoogle Scholar
  29. Ezawa T, Smith SE, Smith FA (2002) P metabolism and transport in AM fungi. Plant Soil 244: 221–230CrossRefGoogle Scholar
  30. Ferrol N, Barea JM, Azcón-Aguilar C (2000a) Molecular approaches to study plasma membrane H + -ATPases in arbuscular mycorrhizas. Plant Soil 226: 219–225CrossRefGoogle Scholar
  31. Ferrol N, Barea JM, Azcón-Aguilar C (2000b) The plasma membrane H + -ATPase gene family in the arbuscular mycorrhizal fungus Glomus mosseae. Curr Genet 37: 112–118PubMedCrossRefGoogle Scholar
  32. Ferrol N, Pozo MJ, Antelo M, Azcón-Aguilar C (2002) Arbuscular mycorrhizal symbiosis regulates plasma membrane H + -ATPase gene expression in tomato plants. J Exp Bot 53: 1683–1687PubMedCrossRefGoogle Scholar
  33. Garbaye J (1994) Helper bacteria, a new dimension to the mycorrhizal symbiosis. New Phytol 128: 197–210CrossRefGoogle Scholar
  34. Gehrig H, Schussler A, Kluge M (1996) Geosiphon pyriforme, a fungus forming endocytobiosis with Nostoc (Cyanobacteria), is an ancestral member of the Glomales: evidence by SSU rRNA analysis. J Mol Evol 43: 71–81PubMedCrossRefGoogle Scholar
  35. Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17: 3489–3499PubMedCrossRefGoogle Scholar
  36. George TS, Richardson AE (2008) Potential and limitations to improving crops for enhanced phosphorus utilization. In: White PJ, Hammond JP (eds), The Ecophysiology of Plant-Phosphorus Interactions. Springer, Dordrecht, The Netherlands, pp 247–270CrossRefGoogle Scholar
  37. Gianinazzi S, Schüepp H, Barea JM, Haselwandter K (2002) (eds) Mycorrhizal Technology in Agriculture: From Genes to Bioproducts. Birkhäuser, Basel, SwitzerlandGoogle Scholar
  38. Gianinazzi-Pearson V, Gianinazzi S (1988) Morphological integration and functional compatibility between symbionts in vesicular-arbuscular endomycorrhizal associations. In: Scannerini S, Smith DC, Bonfante-Fasolo P, Gianinazzi-Pearson V (eds), Cell to Cell Signals in Plant, Animal and Microbial Symbiosis. NATO ASI, Series H, Cell Biology, Springer, Berlin, pp 73–84Google Scholar
  39. Gianinazzi-Pearson V, Arnould C, Oufattole M, Arango M, Gianinazzi S (2000) Differential activation of H + -ATPase genes by an arbuscular mycorrhizal fungus in root cells of transgenic tobacco. Planta 211: 609–613PubMedCrossRefGoogle Scholar
  40. Glick BR, Karaturovic DM, Newell PC (1995) A novel procedure for rapid isolation of plant-growth promoting pseudomonads. Can J Microbiol 41: 533–536CrossRefGoogle Scholar
  41. Grime JP, Mackey JML, Hillier SH, Read DJ (1987) Floristic diversity in a model system using experimental microcosms. Nature 328: 420–422CrossRefGoogle Scholar
  42. Gryndler M (2000) Interactions of arbuscular mycorrhizal fungi with other soil organisms. In: Kapulnik Y, Douds DDJ (eds), Arbuscular Mycorrhizas: Physiology and Function. Kluwer, Dordrecht, The Netherlands, pp 239–262Google Scholar
  43. Harley JL, Smith SE (1983) Mycorrhizal Symbiosis. Academic, New YorkGoogle Scholar
  44. Harrison MJ, Dewbre GR, Liu JY (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14: 2413–2429PubMedCrossRefGoogle Scholar
  45. Harrison MJ, Vanbuuren ML (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378: 626–629PubMedCrossRefGoogle Scholar
  46. Hart M, Klironomos JN (2002) Diversity of arbuscular mycorrhizal fungi and ecosystem functioning. In: van der Heijden MGA, Sanders IR (eds), Mycorrhizal Ecology. Springer, Berlin/Heidelberg/New York, p 242Google Scholar
  47. Hartnett DC, Wilson GWT (1999) Mycorrhizae influence plant community structure and diversity in tallgrass prairie. Ecology 80: 1187–1195CrossRefGoogle Scholar
  48. Jakobsen I (2004) Hyphal fusion to plant species connections-giant mycelia and community nutrient flow. New Phytol 164: 4–7CrossRefGoogle Scholar
  49. Jakobsen I, Abbott LK, Robson AD (1992a) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 1. Spread of hyphae and phosphorus inflow into roots. New Phytol 120: 371–380CrossRefGoogle Scholar
  50. Jakobsen I, Abbott LK, Robson AD (1992b) External hyphae of vesicular arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 2. Hyphal transport of 32P over defined distances. New Phytol 120: 509–516CrossRefGoogle Scholar
  51. Jakobsen I, Gazey C, Abbott IK (2001) Phosphate transport by communities of arbuscular mycorrhizal fungi in intact soil cores. New Phytol 149: 95–103CrossRefGoogle Scholar
  52. Janos DP (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17: 75–91PubMedCrossRefGoogle Scholar
  53. Javot H, Pumplin N, Harrison MJ (2007) Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ 30: 310–322PubMedCrossRefGoogle Scholar
  54. Jeffries P, Barea JM (2001) Arbuscular mycorrhiza - a key component of sustainable plant-soil ecosystems. In: Hock B (ed), The Mycota. Vol. IX. Fungal Associations. Springer, Berlin/Heidelberg/New York, pp 95–113Google Scholar
  55. Jeffries P, Gianinazzi S, Perotto S, Turnau K, Barea JM (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils 37: 1–16Google Scholar
  56. Johansson JF, Paul LR, Finlay RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 48: 1–13CrossRefPubMedGoogle Scholar
  57. Joner EJ, Johansen A (2000) Phosphatase activity of external hyphae of two arbuscular mycorrhizal fungi. Mycol Res 104: 81–86CrossRefGoogle Scholar
  58. Joner EJ, Ravnskov S, Jakobsen I (2000) Arbuscular mycorrhizal phosphate transport under monoxenic conditions using radio-labelled inorganic and organic phosphate. Biotechnol Lett 22: 1705–1708CrossRefGoogle Scholar
  59. Kapulnik Y, Douds DDJ (2000) (eds) Arbuscular Mycorrhizas: Physiology and Function. Kluwer, Dordrecht, The NetherlandsGoogle Scholar
  60. Kar RK, Saxena RK (1976) Algal and fungal microfossils from matanomadh formation (Paleocene), Kutch, India. Paleobotanist 43: 1–19Google Scholar
  61. Kenrick P (2003) Fishing for the first plants. Nature 425: 248–249PubMedCrossRefGoogle Scholar
  62. Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389: 33–39CrossRefGoogle Scholar
  63. Klironomos JN (2002) Another form of bias in conservation research. Science 298: 749–749PubMedCrossRefGoogle Scholar
  64. Koide RT, Kabir Z (2000) Extraradical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate. New Phytol 148: 511–517CrossRefGoogle Scholar
  65. Kojima T, Saito M (2004) Possible involvement of hyphal phosphatase in phosphate efflux from intraradical hyphae isolated from mycorrhizal roots colonized by Gigaspora margarita. Mycol Res 108: 610–615PubMedCrossRefGoogle Scholar
  66. Kucey RMN, Janzen HH, Leggett ME (1989) Microbially mediated increases in plant-available phosphorus. Adv Agron 42: 199–228CrossRefGoogle Scholar
  67. Lambais MR (2006) Unraveling the signaling and signal transduction mechanisms controlling arbuscular mycorrhiza development. Sci Agric 63: 405–413CrossRefGoogle Scholar
  68. Lovera M, Cuenca G (2007) Diversity of arbuscular mycorrhizal fungi (AMF) and mycorrhizal potential of the soil from a natural and a disturbed savannah from La Gran Sabana, Venezuela. Interciencia 32: 108–114Google Scholar
  69. Maeda D, Ashida K, Iguchi K, Chechetka SA, Hijikata A, Okusako Y, Deguchi Y, Izui K, Hata S (2006) Knockdown of an arbuscular mycorrhiza-inducible phosphate transporter gene of Lotus japonicus suppresses mutualistic symbiosis. Plant Cell Physiol 47: 807–817PubMedCrossRefGoogle Scholar
  70. Maldonado-Mendoza IE, Dewbre GR, Harrison MJ (2001) A phosphate transporter gene from the extra-radical mycelium of an arbuscular mycorrhizal fungus Glomus intraradices is regulated in response to phosphate in the environment. Mol Plant-Microbe Interact 14: 1140–1148PubMedCrossRefGoogle Scholar
  71. Marschner H (1995) Mineral Nutrition of Higher Plants (2nd edition). Academic, LondonGoogle Scholar
  72. Marschner P (2008) The effect of rhizosphere microorganisms on P uptake by plants. In: White PJ, Hammond JP (eds), The Ecophysiology of Plant-Phosphorus Interactions. Springer, Dordrecht, The Netherlands, pp 165–176CrossRefGoogle Scholar
  73. Medina A, Vassilev N, Barea JM, Azcón R (2005) Application of Aspergillus niger-treated agrowaste residue and Glomus mosseae for improving growth and nutrition of Trifolium repens in a Cd-contaminated soil. J Biotech 116: 369–378CrossRefGoogle Scholar
  74. Nagy R, Karandashov V, Chague W, Kalinkevich K, Tamasloukht M, Xu GH, Jakobsen I, Levy AA, Amrhein N, Bucher M (2005) The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant J 42: 236–250PubMedCrossRefGoogle Scholar
  75. O’Connor PJ, Smith SE, Smith EA (2002) Arbuscular mycorrhizas influence plant diversity and community structure in a semiarid herbland. New Phytol 154: 209–218CrossRefGoogle Scholar
  76. Offre P, Pivato B, Siblot S, Gamalero E, Corberand T, Lemanceau P, Mougel C (2007) Identification of bacterial groups preferentially associated with mycorrhizal roots of Medicago truncatula. Appl Environ Microbiol 73: 913–921PubMedCrossRefGoogle Scholar
  77. Ohtomo R, Saito M (2005) Polyphosphate dynamics in mycorrhizal roots during colonization of an arbuscular mycorrhizal fungus. New Phytol 167: 571–578PubMedCrossRefGoogle Scholar
  78. Olsson PA, van Aarle IM, Allaway WG, Ashford AE, Rouhier H (2002) Phosphorus effects on metabolic processes in monoxenic arbuscular mycorrhiza cultures. Plant Physiol 130: 1162–1171PubMedCrossRefGoogle Scholar
  79. Paszkowski U (2006) A journey through signaling in arbuscular mycorrhizal symbioses 2006. New Phytol 172: 35–46PubMedCrossRefGoogle Scholar
  80. Phipps CJ, Taylor TN (1996) Mixed arbuscular mycorrhizae from the Triassic of Antarctica. Mycologia 88: 707–714CrossRefGoogle Scholar
  81. Pirozynski KA, Malloch DW (1975) Origin of land plants: matter of mycotropism. Biosystems 6: 153–164PubMedCrossRefGoogle Scholar
  82. Powell CL, Daniel J (1978) Mycorrhizal fungi stimulate uptake of soluble and insoluble phosphate fertilizer from a phosphate-deficient soil. New Phytol 80: 351–358CrossRefGoogle Scholar
  83. Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414: 462–466PubMedCrossRefGoogle Scholar
  84. Read D (1998) Biodiversity - plants on the web. Nature 396: 22–23CrossRefGoogle Scholar
  85. Redecker D, Kodner R, Graham LE (2000a) Glomalean fungi from the Ordovician. Science 289: 1920–1921PubMedCrossRefGoogle Scholar
  86. Redecker D, Morton JB, Bruns TD (2000b) Ancestral lineages of arbuscular mycorrhizal fungi (Glomales). Mol Phylogenet Evol 14: 276–284PubMedCrossRefGoogle Scholar
  87. Reinhardt D (2007) Programming good relations - development of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 10: 98–105PubMedCrossRefGoogle Scholar
  88. Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci USA 91: 11841–11843PubMedCrossRefGoogle Scholar
  89. Requena N, Breuninger M, Franken P, Ocon A (2003). Symbiotic status, phosphate, and sucrose regulate the expression of two plasma membrane H + -ATPase genes from the mycorrhizal fungus Glomus mosseae. Plant Physiol 132: 1540–1549.PubMedCrossRefGoogle Scholar
  90. Reynolds HL, Vogelsang KM, Hartley AE, Bever JD, Schultz PA (2006) Variable responses of old-field perennials to arbuscular mycorrhizal fungi and phosphorus source. Oecologia 147: 348–358PubMedCrossRefGoogle Scholar
  91. Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aust J Plant Physiol 28: 897–906Google Scholar
  92. Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171: 41–53PubMedCrossRefGoogle Scholar
  93. Rillig MC, Mummey DL, Ramsey PW, Klironomos JN, Gannon JE (2006) Phylogeny of arbuscular mycorrhizal fungi predicts community composition of symbiosis-associated bacteria. FEMS Microbiol Ecol 57: 389–395PubMedCrossRefGoogle Scholar
  94. Roesti D, Ineichen K, Braissant O, Redecker D, Wiemken A, Aragno M (2005) Bacteria associated with spores of the arbuscular mycorrhizal fungi Glomus geosporum and Glomus constrictum. Appl Environ Microbiol 71: 6673–6679PubMedCrossRefGoogle Scholar
  95. Sanders IR (2002) Specificity in the arbuscular mycorrhizal symbiosis. In: van der Heijden MGA, Sanders IR (eds), Mycorrhizal Ecology. Springer, Berlin, pp 415–437Google Scholar
  96. Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116: 447–453PubMedCrossRefGoogle Scholar
  97. Schopf JW (1983) (ed) Earth’s Earliest Biosphere. It’s Origin and Evolution. Princeton University Press, Princeton, NJGoogle Scholar
  98. Schüβler A, Gehrig H, Schwarzott D, Walker C (2001a) Analysis of partial Glomales SSU rRNA gene sequences: implications for primer design and phylogeny. Mycol Res 105: 5–15CrossRefGoogle Scholar
  99. Schüβler A, Schwarzott D, Walker C (2001b) A new fungal phylum, the Glomeromycota, phylogeny and evolution. Mycol Res 105: 1413–1421CrossRefGoogle Scholar
  100. Simon L, Bousquet J, Levesque RC, Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363: 67–69CrossRefGoogle Scholar
  101. Smith FW (2002) The phosphate uptake mechanism. Plant Soil 245: 105–114CrossRefGoogle Scholar
  102. Smith FW, Mudge SR, Rae AL, Glassop D (2003) Phosphate transport in plants. Plant Soil 248: 71–83CrossRefGoogle Scholar
  103. Smith SE, Gianinazzi-Pearson V (1988) Physiological interactions between symbionts in vesicular-arbuscular mycorrhizal plants. Ann Rev Plant Physiol Plant Mol Biol 39: 221–244CrossRefGoogle Scholar
  104. Smith SE, Read DJ (1997) Mycorrhizal Symbiosis. Academic, San Diego, CAGoogle Scholar
  105. Smith SE, Smith FA, Jakobsen I (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol 162: 511–524CrossRefGoogle Scholar
  106. Stubblefield SP, Taylor TN, Trappe JM (1987) Fossil mycorrhizae: a case for symbiosis. Science 237: 59–60PubMedCrossRefGoogle Scholar
  107. Tawaraya K, Naito M, Wagatsuma T (2006) Solubilization of insoluble inorganic phosphate by hyphal exudates of arbuscular mycorrhizal fungi. J Plant Nutr 29: 657–665CrossRefGoogle Scholar
  108. Tisserant B, Gianinazzi-Pearson V, Gianinazzi S, Gollotte A (1993) In planta histochemical staining of fungal alkaline phosphatase activity for analysis of efficient arbuscular mycorrhizal infections. Mycol Res 97: 245–250CrossRefGoogle Scholar
  109. Toljander JF, Artursson V, Paul LR, Jansson JK, Finlay RD (2005) Attachment of different soil bacteria to arbuscular mycorrhizal fungal extraradical hyphae is determined by hyphal vitality and fungal species. FEMS Microbiol Lett 254: 34–40CrossRefGoogle Scholar
  110. Toro M, Azcón R, Barea JM (1997) Improvement of arbuscular mycorrhiza development by inoculation of soil with phosphate-solubilizing rhizobacteria to improve rock phosphate bioavailability (32P) and nutrient cycling. Appl Environ Microbiol 63: 4408–4412PubMedGoogle Scholar
  111. Truong BJ, Zapata F (2002) Standard characterization of phosphate rock samples from the FAO/IAEA a phosphate project. In: Assessment of Soil Phosphorus Status and Management of Phosphatic Fertilisers to Optimise Crop Production. IAEA, Vienna, pp 9–23Google Scholar
  112. Turnau K, Jurkiewicz A, Lingua G, Barea JM, Gianinazzi-Pearson V (2006) Role of arbuscular mycorrhiza and associated microorganisms in phytoremediation of heavy metal-polluted sites. In: Prasad MNV, Sajwan KS, Naidu R (eds), Trace Elements in the Environment. Biogeochemistry, Biotechnology and Bioremediation. CRC/Taylor & Francis, Boca Raton, FL, pp 235–252Google Scholar
  113. Uetake Y, Kojima T, Ezawa T, Saito M (2002) Extensive tubular vacuole system in an arbuscular mycorrhizal fungus, Gigaspora margarita. New Phytol 154: 761–768CrossRefGoogle Scholar
  114. van der Heijden MGA (2002) Arbuscular mycorrhizal fungi as a determinant of plant diversity: in search for underlying mechanisms and general principles. In: van der Heijden MGA, Sanders IR (eds), Mycorrhizal Ecology. Springer, Berlin, pp 243–265Google Scholar
  115. van der Heijden MGA, Sanders IR (2002) (eds) Mycorrhizal Ecology. Springer, BerlinGoogle Scholar
  116. van der Heijden MGA, Boller T, Wiemken A, Sanders IR (1998a) Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79: 2082–2091CrossRefGoogle Scholar
  117. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998b) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396: 69–72CrossRefGoogle Scholar
  118. van der Heijden MGA, Streitwolf-Engel R, Riedl R, Siegrist S, Neudecker A, Ineichen K, Boller T, Wiemken A, Sanders IR (2006) The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. New Phytol 172: 739–752PubMedCrossRefGoogle Scholar
  119. Vassilev N, Vassileva M, Azcón R, Medina A (2001) Application of free and Ca-alginate-entrapped Glomus deserticola and Yarowia lipolytica in a soil-plant system. J Biotechnol 91: 237–242PubMedCrossRefGoogle Scholar
  120. Vassilev N, Vassileva M, Azcón R, Barea JM (2002) The use of 32P dilution techniques to evaluate the effect of mycorrhizal inoculation on plant uptake of P from products of fermentation mixtures including agrowastes Aspergillus niger and rock phosphate. In: Assessment of Soil Phosphorus Status and Management of Phosphatic Fertilisers to Optimise Crop Production. IAEA, Vienna, pp 47–53Google Scholar
  121. Vassilev N, Medina A, Azcón R, Vassileva M (2006) Microbial solubilization of rock phosphate on media containing agro-industrial wastes and effect of the resulting products on plant growth and P uptake. Plant Soil 287: 77–84CrossRefGoogle Scholar
  122. Vogelsang KM, Reynolds HL, Bever JD (2006) Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol 172: 554–562PubMedCrossRefGoogle Scholar
  123. Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16: 299–363PubMedCrossRefGoogle Scholar
  124. Zapata F, Axmann H (1995) 32P isotopic techniques for evaluating the agronomic effectiveness of rock phosphate materials. Fert Res 41: 189–195CrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media B.V 2008

Authors and Affiliations

  • José-Miguel Barea
    • 1
  • Nuria Ferrol
    • 1
  • Concepción Azcón-Aguilar
    • 1
  • Rosario Azcón
    • 1
  1. 1.Departamento de Microbiología del Suelo y Sistemas SimbióticosEstación Experimental del Zaidín Consejo Superior de Investigaciones Científi casSpain

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