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Arbuscular Mycorrhizas: Physiology and Function pp 137–167Cite as

Nutrient Uptake: The Arbuscular Mycorrhiza Fungal Symbiosis as a Plant Nutrient Acquisition Strategy

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Abstract

Symbiotic association of roots with arbuscular mycorrhizal (AM) fungi is a very widespread strategy by which plants facilitate their acquisition of mineral elements from the soil. Studies employing sophisticated methodology in the fields of in vitro culture of AM colonized roots, microscopy, isotope labeling and molecular biology have shed light into the physiology of AM fungal nutrient uptake, transport and delivery to the host plant. In addition to the direct contribution to element uptake via the symbiotic pathway, AM mycelia have also been shown to affect root morphology and functioning, as well as mycorrhizosphere soil properties. This may lead to indirect effects of the AM association on plant nutrient availability and uptake. With their thin diameter, AM hyphae might be able to access smaller soil pores, and better compete with soil microbes for nutrient resources, compared with plant roots. Alone or in collaboration with associated hyphosphere bacteria, AM mycelia might also promote chemical mobilization of nutritional elements from sparingly plant available resources. Similar with plant root systems, AM mycelia appear to differ considerably in their architecture and physiological activities depending on their genotype. Whether such inherent traits represent different strategies in nutrient acquisition in collaboration with functionally compatible host roots, still remains speculative. Not much is known about how the AM fungal symbiosis is integrated into particular plant nutrient acquisition strategies, but it can be assumed that individual symbiotic strategies are highly diverse. The AM mycelium might assist the roots in spatial and/or chemical soil nutrient resource exploitation in a complementary and/or synergistic way. Knowledge about what factors determine the extent of functional compatibility between individual plant nutrient acquisition strategies and certain AM fungal traits would contribute to our understanding of ecosystem functioning, and might assist further development of mycorrhiza technology for plant production.

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Abbreviations

AM:

Arbuscular mycorrhiza

BAS:

Branched absorbing structure

C:

Carbohydrate

References

  • Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    CAS  PubMed  Google Scholar 

  • Al-Karaki GN, Al-Raddad A, Clark RB (1998) Water stress and mycorrhizal isolate effects on growth and nutrient acquisition of wheat. J Plant Nutr 21:891–903

    CAS  Google Scholar 

  • Allaway WG, Ashford AE (2001) Motile tubular vacuoles in extramatrical mycelium and sheath hyphae of ectomycorrhizal systems. Protoplasma 215:218–225

    CAS  PubMed  Google Scholar 

  • Allen JW, Shachar-Hill Y (2009) Sulfur transfer through and arbuscular mycorrhiza. Plant Physiol 149:549–560

    CAS  PubMed  Google Scholar 

  • Alloush GA, Zeto SK, Clark RB (2000) Phosphorus source, organic matter, and arbuscular mycorrhiza effects on growth and mineral acquisition of chickpea grown in acidic soil. J Plant Nutr 23:1351–1369

    CAS  Google Scholar 

  • Ames RN, Reid CPP, Porter LK, Cambardella C (1983) Hyphal uptake and transport of nitrogen from two 15N-labeled sources by Glomus mosseae, a vesicular-arbuscular mycorrhizal fungus. New Phytol 95:381–396

    Google Scholar 

  • Andrade G, Mihara KL, Lindermann RG, Bethlenfalvay GJ (1998) Soil aggregation and rhizobacteria in the mycorrhizosphere. Plant Soil 202:89–96

    CAS  Google Scholar 

  • Antunes PM, Schneider K, Hillis D, Klironomos J (2007) Can the arbuscular mycorrhizal fungus Glomus intraradices actively mobilize P from rock phosphates? Pedobiologia 51:281–286

    CAS  Google Scholar 

  • Aristizábal C, Rivera E, Janos D (2004) Arbuscular mycorrhizal fungi colonize decomposing leaves of Myrica parvifolia, M. pubescens and Paepalanthus sp. Mycorrhiza 14:221–228

    PubMed  Google Scholar 

  • Atkinson D, Berta G, Hooker JE (1994) Impact of mycorrhizal colonization on root architecture, root longevity and the formation of growth regulators. In: Gianiazzi S, Schüepp H (eds) Impact of arbuscular mycorrhizas on sustainable agriculture and natural ecosystems. Birkhäuser, Berlin

    Google Scholar 

  • Azcón R, Rodriguez R, Amora-Lazcano E, Ambrosano E (2008) Uptake and metabolism of nitrate in mycorrhizal plants as affected by water availability and N concentration in soil. Eur J Soil Sci 59:131–138

    Google Scholar 

  • Bago B (2000) Putative sites for nutrient uptake in arbuscular mycorrhizal fungi. Plant Soil 226:263–274

    CAS  Google Scholar 

  • Bago B, Cano C (2005) Breaking myths on arbuscular mycorrhizas in vitro biology. In: Declerck S, Strullu DG, Fortin A (eds) In vitro culture of mycorrhizas: soil biology series, vol 4. Springer, Berlin/Heidelberg/New York

    Google Scholar 

  • Bago B, Azcon-Aguilar C, Goulet A, Piché Y (1998) Branched absorbing structures (BAS): a feature of the extraradical mycelium of arbuscular mycorrhizal fungi. New Phytol 139:375–388

    Google Scholar 

  • Bago B, Zipfel W, Williams RM, Jun J, Arreola R, Lammers PJ, Pfeffer PE, Shachar-Hill Y (2002) Translocation and utilization of fungal storage lipids in the arbuscular mycorrhizal symbiosis. Plant Physiol 128:108–124

    CAS  PubMed  Google Scholar 

  • Bago B, Cano C, Azcón-Aguilar C, Samson J, Coughlan AP, Piché Y (2004) Differential morphogenesis of the extraradical mycelium of an arbuscular mycorrhizal fungus grown monoxenically on spatially heterogeneous culture media. Mycologia 96:452–462

    PubMed  Google Scholar 

  • Barker SJ, Stummer B, Gao L, Dispain I, O’Connor PJ, Smith SE (1998) A mutant in Lycopersicon esculentum Mill. with highly reduced VA mycorrhizal colonization: isolation and preliminary characterisation. Plant J 15:791–797

    CAS  Google Scholar 

  • Benedetto A, Magurno F, Bonfante P, Lanfranco L (2005) Expression profiles of a phosphate transporter gene (GmosPT) from the endomycorrhizal fungus Glomus mosseae. Mycorrhiza 15:620–627

    CAS  PubMed  Google Scholar 

  • Bermudez M, Azcón R (1996) Calcium uptake by alfalfa as modified by a mycorrhizal fungus and liming. Symbiosis 20:175–184

    CAS  Google Scholar 

  • Berta G, Fusconi A, Trotta A, Scannerini S (1990) Morphogenetic modifications induced by the mycorrhizal fungus Glomus strain E3 in the root system of Allium porrum L. New Phytol 114:207–215

    Google Scholar 

  • Berta G, Fusconi A, Trotta A (1993) VA mycorrhizal infection and the morphology and function of root systems. Environ Exp Bot 33:159–173

    Google Scholar 

  • Bianciotto V, Andreotti S, Balestrini R, Bonfante P, Perotto S (2001) Extracellular polysaccharides are involved in the attachment of Azospirillum brasiliense and Rhizobium leguminosarum to arbuscular mycorrhizal structures. Eur J Histochem 45:39–49

    CAS  PubMed  Google Scholar 

  • Bianciotto V, Perotto S, Ruiz-Lozano JM, Bonfante P (2002) Arbuscular mycorrhizal fungi and soil bacteria: From cellular investigations to biotechnological perspectives. In: Gianiazzi S, Schüepp H (eds) Impact of arbuscular mycorrhizas on sustainable agriculture and natural ecosystems. Birkhäuser, Berlin

    Google Scholar 

  • Blal B, Morel C, Gianinazzi-Pearson V, Fardeau JC, Gianinazzi S (1990) Influence of vesicular-arbuscular mycorrhizae on phosphate fertiliser efficiency in two tropical acid soils planted with micropropagated oil palm (Elaeis guineensis Jacq). Biol Fert Soil 9:43–48

    CAS  Google Scholar 

  • Blee KA, Anderson AJ (1998) Regulation of arbuscule formation by carbon in the plant. Plant J 16:523–530

    Google Scholar 

  • Bruce A, Smith SE, Tester M (1994) The development of mycorrhizal infection in cucumber: effects of P supply on root growth, formation of entry points and growth of infection units. New Phytol 127:507–514

    Google Scholar 

  • Bürkert B, Robson A (1994) 65Zn uptake in subterranean clover (Trifolium subterraneum L.) by 3 vesicular arbuscular mycorrhizal fungi in a root-free sandy soil. Soil Biol Biochem 26:1117–1124

    Google Scholar 

  • Caris C, Hördt W, Hawkins H-J, Römheld V, George E (1998) Studies of iron transport by arbuscular mycorrhizal hyphae from soil to peanut and sorghum plants. Mycorrhiza 8:35–39

    CAS  Google Scholar 

  • Cavagnaro TR (2008) The role of arbuscular mycorrhizas in improving plant zinc nutrition under low soil zinc concentrations: a review. Plant Soil 304:315–325

    CAS  Google Scholar 

  • Cavagnaro TR, Smith FA, Smith SE, Jakobsen I (2005) Functional diversity in arbuscular ­mycorrhizas: exploitation of soil patches with different phosphate enrichment differs among fungal species. Plant Cell Environ 28:642–650

    CAS  Google Scholar 

  • Cavagnaro TR, Jackson LE, Six J, Ferris H, Goyal S, Asami D, Scow KM (2006) Arbuscular mycorrhizas, microbial communities, nutrient availability, and soil aggregates in organic tomato production. Plant Soil 282:209–225

    CAS  Google Scholar 

  • Chalot M, Blaudez D, Brun A (2006) Ammonia: a candidate for nitrogen transfer at the mycorrhizal­ interface. Trends Plant Sci 11:263–266

    CAS  PubMed  Google Scholar 

  • Chen BD, Christie P, Li X-L (2001) A modified glass bead compartment cultivation system for studies on nutrient and trace metal uptake by arbuscular mycorrhiza. Chemosphere 42:185–192

    CAS  PubMed  Google Scholar 

  • Chen BD, Li XL, Tao HQ, Christie P, Wong MH (2003) The role of arbuscular mycorrhiza in zinc uptake by red clover grown in a calcareous soil spiked with various quantities of zinc. Chemosphere 50:839–846

    CAS  PubMed  Google Scholar 

  • Christie P, Li XL, Chen BD (2004) Arbuscular mycorrhiza can depress translocation of zinc to shoots of host plants in soils moderately polluted with zinc. Plant Soil 261:209–217

    CAS  Google Scholar 

  • Ciereszko I, Gniazdowska A, Mikulska M, Rychter AM (1996) Assimilate translocation in bean plants (Phaseolus vulgaris L.) during phosphate deficiency. J Plant Physiol 149:343–348

    CAS  Google Scholar 

  • Clark RB, Zeto SK, Zobel RW (1999a) Arbuscular mycorrhizal fungal isolate effectiveness on growth and root colonization of Panicum virgatum in acidic soil. Soil Biol Biochem 31:1757–1763

    CAS  Google Scholar 

  • Clark RB, Zobel RW, Zeto SK (1999b) Effects of mycorrhizal fungus isolates on mineral acquisition by Panicum virgatum in acidic soil. Mycorrhiza 9:167–176

    CAS  Google Scholar 

  • Clay K (2001) Symbiosis and the regulation of communities. Am Zool 41:810–814

    Google Scholar 

  • Coperman RH, Martin CA, Stutz JC (1996) Tomato growth in response to salinity and mycorrhizal fungi from saline or nonsaline soils. Hortscience 31:341–344

    Google Scholar 

  • Croll D, Giovannetti M, Koch AM, Sbrana C, Ehinger M, Lammers PJ, Sanders IR (2009) Nonself vegetative fusion and genetic exchange in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 181:924–937

    CAS  PubMed  Google Scholar 

  • Cruz C, Egsgaard H, Trujillo C, Ambus P, Requena N, Martins-Lução MA, Jakobsen I (2007) Enzymatic evidence for the key role in arginine in nitrogen translocation by arbuscular mycorrhizal fungi. Plant Physiol 144:782–792

    CAS  PubMed  Google Scholar 

  • Cui M, Caldwell M (1996) Facilitation of plant phosphate acquisition by arbuscular mycorrhizas from enriched soil patches. I. Roots and hyphae exploiting the same soil volume. New Phytol 133:453–460

    CAS  Google Scholar 

  • Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47

    CAS  Google Scholar 

  • Davies FT Jr, Potter JR, Lindemann RG (1992) Mycorrhiza and repeated drought exposure affect drought resistance and extraradical hyphae development of pepper plants independent of plant size and nutrient content. J Plant Physiol 139:289–294

    Google Scholar 

  • De la Providencia IE, de Souza FA, Fernández F, Séjalon Delmas N, Declerck S (2004) Arbuscular mycorrhizal fungi reveal distinct patterns of anastomosis formation and hyphal healing mechanisms between different phylogenetic groups. New Phytol 165:261–271

    Google Scholar 

  • De Miranda JCC, Harris PJ (1994) Effects of soil phosphorus on spore germination and hyphal growth of arbuscular mycorrhizal fungi. New Phytol 128:103–108

    CAS  Google Scholar 

  • De Souza FA, Declerck S (2003) Mycelium development and architecture, and spore production of Scutellospora reticulata in monoxenic culture with Ri T-DNA transformed carrot roots. Mycologia 95:1004–1012

    PubMed  Google Scholar 

  • Del Val C, Barea JM, Azcón-Aguilar C (1999) Diversity of arbuscular mycorrhizal fungus populations in heavy-metal-contaminated soils. Appl Environ Microbiol 65:718–723

    CAS  PubMed  Google Scholar 

  • Desnos T (2008) Root branching responses to phosphate and nitrate. Curr Opin Plant Biol 11:82–87

    CAS  PubMed  Google Scholar 

  • Dodd JC, Burton CC, Burns RG, Jeffries P (1987) Phosphatase activity associated with the roots and the rhizosphere of plants infected with vesicular-arbuscular mycorrhizal fungi. New Phytol 107:163–172

    CAS  Google Scholar 

  • Dodd JC, Boddington CL, Rodriguez A, Gonzalez-Chavez C, Mansur I (2000) Mycelium of arbuscular mycorrhizal fungi (AMF) from different genera: form, function and detection. Plant Soil 226:131–151

    CAS  Google Scholar 

  • Douds DD Jr, Pfeffer PE, Shachar-Hill Y (2000) Carbon partitioning, cost and metabolism of arbuscular mycorrhizas. In: Kapulnik Y, Douds DD Jr (eds) Arbuscular mycorrhizas: physiology­ and function. Kluwer, Dordrecht

    Google Scholar 

  • Drew EA, Murray RS, Smith SE (2006) Functional diversity of external hyphae of AM ­fungi: Ability to colonise new hosts is influenced by fungal species, distance and soil conditions. Appl Soil Ecol 32:350–365

    Google Scholar 

  • Driver JD, Holben WE, Rillig MC (2005) Characterization of glomalin as a hyphal wall component of arbuscular mycorrhizal fungi. Soil Biol Biochem 37:101–106

    CAS  Google Scholar 

  • Eom A-H, Hartnett DC, Wilson GWT (2000) Host plant species effects on arbuscular mycorrhizal fungal communities in tallgrass prairie. Oecologia 122:435–444

    Google Scholar 

  • Ezawa T, Hayatsu M, Saito M (2005) A new hypothesis on the strategy for acquisition of phosphorus in arbuscular mycorrhiza: up-regulation of secreted acid phosphatase gene in the host plant. Mol Plant Microbe Int 18:1046–1053

    CAS  Google Scholar 

  • Faber BA, Zasoski RD, Munns DN (1991) A method for measuring hyphal nutrient and water uptake in mycorrhizal plants. Can J Bot 69:87–94

    Google Scholar 

  • Farley RA, Fitter AH (1999) Temporal and spatial variation in soil resources in a deciduous woodland. J Ecol 87:688–696

    Google Scholar 

  • Fitter AH (2006) What is the link between carbon and phosphorus fluxes in arbuscular mycorrhizas? A null hypothesis for symbiotic function. New Phytol 172:3–6

    CAS  PubMed  Google Scholar 

  • Frey B, Schüepp H (1992) Transfer of symbiotically fixed nitrogen from berseem (Trifolium alexandrinum L.) to maize via arbuscular mycorrhizal hyphae. New Phytol 122:447–454

    CAS  Google Scholar 

  • Frey B, Schüepp H (1993) Acquisition of nitrogen by external hyphae of arbuscular mycorrhizal fungi associated with Zea mays L. New Phytol 124:221–230

    Google Scholar 

  • Friese C, Allen MF (1991) The spread of VA mycorrhizal fungal hyphae in the soil: Inoculum types and external hyphal architecture. Mycologia 83:409–418

    Google Scholar 

  • Fusconi A, Gnavi E, Trotta A, Berta G (1999) Apical meristems of tomato roots and their modifications induced by arbuscular mycorrhizal and soil borne pathogenic fungi. New Phytol 142:505–516

    Google Scholar 

  • Fusconi A, Tagliasacchi AM, Berta G, Trotta A, Brazzaventre S, Ruberti F, Scannerini S (2000) Root apical meristems of Allium porrum L. as affected by arbuscular mycorrhizae and phosphorus. Protoplasma 214:219–226

    CAS  Google Scholar 

  • Gahoonia TS, Raza S, Nielsen NE (1994) Phosphorus depletion in the rhizosphere as influenced by soil moisture. Plant Soil 159:213–218

    CAS  Google Scholar 

  • Garcia-Garrido JM, Garcia-Romera JM, Ocampo JA (1992) Cellulase production by the vesicular arbuscular mycorrhizal fungus Glomus mosseae (Nicol and Gerd) and Trappe. New Phytol 121:221–226

    CAS  Google Scholar 

  • George E, Häussler K-U, Vetterlein D, Gorgus E, Marschner H (1992) Water and nutrient translocation by hyphae of Glomus mosseae. Can J Bot 70:2130–2137

    Google Scholar 

  • Gianinazzi-Pearson V (1984) Host-fungus specifity, recognition and compatibility in mycorrhizae. In: Verma DPS, Hohn TH (eds) Genes involved in plant-microbe interactions. Springer, Vienna

    Google Scholar 

  • Govindarajulu M, Pfeffer P, Jin H, Abubaker J, Douds DD, Allen JW, Bücking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823

    CAS  PubMed  Google Scholar 

  • Graham JH, Abbott LK (2000) Wheat response to aggressive and non-aggressive arbuscular mycorrhizal fungi. Plant Soil 220:207–218

    CAS  Google Scholar 

  • Graham JH, Eissenstat DM (1994) Host genotype and the formation and function of VA mycorrhizae. Plant Soil 159:179–185

    Google Scholar 

  • Gryndler M, Hršelová H, Sudová R, Gryndlerová H, Řezáčová V, Merhautová V (2005) Hyphal growth and mycorrhiza formation by the arbuscular mycorrhizal fungus Glomus claroideum BEG 23 is stimulated by humic substances. Mycorrhiza 15:483–488

    CAS  PubMed  Google Scholar 

  • Gutjahr C, Paszkowski U (2009) Weights in the balance: Jasmonic acid and salicylic acid signaling­ in root-biotroph interactions. Mol Plant Microbe Int 22:763–772

    CAS  Google Scholar 

  • Gutjahr C, Casieri L, Paszkowski U (2009) Glomus intraradices induces changes in root system architecture of rice independently of common symbiosis signalling. New Phytol 182:829–837

    PubMed  Google Scholar 

  • Gutschick V (1993) Nutrient-limited growth rates: roles of nutrient-use efficiency and of adaptations­ to increase uptake rate. J Exp Bot 44:41–51

    Google Scholar 

  • Habte M, Manjunath A (1991) Categories of vesicular-arbuscular mycorrhizal dependency of host species. Mycorrhiza 1:3–12

    Google Scholar 

  • Hamel C, Dalpe Y, Furlan V, Parent S (1997) Indigenous populations of arbuscular mycorrhizal fungi and soil aggregate stability are major determinants of leek (Allium porrum L.) response to inoculation with Glomus intraradices Schenck & Smith or Glomus versiforme (Karsten) Berch. Mycorrhiza 7:187–196

    Google Scholar 

  • Hanssen JF, Thingstad TF, Gohsøn J (1974) Evaluation of hyphal lengths and fungal biomass in soil by a membrane filter method. Oikos 25:102–107

    Google Scholar 

  • Harinikumar KM, Bagyaraj DJ (1995) Spread of vesicular-arbuscular mycorrhizal fungal hyphae in soil. Microbiol Res 150:77–80

    Google Scholar 

  • Harrison MJ, van Buuren ML (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626–629

    CAS  PubMed  Google Scholar 

  • Harrison MJ, Dewbre GR, Liu J (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:1–17

    Google Scholar 

  • Hart MM, Reader RJ (2001) Taxonomic basis for the variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153:335–344

    Google Scholar 

  • Hart MM, Reader RJ, Klironomos JN (2003) Plant coexistence mediated by arbuscular mycorrhizal fungi. Trends Ecol Evol 18:418–423

    Google Scholar 

  • Hattingh MJ, Gray LE, Gerdemann JW (1973) Uptake and translocation of P32 labeled phosphate to onion roots by endomycorrhizal fungi. Soil Sci 116:383–387

    CAS  Google Scholar 

  • Hawkins H-J, Cramer MD, George E (1999) Root respiratory quotient and nitrate uptake in hydroponically grown non-mycorrhizal and mycorrhizal wheat. Mycorrhiza 9:57–60

    CAS  Google Scholar 

  • Hawkins JH, Johansen A, George E (2000) Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 226:275–285

    CAS  Google Scholar 

  • Helgason T, Merryweather JW, Denison J, Wilson P, Young JPW, Fitter AH (2002) Selectivity and functional diversity in arbuscular mycorrhizas of co-occurring fungi and plants from a temperate deciduous woodland. J Ecol 90:371–384

    Google Scholar 

  • Herrera-Medina MJ, Steinkellner S, Vierheilig H, Bote JAO, Garrido JMG (2007) Abscisic acid determines arbuscule development and functioning in the tomato arbuscular mycorrhiza. New Phytol 175:554–564

    CAS  PubMed  Google Scholar 

  • Hetrick BAD, Leslie JF, Wilson GT, Kitt GG (1988) Physiological and topological assessment of effects of a vesicular-arbuscular mycorrhizal fungus on root architecture of big bluestem. New Phytol 110:85–96

    Google Scholar 

  • Hildebrand U, Schmelzer E, Bothe H (2002) Expression of nitrate transporter genes in tomato colonized with an arbuscular mycorrhizal fungus. Physiol Plant 115:125–136

    Google Scholar 

  • Hildebrandt U, Kaldorf M, Bothe H (1999) The zinc violet and its colonization by arbuscular mycorrhizal fungi. J Plant Physiol 154:709–711

    CAS  Google Scholar 

  • Hodge A (2001) Arbuscular mycorrhizal fungi influence decomposition of, but not plant nutrient capture from, glycine patches in the soil. New Phytol 151:725–734

    CAS  Google Scholar 

  • Hodge A (2003a) Plant nitrogen capture from organic matter as affected by spatial dispersion, interspecific competition and mycorrhizal colonization. New Phytol 157:303–314

    Google Scholar 

  • Hodge A (2003b) N capture by Plantago lanceolata and Brassica napus from organic material – the influence of spatial dispersion, plant competition and arbuscular mycorrhizal fungus. J Exp Bot 54:2331–2342

    CAS  PubMed  Google Scholar 

  • Hodge A (2006) Plastic plants and patchy soils. J Exp Bot 57:401–411

    CAS  PubMed  Google Scholar 

  • Hodge A (2009) Root decisions. Plant Cell Environ 32:628–640

    PubMed  Google Scholar 

  • Hodge A, Robinson D, Griffiths BS, Fitter AH (1999) Nitrogen capture by plants grown in N-rich organic patches of contrasting size and strength. J Exp Bot 50:1243–1252

    CAS  Google Scholar 

  • Hodge A, Robinson D, Fitter AH (2000) An arbuscular mycorrhizal inoculum enhances root proliferation in, but not nitrogen capture from, nutrient-rich patches in the soil. New Phytol 145:575–584

    CAS  Google Scholar 

  • Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates ­decomposition and acquires nitrogen directly from organic material. Nature 413:297–299

    CAS  PubMed  Google Scholar 

  • Jakobsen I, Abbott K, Robson AD (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. I Spread of hyphae and phosphorus inflow into roots. New Phytol 120:371–380

    CAS  Google Scholar 

  • Jakobsen I, Gazey C, Abbott LK (2001) Phosphate transport by communities of arbuscular mycorrhizal fungi in intact soil cores. New Phytol 149:95–103

    CAS  Google Scholar 

  • Jakobsen I, Chen B, Munkvold L, Lundsgaard T, Zhu Y-G (2005) Contrasting phosphate acquisition of mycorrhizal fungi with that of root hairs using the root hairless barley mutant. Plant Cell Environ 28:928–938

    CAS  Google Scholar 

  • Janos DP (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17:75–91

    PubMed  Google Scholar 

  • Jansa J, Mozafar A, Frossard E (2003) Long-distance transport of P and Zn through the hyphae of an arbuscular mycorrhizal fungus in symbiosis with maize. Agronomie 23:481–488

    CAS  Google Scholar 

  • Jayachandran K, Schwab AP, Hetrick BAD (1989) Mycorrhizal mediation of phosphorus availability-synthetic iron chelate effects on phosphorus solubilisation. Soil Sci Soc Am J 53:1701–1706

    CAS  Google Scholar 

  • Jentschke G, Brandes B, Heinzemann J, Marschner P, Godbold D (1999) Sand culture of mycorrhizal plants. J Plant Nutr Soil Sci 162:107–112

    CAS  Google Scholar 

  • Jin H, Pfeffer PE, Douds DD, Piotrowski E, Lammers PJ, Shachar-Hill Y (2005) The uptake, metabolism, transport and transfer of nitrogen in arbuscular mycorrhizal symbiosis. New Phytol 168:687–696

    CAS  PubMed  Google Scholar 

  • Johansen A, Jakobsen I, Jensen ES (1992) Hyphal transport of 15N-labelled nitrogen by a vesicular-arbuscular mycorrhizal fungus and its effect on depletion of inorganic soil N. New Phytol 122:281–288

    CAS  Google Scholar 

  • Johansen A, Jakobsen I, Jensen ES (1994) Hyphal N transport by a vesicular-arbuscular mycorrhizal fungus associated with cucumber grown at three nitrogen levels. Plant Soil 160:1–9

    CAS  Google Scholar 

  • St. John TV, Coleman DC, Reid CPP (1983) Association of vesicular-arbuscular mycorrhizal hyphae with soil organic particles. Ecology 64:957–959

    Google Scholar 

  • Johnson SE, Loeppert RH (2006) Role of organic acids in phosphate mobilization from iron oxide. Soil Sci Soc Am J 70:222–234

    CAS  Google Scholar 

  • Joner EJ, Jakobsen I (1995) Growth and extracellular phosphatase activity of arbuscular mycorrhizal hyphae as influenced by soil organic matter. Soil Biol Biochem 27:1153–1159

    CAS  Google Scholar 

  • Joner EJ, Leyval C (2001) Time-course of heavy metal uptake on maize and clover as affected by different mycorrhiza inoculation regimes. Biol Fert Soils 33:351–357

    CAS  Google Scholar 

  • Joslin JD, Gaudinski JB, Torn MS, Riley WJ, Hanson PJ (2006) Fine root turnover patterns and their relationship to root diameter and soil depth in a 14C -labeled hardwood forest. New Phytol 172:523–535

    CAS  PubMed  Google Scholar 

  • Jungk (1987) Soil-root interactions in the rhizosphere affecting plant availability of phosphorus. J Plant Nutr 10:1197–1204

    CAS  Google Scholar 

  • Karandashov V, Kuzovkina I, Hawkins H-J, George E (2000) Growth and sporulation of the arbuscular mycorrhizal fungus Glomus caledonium in dual culture with transformed carrot roots. Mycorrhiza 10:23–28

    CAS  Google Scholar 

  • Khalil S, Loynachan TE, Tabatabi MA (1994) Mycorrhizal dependency and nutrient uptake by improved and unimproved corn and soybean cultivars. Agron J 86:949–958

    Google Scholar 

  • Koide R (2000) Functional complementarity in the arbuscular mycorrhizal symbiosis. New Phytol 147:233–235

    Google Scholar 

  • Koide RT, Kabir Z (2000) Extraradical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate. New Phytol 148:511–517

    CAS  Google Scholar 

  • Kuga Y, Saito K, Nayuki K, Peterson RL, Saito M (2007) Ultrastructure of rapidly frozen and freeze-substituted germ tubes of an arbuscular mycorrhizal fungus and localization of polyphosphate. New Phytol 178:189–200

    Google Scholar 

  • Leake JR, Johnson D, Donnelly DP, Muckle GE, Boddy L, Read DJ (2004) Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and ­agroecosystems functioning. Can J Bot 82:1016–1045

    Google Scholar 

  • Lee YJ, George E (2005) Contribution of mycorrhizal hyphae to the uptake of metal cations by cucumber plants at two levels of phosphorus supply. Plant Soil 278:361–370

    CAS  Google Scholar 

  • Leigh J, Hodge A, Fitter AH (2009) Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol 181:199–207

    CAS  PubMed  Google Scholar 

  • Leyval B, Binet C (1998) Effect of polyaromatic hydrocarbons (PAHs) on arbuscular mycorrhizal colonization of plants. J Environ Qual 27:402–407

    CAS  Google Scholar 

  • Li X-L, George E, Marschner H (1991a) Phosphorus depletion and pH decrease at the root-soil and hyphae-soil interfaces of VA mycorrhizal white clover fertilised with ammonium. New Phytol 119:397–404

    CAS  Google Scholar 

  • Li X-L, Marschner H, Römheld V (1991b) Acquisition of phosphorus and copper by VA-mycorrhizal hyphae and root-to-shoot transport in white clover. Plant Soil 136:49–57

    CAS  Google Scholar 

  • Liu A, Hamel C, Hamilton RI, Ma BL, Smith DL (2000) Acquisition of Cu, Zn, Mn and Fe by mycorrhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels. Mycorrhiza 9:331–336

    CAS  Google Scholar 

  • López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287

    PubMed  Google Scholar 

  • López-Pedrosa A, González-Guerrero M, Valderas A, Azcón-Aguilar C, Ferrol N (2006) GintAMTi encodes a functional high-affinity ammonium transporter that is expressed in the extraradical mycelium of Glomus intraradices. Fungal Genet Biol 43:102–110

    PubMed  Google Scholar 

  • Ma Z, Baskin TI, Brown KM, Lynch JP (2003) Regulation of root elongation under phosphorus stress involves changes in ethylene responsiveness. Plant Physiol 131:1381–1390

    CAS  PubMed  Google Scholar 

  • 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 Int 14:1140–1148

    CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic, London

    Google Scholar 

  • Marschner H, Kirkby E, Cakmak I (1996) Effect of mineral nutritional status on shoot-root partitioning of photoassimilates and cycling of mineral nutrients. J Exp Bot 47:1255–1263

    CAS  PubMed  Google Scholar 

  • Martins MA, Cruz AF (1998) The role of the external mycelial network of arbuscular mycorrhizal fungi: III. A study of nitrogen transfer between plants interconnected by a common mycelium. Rev Microbiol 29:289–294

    Google Scholar 

  • Martins MA, Read DJ (1996) The role of the external mycelial network of arbuscular mycorrhizal (AM) fungi. 2. A study of phosphorus transfer between plants interconnected by a common mycelium. Rev Microbiol 27:100–105

    Google Scholar 

  • Masaoka Y, Kojima M, Sugihara S, Yoshihara T, Koshina M, Ichihara A (1993) Dissolution of ferric phosphate by alfalfa (Medicago sativa L.) root exudates. Plant Soil 155:75–78

    Google Scholar 

  • McArthur DAJ, Knowles NR (1993) Influence of vesicular-arbuscular mycorrhizal fungi on the response of potato to phosphorus deficiency. Plant Physiol 101:147–160

    CAS  PubMed  Google Scholar 

  • McDonald A, Ericsson T, Larsson C (1996) Plant nutrition, dry matter gain and partitioning at the whole plant level. J Exp Bot 47:1245–1253

    CAS  PubMed  Google Scholar 

  • Meharg AA, Cairney JWG (2000) Co-evolution of mycorrhizal symbionts and their hosts to metal-contaminated environments. Adv Ecol Res 30:69–112

    CAS  Google Scholar 

  • Miller RM, Jastrow JD (1990) Hierarchy of root and mycorrhizal fungal interactions with soil aggregation. Soil Biol Biochem 22:579–584

    Google Scholar 

  • Nagahashi G, Douds DD Jr, Abney GD (1996) Phosphorus amendment inhibits hyphal branching of the VAM fungus Gigaspora margarita directly and indirectly through its effect on root exudation. Mycorrhiza 6:403–408

    CAS  Google Scholar 

  • Nair MG, Safir GR, Siqueira JO (1991) Isolation and identification of vesicular-arbuscular ­mycorrhiza-stimulatory compounds from clover (Trifolium repens) roots. Appl Environ Microbiol 57:434–439

    CAS  PubMed  Google Scholar 

  • Neumann E, George E (2004) Colonisation with the arbuscular mycorrhizal fungus Glomus mosseae (Nicol. & Gerd.) enhanced phosphorus uptake from dry soil in Sorghum bicolor (L.). Plant Soil 231:245–255

    Google Scholar 

  • Neumann E, George E (2005a) Extraction of arbuscular mycorrhiza mycelium from compartments filled with wet sieved soil and glass beads. Mycorrhiza 15:533–537

    PubMed  Google Scholar 

  • Neumann E, George E (2005b) Does the presence of arbuscular mycorrhizal fungi influence growth and nutrient uptake of a wild-type tomato cultivar and a mycorrhiza-defective mutant, cultivated with roots sharing the same soil volume? New Phytol 166:601–609

    CAS  PubMed  Google Scholar 

  • Neumann E, Schmid B, Römheld V, George E (2009) Extraradical development and contribution to plant performance of an arbuscular mycorrhizal symbiosis exposed to complete or partial rootzone drying. Mycorrhiza 20:13–23

    PubMed  Google Scholar 

  • Oades JM (1984) Soil organic matter and structural stability: Mechanisms and implications for management. Plant Soil 76:319–337

    CAS  Google Scholar 

  • Oehl F, Sieverding E, Ineichen K, Ris E-A, Boller T, Wiemken A (2005) Community structure of arbuscular mycorrhizal fungi at different soil depths in extensively and intensively managed agroecosystems. New Phytol 165:273–283

    PubMed  Google Scholar 

  • Ojala JC, Jarrell WM, Menge JA, Johnson ELV (1983) Influence of mycorrhizal fungi on the mineral nutrition and yield of onion in saline soils. Agron J 75:255–259

    CAS  Google Scholar 

  • Olsson PA, Wilhelmsson P (2000) The growth of external AM fungal mycelium in sand dunes and in experimental systems. Plant Soil 226:161–169

    CAS  Google Scholar 

  • Olsson PA, van Arle IM, Allaway WG, Ashford AE, Rouhier H (2002) Phosphorus effects on metabolic processes in monoxenic arbuscular mycorrhiza cultures. Plant Physiol 130:1162–1171

    CAS  PubMed  Google Scholar 

  • Olsson PA, Jakobsen I, Wallander H (2003) Foraging and resource allocation strategies of mycorrhizal fungi in a patchy environment. In: Van der Heijden MGA, Sanders I (eds) Ecological studies vol. 157, mycorrhizal ecology. Springer, Berlin

    Google Scholar 

  • Passioura JB (2002) Soil conditions and plant growth. Plant Cell Environ 25:311–318

    PubMed  Google Scholar 

  • Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionary divergent gene specifically activated in arbuscular mycorrhizal symbiosis. P Natl Acad Sci USA 99:13324–13329

    CAS  Google Scholar 

  • Pearson JN, Jakobsen I (1993a) The relative contribution of hyphae and roots to phosphorus uptake by arbuscular mycorrhizal plants, measured by dual labeling with 32P and 33P. New Phytol 124:489–494

    CAS  Google Scholar 

  • Pearson JN, Jakobsen I (1993b) Symbiotic exchange of carbon and phosphorus between cucumber and three arbuscular mycorrhizal fungi. New Phytol 124:481–488

    CAS  Google Scholar 

  • Phillips RP, Fahey TJ (2006) Tree species and mycorrhizal associations influence the magnitude of rhizosphere effects. Ecology 87:1302–1313

    PubMed  Google Scholar 

  • Pregitzer KS, Zak DR, Curtis PS, Kubiske ME, Teeri JA, Vogel CS (1995) Atmospheric CO2, soil nitrogen and turnover of fine roots. New Phytol 129:579–585

    Google Scholar 

  • Pringle A, Bever JD (2002) Divergent phenologies may facilitate the coexistence of arbuscular mycorrhizal fungi in a North Carolina grassland. Am J Bot 89:1439–1446

    PubMed  Google Scholar 

  • Purin S, Rillig MC (2007) The arbuscular mycorrhizal fungal protein glomalin: Limitations, progress, and a new hypohesiss for its function. Pedobiologia 51:123–130

    CAS  Google Scholar 

  • Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein M, Bucher M (2001) A phosphate transporter expressed in arbuscule containing cells in potato. Nature 416:462–466

    Google Scholar 

  • Ravnskov S, Jakobsen I (1995) Functional compatibility in arbuscular mycorrhizas measured as hyphal P transport to the plant. New Phytol 129:611–618

    Google Scholar 

  • Redecker D, Thierfelder H, Werner D (1998) Production of biomass of arbuscular mycorrhizal fungi in the glassbead compartment system. In: Varma A (ed) Mycorrhiza manual. Springer, Berlin

    Google Scholar 

  • Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovican. Science 289:1920–1921

    CAS  PubMed  Google Scholar 

  • Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. P Natl Acad Sci USA 91:11841–11843

    CAS  Google Scholar 

  • Rhodes LH, Gerdemann JW (1978) Hyphal translocation and uptake of sulfur by vesicular-arbuscular mycorrhizae of onion. Soil Biol Biochem 10:355–360

    CAS  Google Scholar 

  • Rillig MC (2004) Arbuscular mycorrhizae, glomalin and soil aggregation. Can J Soil Sci 84:355–363

    Google Scholar 

  • Rillig MC, Lutgen ER, Ramsey PW, Klironomos JN, Gannon JE (2005) Microbiota accompanying different arbuscular mycorrhizal fungal isolates influence soil aggregation. Pedobiologia 49:251–259

    Google Scholar 

  • Rillig MC, Hoye AT, Carran A (2006) Minimal direct contribution of arbuscular mycorrhizal fungi to DOC leaching in grassland through losses of glomalin-related soil protein. Soil Biol Biochem 38:2967–2970

    CAS  Google Scholar 

  • Ritz K, Newman EI (1985) Evidence for rapid cycling of phosphorus from dying roots to living plants. Oikos 45:174–180

    Google Scholar 

  • Roemheld V, Mueller C, Marschner H (1984) Localization and capacity of proton pumps in roots of intact sunflower, Helianthus annus, plants. Plant Physiol 76:603–606

    CAS  Google Scholar 

  • Schaarschmidt S, González M-C, Roitsch T, Strack D, Sonnewald U, Hause B (2007) Regulation of arbuscular mycorrhization by carbon. The symbiotic interaction cannot be improved by increased carbon availability accomplished by root-specifically enhanced invertase activity. Plant Physiol 143:1827–1840

    CAS  PubMed  Google Scholar 

  • Selosse M-A, Richard F, He X, Simard SW (2006) Mycorrhizal networks: des liaisons dangereuses? Trends Ecol Evol 21:621–628

    PubMed  Google Scholar 

  • Shibata S, Yano K (2003) Phosphorus acquisition from non-labile sources in peanut and pigeonpea with mycorrhizal interaction. Appl Soil Ecol 24:133–141

    Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbioses, 3rd edn. Academic, London

    Google Scholar 

  • Smith FA, Jakobsen I, Smith SE (2000) Spatial differences in acquisition of soil phosphate between two arbuscular mycorrhizal fungi in symbiosis with Medicago truncatula. New Phytol 147:357–366

    Google Scholar 

  • Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespecitve of growth responses. Plant Physiol 133:16–20

    CAS  PubMed  Google Scholar 

  • Smith SE, Smith FA, Jakobsen I (2004) Functional diversity in arbuscular mycorrhizal symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol 162:511–524

    Google Scholar 

  • Smith FA, Grace EJ, Smith SE (2009) More than carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol 182:347–358

    CAS  PubMed  Google Scholar 

  • St-Arnaud M, Hamel C, Vimard B, Caron M, Fortin JA (1996) Enhanced hyphal growth and spore production of the arbuscular mycorrhizal fungus Glomus intraradices in an in vitro system in the absence of host roots. Mycol Res 100:328–332

    Google Scholar 

  • Subramanian KS, Charest C (1999) Acquisition of N by external hyphae of an arbuscular mycorrhizal fungus and its impact on physiological responses in maize under drought-stressed and well-watered conditions. Mycorrhiza 9:69–75

    CAS  Google Scholar 

  • Tanaka Y, Yano K (2005) Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant Cell Environ 28:1247–1254

    CAS  Google Scholar 

  • Thomson BD, Robson AD, Abbott LK (1991) Soil-mediated effects of phosphorus supply on the formation of mycorrhizas by Scutellospora calospora (Nicol. & Gerd.) Walker & Sanders on subterranean clover. New Phytol 118:463–470

    CAS  Google Scholar 

  • Tibbett M (2000) Roots, foraging and the exploitation of soil nutrient patches: the role of mycorrhizal symbiosis. Funct Ecol 14:397–399

    Google Scholar 

  • Torrisi V, Pattinson GS, McGee PA (1999) Localized elongation of roots of cotton follows establishment of arbuscular mycorrhizas. New Phytol 142:103–122

    Google Scholar 

  • Toussaint J-P, St-Arnaud M, Charest C (2004) Nitrogen transfer and assimilation between the arbuscular mycorrhizal fungus Glomus intraradices Schenck & Smith and Ri T-DNA roots of Daucus carota L. in an in vitro compartmented system. Can J Microbiol 50:251–560

    CAS  PubMed  Google Scholar 

  • Treeby MT (1992) The role of mycorrhizal fungi and non-mycorrhizal micro-organisms in iron nutrition of citrus. Soil Biol Biochem 24:857–864

    CAS  Google Scholar 

  • Trotta A, Carminati C, Schellenbaum L, Scannerini S, Fusconi A, Berta G (1991) Correlation between root morphogenesis, VA mycorrhizal infection and phosphorus nutrition. In: McMichael BL, Persson H (eds) Plant roots and their environment. Elsevier, New York

    Google Scholar 

  • Uetake Y, Kojima T, Ezawa T, Saito M (2002) Extensive tubular vacuole system in an arbuscular mycorrhizal fungus, Gigaspora margarita. New Phytol 154:761–768

    Google Scholar 

  • 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 172:739–752

    PubMed  Google Scholar 

  • Van Iren F, Boers-van der Sluijs P (1980) Symplasmic and apoplasmic radial ion transport in plant roots. Planta 148:130–137

    Google Scholar 

  • Vigo C, Norman JR, Hooker JE (2000) Biocontrol of the pathogen Phytophotora parasitica by arbuscular mycorrhizal fungi is a consequence of infection loci. Plant Pathol 49:509–514

    Google Scholar 

  • Voets L, de la Providencia IE, Fernandez K, Ijdo M, Cranenbrouck S, Declerck S (2009) Extraradical mycelium network of arbuscular mycorrhizal fungi allows fast colonization of seedlings under in vitro conditions. Mycorrhiza 19:347–356

    PubMed  Google Scholar 

  • Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51

    CAS  PubMed  Google Scholar 

  • Wang B, Funakoshi DM, Dalpé Y, Hamel C (2002) Phosphorus-32 absorption and translocation to host plants by arbuscular mycorrhizal fungi at low root-zone temperature. Mycorrhiza 12:93–96

    PubMed  Google Scholar 

  • Wang MY, Christie P, Xiao ZY, Qin CP, Wang P, Xie LJF, YC XRX (2008) Arbuscular mycorrhizal enhancement of iron concentration by Poncirus trifoliata L. Raf and Citrus reticulata Blanco grown on sand medium under different pH. Biol Fert Soils 45:65–72

    CAS  Google Scholar 

  • Wardle D, Bardgett R, Klironomos J, Setälä H, Van der Putten W, Wall D (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    CAS  PubMed  Google Scholar 

  • Wright SF, Upadhyaya A (1998) A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant Soil 198:97–107

    CAS  Google Scholar 

  • Wright SF, Franke-Snyder M, Morton JB, Upadhyaya A (1996) Time-course study and partial characterization of a protein on hyphae of arbuscular mycorrhizal fungi during active colonization of roots. Plant Soil 181:193–203

    CAS  Google Scholar 

  • Yano K, Yamauki A, Kono Y (1996) Localized alteration in lateral root development in roots colonized by an arbuscular mycorrhizal fungus. Mycorrhiza 6:409–415

    Google Scholar 

  • Zhang H, Forde B (2000) Regulation of Arabidopsis root development by nitrate availability. J Exp Bot 51:51–59

    CAS  PubMed  Google Scholar 

  • Zhang X-H, Lin A-J, Gao Y-L, Reid RJ, Wong M-H, Zhu Y-G (2009) Arbuscular mycorrhizal colonization increases copper binding capacity of root cell walls of Oryza sativa L. and reduces copper uptake. Soil Biol Biochem 41:930–935

    CAS  Google Scholar 

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  1. Leibniz Institute of Vegetable and Ornamental Crops (IGZ), 14979, Grossbeeren, Germany

    Elke Neumann & Eckhard George

  2. Plant Nutrition, Faculty of Agriculture and Horticulture, Humboldt University Berlin, Berlin, Germany

    Eckhard George

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    Hinanit Koltai

  2. Dept. Agronomy & Natural Resources, Sec. Forestry, Agricultural Research Organization (ARO), Bet Dagan, 50250, Israel

    Yoram Kapulnik

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Neumann, E., George, E. (2010). Nutrient Uptake: The Arbuscular Mycorrhiza Fungal Symbiosis as a Plant Nutrient Acquisition Strategy. In: Koltai, H., Kapulnik, Y. (eds) Arbuscular Mycorrhizas: Physiology and Function. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9489-6_7

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