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Symbiotic Associations

  • Chapter
Plant Physiological Ecology

Abstract

Symbiosis is the “living together” of two or more organisms. In its broadest sense, symbiotic associations include parasitic and commensal as well as mutually beneficial partnerships. As is common in the ecophysiological literature, however, we use the term symbiosis in a narrow sense to refer to mutually beneficial associations between higher plants and microorganisms.

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References

  • Akiyama, K. & Hayashi, H. 2006. Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots. Ann. Bot. 97: 925–931.

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Akkermans, A.D.L. & Hirsch, A.M. 1997. A reconsideration of terminology in Frankia research: A need for congruence. Physiol. Plant. 99: 574–578.

    CAS  Google Scholar 

  • Allen, E.B. & Allen, M.F. 1984. Competition between plants of different successional stages: mycorrhizae as regulators. Can J. Bot. 62: 2625– 2629.

    Google Scholar 

  • Allen, M.F., Allen, E.B., & Friese, C.G. 1989. Responses of the non-mycotrophic plant Salsola kali to invasion by vesicular-arbuscular mycorrhizal fungi. New Phytol. 111: 45–49.

    Google Scholar 

  • Augé, R.M. 2001. Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11: 3–42.

    Google Scholar 

  • Arredondo-Peter, R., Hargrove, M.S., Moran, J.F., Sarath, G., & Klucas, R.V. 1998. Plant hemoglobins. Plant Physiol. 118: 1121–1125.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Baas, R., & Lambers, H. 1988. Effects of vesicular–arbuscular mycorrhizal infection and phosphate on Plantago major ssp. pleiosperma in relation to the internal phosphate concentration. Physiol. Plant. 74: 701–707.

    CAS  Google Scholar 

  • Baas, R., Van der Werf, A., & Lambers, H. 1989. Root respiration and growth in Plantago major as affected by vesicular-arbuscular mycorrhizal infection. Plant Physiol. 91: 227–232.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bacon, C.W. & De Battista, J. 1991. Endophytic fungi of grasses. In: Handbook of applied mycology. Vol. 1: Soil and plants, D.K. Arora, B. Rai, K.G. Mukerji, & G.R. Knudsen (eds). Marcel Dekker, New York, pp 231–256.

    Google Scholar 

  • Bago, B., Pfeffer, P.E., & Shachar-Hill, Y. 2000. Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol. 124: 949–958.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Barker, S.J., Tagu, D., & Delp, G. 1998. Regulation of root and fungal morphogenesis in mycorrhizal symbioses. Plant Physiol. 116: 1201–1207.

    CAS  Google Scholar 

  • Batty, A.L., Dixon, K.W., Brundrett, M.C., & Sivasithamparam, K. 2004. Orchid conservation and mycorrhizal associations. In: Microorganisms in plant conservation and biodiversity, K. Sivasithamparam, K.W. Dixon, & R.L. Barrett (eds). (Kluwer Academic Publishers, Dordrecht, pp. 195–226.

    Google Scholar 

  • Bearden, B. & Petersen, L. 2000. Influence of arbuscular mycorrhizal fungi on soil structure and aggregate stability of a vertisol. Plant Soil 218: 173–183.

    CAS  Google Scholar 

  • Bécard, G., Taylor, L.P., Douds, D.D., Pfeffer, P.E., & Donner, L. 1995. Flavonoids are not necessary plant signal compounds in arbuscular mycorrhizal symbiosis. Mol. Plant-Microbe Interact. 8: 252–258.

    Google Scholar 

  • Bécard, G., Kosuta, S., Tamasloukht M., Sejalon-Delmas, N., & Roux, C. 2004. Partner communication in the arbuscular mycorrhizal interaction. Can. J. Bot. 82: 1186–1197.

    Google Scholar 

  • Besserer, A., Puech-Pagès, V., Kiefer, P., Gomez-Roldan, V., Jauneau, A., Roy, S., Portais, J.-C., Roux, C., Bécard, G., & Séjalon-Delmas, N. 2006. Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol. 4: 1239–1247.

    CAS  Google Scholar 

  • Bethlenfalvay, G.J., Pacovsky, R.S., Bayne, H.G., & Stafford, A.E. 1982. Interactions between nitrogen fixation, mycorrhizal colonization, and host-plant growth in the Phaseolus-Rhizobium-Glomus symbiosis. Plant Physiol. 70: 446–450.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bidartondo, M.I., Burghardt, B., Gebauer, G., Bruns, T.D., Read, D.J. 2004. Changing partners in the dark: isotopic and molecular evidence of ectomycorrhizal liaisons between forest orchids and trees. Proc. R Soc. B: Biol. Sci. 271: 1799–1806.

    CAS  Google Scholar 

  • Black, K. & Osborne, B. 2004. An assessment of photyosynthetic down-regulation in cyanobacteria from the Gunnera-Nostoc symbiosis. New Phytol. 162: 125–132.

    CAS  Google Scholar 

  • Boddey, R.M., Urquiaga, S., Alves, B.J.R., & Reis, V. 2003. Endophytic nitrogen fixation in sugarcane: present knowledge and future applications. Plant Soil 252: 139–149.

    CAS  Google Scholar 

  • Bolan, N.S., Robson, A.D., & Barrow, N.J. 1987. Effect of vesicular-arbuscular mycorrhiza on the availability of iron phosphates to plants. Plant Soil 99: 401–410.

    CAS  Google Scholar 

  • Boller, B.C. & Nösberger, J. 1987. Symbiotically fixed nitrogen from field-grown white and red clover mixed with ryegrass at low levels of 15N-fertilization. Plant Soil 104: 219–226.

    CAS  Google Scholar 

  • Boulet, F. & Lambers, H. 2005. Characterisation of arbuscular mycorrhizal fungi colonisation in cluster roots of shape Hakea verrucosa F. Muell (Proteaceae), and its effect on growth and nutrient acquisition in ultramafic soil. Plant Soil 269: 357–367.

    CAS  Google Scholar 

  • Bouwmeester, H.J., Roux, C., Lopez-Raez, J.A., & Becard, G. 2007. Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci. 12: 224–230.

    CAS  PubMed  Google Scholar 

  • Brown, S.M., Oparka, K.J., Sprent, J.I., & Walsh, K.NB. 1995. Symplasmic transport in soybean root nodules. Soil Biol. Biochem. 27: 387–399.

    CAS  Google Scholar 

  • Brundrett, M.C. 2002. Coevolution of roots and mycorrhizas of land plants. New Phytol. 154: 275–304.

    Google Scholar 

  • Buee, M., Rossignol, M., Jauneau, A., Ranjeva, R., & Bécard, G.2000. The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol. Plant-Microbe Interact. 13: 693–698.

    CAS  PubMed  Google Scholar 

  • Cairney, J.W.G. 2000. Evolution of mycorrhiza systems. Naturwissensch. 87: 467–475.

    CAS  Google Scholar 

  • Cairney, J.W.G. & Ashford, A.E, 2002 Biology of mycorrhizal associations of epacrids (Ericaceae). New Phytol. 154: 305–326.

    Google Scholar 

  • Cairney, J.W.G. & Burke, R.M. 1998. Extracellular enzyme activities of the ericoid mycorrhizal endophyte Hymenoscyphus ericae (Read) Korf & Kernan: their likely roles in decomposition of dead plant tissue in soil. Plant Soil 205: 181–192.

    CAS  Google Scholar 

  • Cameron, D.D., Leake, J.R., & Read, D.J. 2006. Mutualistic mycorrhiza in orchids: evidence from plant-fungus carbon and nitrogen transfers in the green-leaved terrestrial orchid Goodyera repens. New Phytol. 171: 405–416.

    CAS  PubMed  Google Scholar 

  • Catford, J.G., Staehelin, C., Larose, G., Piché, Y., & Vierheilig, H. 2006. Systemically suppressed isoflavonoids and their stimulating effects on nodulation and mycorrhization in alfalfa split-root systems. Plant Soil 285: 257–266.

    CAS  Google Scholar 

  • Cavagnaro, T.R., Smith, F.A., Hay, G., Carne-Cavagnaro, V.L., & Smith, S.E. 2004. Inoculum type does not affect overall resistance of an arbuscular mycorrhiza-defective tomato mutant to colonisation but inoculation does change competitive interactions with wild-type tomato. New Phytol. 161: 485–494.

    Google Scholar 

  • Cavalcante, V.A. & Döbereiner, J. 1988. A new acid-tolerant nitrogen fixing bacterium associated with sugarcane. Plant Soil 108: 23–31.

    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 

  • Christiansen-Weniger, C., Groneman, A.F., & Van Veen, J.A. 1992. Associative N2 fixation and root exudation of organic acids from wheat cultivars of different aluminium tolerance. Plant Soil 139: 167–174.

    CAS  Google Scholar 

  • Clay, K. 1988. Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69: 10–16.

    Google Scholar 

  • Clay, K., Marks, S., & Cheplick, G.P. 1993. Effects of insect herbivory and fungal endophyte infection on competitive interactions among grasses. Ecology 74: 1767–1777.

    Google Scholar 

  • Cohen, E., Okon, Y., Kigel, J., Nur, I., & Henis, Y. 1980. Increase in dry weight and total nitrogen content in Zea mays and Setaria italica associated with nitrogen-fixing Azospirillum. Plant Physiol. 66: 746–749.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Collier, S.C., Yarnes, C.T., & Herman, R.P. 2003. Mycorrhizal dependency of Chihuahuan Desert plants is influenced by life history strategy and root morphology. J. Arid Environ. 55: 223–229.

    Google Scholar 

  • Coronado, C., Zuanazzi, J.A.S., Sallaud, C., Quirion, J.-C., Esnault, R., Husson, H.-P., Kondorosi, A., & Ratet, P. 1995. Alfalfa root flavonoid production is nitrogen regulated. Plant Physiol. 108: 533–542.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Day, D.A. & Copeland, L. 1991. Carbon metabolism and compartmentation in nitrogen-fixing legume nodules. Plant Physiol. Biochem. 29: 185–201.

    CAS  Google Scholar 

  • Dewan, M.M. & Sivasithamparam, K. 1988. A plant-growth-promoting sterile fungus from wheat and rye-grass roots with potential for suppressing take-all. New Phytol. 91: 687–692.

    Google Scholar 

  • Diaz, C.L., Melchers, L.S., Hooykaas, P.J.J., Lugtenberg, B.J.J., & Kijne, J.W. 1989. Root lectin as a determinant of host-plant specificity in the Rhizobium-legume symbiosis. Nature 338: 579–581.

    CAS  Google Scholar 

  • Dobbelaere, S., Croonenebosch, A., Thys, A., Vande Broek, A., Vanderleyden, J. 1999. Phytostimulatory effect of Azospirillum brasiliense wild type and mutant strains altered in IAA production on wheat. Plant Soil 212: 155–164.

    CAS  Google Scholar 

  • Dong, Z., Canny, M.J., McCully, M.E., Roboredo, M.R., Cabadilla, C.F., Ortega, E., & Rodes, R. 1994. A nitrogen-fixing endophyte of sugarcane stems. A new role for the apoplast. Plant Physiol. 105: 1139–1147.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Douds, D.D., Johnson, C.R., & Koch, K.E. 1988. Carbon cost of the fungal symbiont relative to net leaf P accumulation in a split-root VA mycorrhizal symbiosis. Plant Physiol. 86: 491–496.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Duc, G., Trouvelot, A., Gianinazzi-Pearson, V., & Gianinazzi, S. 1989. First report of non-mycorrhizal plant mutants (Myc) obtained in pea (Pisum sativum) and fababean (Vicia faba L.). Plant Sci. 60: 215–222.

    Google Scholar 

  • Eissenstat, D.M. 1990. A comparison of phosphorus and nitrogen transfer between plants of different phosphorus status. Oecologia 82: 342–347.

    Google Scholar 

  • Eissenstat, D.M., Graham, J.H., Syvertsen, J.P., & Drouillard, D.L. 1993. Carbon economy of sour orange in relation to mycorrhizal colonization and phosphorus status. Ann. Bot. 71: 1–10.

    CAS  Google Scholar 

  • 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: 57–63.

    CAS  Google Scholar 

  • Ezawa, T., Smith, S.E., & Smith, F.A. 2002. P metabolism and transport in AM fungi. Plant Soil 244: 221–230.

    CAS  Google Scholar 

  • Ferrol, N., Pozo, M., Antelo, M., & Azcón-Aguilar, C. 2002. Arbuscular mycorrhizal symbiosis regulates plasma membrane H+-ATPase gene expression in tomato plants. J. Exp. Bot. 53: 1683–1687.

    CAS  PubMed  Google Scholar 

  • Fischer Walter, L.E., Hartnett, D.C., Hetrick, B.A.D., & Schwab, A.P. 1996. Interspecific nutrient transfer in a tallgrass prairie plant community. Am. J. Bot. 83: 180–184.

    Google Scholar 

  • Francis, R. & Read, D.J. 1994. The contribution of mycorrhizal fungi to the determination of plant community structure. Plant Soil 159: 11–25.

    Google Scholar 

  • Fredeen, A.L. & Terry, N. 1988. Influence of vesicular-arbuscular mycorrhizal infection and soil phosphorus level on growth and carbon metabolism of soybean. Can. J. Bot. 66: 2311–2316.

    Google Scholar 

  • Gadkar, V., David-Schwartz, R., Kunik, T., and Kapulnik, Y. 2001. Arbuscular mycorrhizal fungal colonization. Factors involved in host recognition. Plant Physiol. 127: 1493–1499.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gault, R.R., Peoples, M.B., Turner, G.L., Lilley, D.M., Brockwell, J., & Bergersen, F.J. 1995. Nitrogen fixation by irrigated lucerne during the first three years after establishment. Aust. J. Agric. Res. 56: 1401–1425.

    Google Scholar 

  • Gebauer, G. & Meyer, M. 2003. 15N and 13C natural abundance of autotrophic and mycoheterotrophic orchids provides insight into nitrogen and carbon gain from fungal association. New Phytol. 160: 2209–2223.

    Google Scholar 

  • Genre, A. & Bonfante, P. 2005. Building a mycorrhizal cell: How to reach compatibility between plants and arbuscular mycorrhizal fungi. J. Plant Interact. 1: 3–13.

    CAS  Google Scholar 

  • Geurts, R. & Bisseling, T. 2002. Rhizobium Nod factor perception and signalling. Plant Cell 14: 239–249.

    Google Scholar 

  • Giraud, E., Moulin, L., Vallenet, D., Barbe, V., Cytryn, E., Avarre, J.-C., Jaubert, M., Simon, D., Cartieaux, F., Prin, Y., Bena, G., Hannibal, L., Fardoux, J., Kojadinovic, M., Vuillet, L., Lajus, A., Cruveiller, S., Rouy, Z., Mangenot, S., Segurens, B., Dossat, C., Franck, W.L., Chang, W.-S., Saunders, E., Bruce, D., Richardson, P., Normand, P., Dreyfus, B., Pignol, D., Stacey, G., Emerich, D., Vermeglio, A., Medigue, C., & Sadowsky, M. 2007. Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science 316: 1307–1312.

    Google Scholar 

  • Glassop, D., Smith, S.E., & Smith, F.W. 2005. Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222: 688–698.

    CAS  PubMed  Google Scholar 

  • Govindarajulu, M., Pfeffer, P., Jin, H., Abubaker, J., Douds, D., Allen, J.W., Bucking, H., Lammers, P., & Shachar Hill, Y. 2005. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435: 819–823.

    CAS  PubMed  Google Scholar 

  • Graham, J.H., Eissenstat, D.M., & Drouillard, D.L. 1991. On the relationship between a plant’s mycorrhizal dependency and rate of vesicular-arbuscular mycorrhizal colonization. Funct. Ecol. 5: 773–779.

    Google Scholar 

  • Grimoldi, A.A., Kavanová, M., Lattanzi, F.A., & Schnyder, H. 2005. Phosphorus nutrition-mediated effects of arbuscular mycorrhiza on leaf morphology and carbon allocation in perennial ryegrass. New Phytol. 168: 435–444.

    CAS  PubMed  Google Scholar 

  • Grimoldi, A.A., Kavanová, M., Lattanzi, F.A., Schaufele, R., & Schnyder, H. 2006. Arbuscular mycorrhizal colonization on carbon economy in perennial ryegrass: quantification by 13CO2/12CO2 steady-state labelling and gas exchange. New Phytol. 172: 544–553.

    CAS  PubMed  Google Scholar 

  • Gualtieri, G. & Bisseling, T, 2000. The evolution of nodulation. Plant Mol. Biol. 42: 181–194.

    CAS  PubMed  Google Scholar 

  • Handley, L.L. & Raven, J.A. 1992. The use of natural abundance of nitrogen isotopes in plant physiology and ecology. Plant Cell Environ. 15: 965–985.

    CAS  Google Scholar 

  • Handley, L.L., Daft, M.J., Wilson, J., Scrimgeour, C.M., Ingelby, K., & Sattar, M.A. 1993. Effects of the ectoand VA-mycorrhizal fungi Hydnagium carneum and Glomus clarum on the δ15N and δ13C values of Eucalyptus globulus and Ricinus communis. Plant Cell Environ. 16: 375–382.

    CAS  Google Scholar 

  • Harrison, M.J. 1999. Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 361–389.

    CAS  PubMed  Google Scholar 

  • Harrison, M.J. 2005. Signaling in the arbuscular mycorrhizal symbiosis. Annu. Rev. Microbiol. 59: 19–42.

    CAS  PubMed  Google Scholar 

  • Harrison, M., & Dixon, R. 1994. Spatial patterns of expression of flavonoid/isoflavonoid pathway genes during interactions between roots of Medicago truncatula and the mycorrhizal fungus Glomus versiforme. Plant J. 6: 9–20.

    CAS  Google Scholar 

  • Hartnett, D.C. & Wilson, G.W.T. 2002. The role of mycorrhizas in plant community structure and dynamics: lessons from grasslands. Plant Soil 244: 319–331.

    CAS  Google Scholar 

  • Hause, B. & Fester, T. 2005. Molecular and cell biology of arbuscular mycorrhizal symbiosis. Planta 221: 184–196.

    CAS  PubMed  Google Scholar 

  • He, X., Critchley, C., Ng, H., & Bledsoe, C. 2004. Reciprocal N (15NH4 + or 15NO3 ) transfer between nonN2–fixing Eucalyptus maculata and N2-fixing Casuarina cunninghamiana linked by the ectomycorrhizal fungus Pisolithus sp. New Phytol. 163: 692–640.

    Google Scholar 

  • He, X., Critchley, C., Ng, H., & Bledsoe, C. 2005. Nodulated N2–fixing Casuarina cunninghamiana is the sink for net N transfer from non-N2-fixing Eucalyptus maculata via an ectomycorrhizal fungus Pisolithus sp. using 15NH4 + or 15NO3 supplied as ammonium nitrate. New Phytol. 167: 897–912.

    CAS  PubMed  Google Scholar 

  • Hobbie, E.A. 2006. Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. Ecology 87: 563–569.

    PubMed  Google Scholar 

  • Högberg, P. 1990. 15N natural abundance as a possible marker of the ectomycorrhizal habit of trees in mixed African woodlands. New Phytol. 115: 483–486.

    Google Scholar 

  • Hungate, B.A., Stiling, P.D., Dijkstra, P., Johnson, D.W., Ketterer, M.E., Hymus, G.J., Hinkle, C.R., & Drake, B.G. 2004. CO2 elicits long-term decline in nitrogen fixation. Science 304: 1291.

    CAS  PubMed  Google Scholar 

  • Hunt, S., & Layzell, D.B. 1993. Gas exchange of legume nodules and the regulation of nitrogenase activity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44: 483–511.

    CAS  Google Scholar 

  • Hutton, B.J., Dixon, K.W., & Sivasithamparam, K. 1994. Ericoid endophytes of Western Australian heaths (Epacridaceae). New Phytol. 127: 557–655.

    Google Scholar 

  • Hutton, B.J., Sivasithamparam, K., Dixon, K.W., & Pate, J.S. 1996. Pectic zymograms and water stress tolerance of endophytic fungi isolated from Western Australian heaths (Epacridaceae). Ann. Bot. 77: 399–404.

    CAS  Google Scholar 

  • Israel. D.W. 1987. Investigation of the role of phosphorus in symbiotic dinitrogen fixation. Plant Physiol. 84: 835–840.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jakobsen, I. & Rosendahl, L. 1990. Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytol. 115: 77–83.

    Google Scholar 

  • James, E.K., Reis, V.M., Olivars, F.L., Baldani, J.I., & Döbereiner, J. 1994.. Infection of sugar cane by the nitrogen-fixing bacterium Acetobacter diazotrophicus. J. Exp. Bot. 45: 757–766.

    CAS  Google Scholar 

  • Javot, H., Pumplin, N., & Harrison, M.J. 2007. Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ. 30: 310–322.

    CAS  PubMed  Google Scholar 

  • Jin, H., Pfeffer, P.E., Douds, D.D., Piotrowski, E., Lammers, P.J., Shachar-Hill, Y. 2005. The uptake, metabolism, transport and transfer of nitrogen in an arbuscular mycorrhizal symbiosis. New Phytol. 168: 687–696.

    CAS  PubMed  Google Scholar 

  • Johansen, A. & Jensen, E.S. 1996. Transfer of N and P from intact or decomposing roots of pea to barley interconnected by an arbuscular mycorrhizal fungus. Soil Biol. Biochem. 28: 73–81.

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Johnson, N.C., Graham, J.H., & Smith, F.A. 1997. Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol. 135: 575–585.

    Google Scholar 

  • Joner, E.J. & Jakobsen, I. 1995. Uptake of 32P from labelled organic matter by mycorrhizal and non-mycorrhizal subterranean clover ((Trifolium subterraneum L.). Plant Soil 172: 221–227.

    CAS  Google Scholar 

  • Joner, E.J., Van Aarle, I.M., & Vosatka, M. 2000a. Phospatase activity of extra-radical arbuscular mycorrhizal hyphae: a review. Plant Soil 226: 199–210.

    CAS  Google Scholar 

  • Joner, E.J., Ravnskov, S., & Jakobsen, I. 200b. Arbuscular mycorrhizal phosphate transport under monoxenic conditions using radio-labelled inorganic and organic phosphate. Biotechnol. Lett. 22: 1705–1708.

    Google Scholar 

  • Jongmans, A.G., Van Breemen, N., Lundström, U., Van Hees, P.A.W., Finlay, R.D., Srinivasan, M., Unestam, T., Giesler, R., Melkerud, P.-A., & Olsen, M. 1997. Rock-eating fungi. Nature 389: 682–683.

    CAS  Google Scholar 

  • Kaiser, B.N., Layzell, D.B., & Shelp, B.J. 1997. Role of oxygen limitation and nitrate metabolism in the nitrate inhibition of nitrogen fixation by pea. Physiol. Plant. 101: 45–50.

    CAS  Google Scholar 

  • Karandashov, V. & Bucher, M. 2005. Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci. 10: 22–29.

    CAS  PubMed  Google Scholar 

  • Kearns, A., Whelan, J., Young, S., Elthon, T.E., & Day, D.A. 1992. Tissue-specific expression of the alternative oxidase in soybean and siratro. Plant Physiol. 99: 712–717.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kennedy, I.R. & Tchan, Y.-T. 1992. Biological nitrogen fixation in non-leguminous field crops: Recent advances. Plant Soil 141: 93–118.

    CAS  Google Scholar 

  • Khaosaad, T., Garcia-Garrido, J.M., Steinkellner, S., & Vierheilig, H. 2007. Take-all disease is systemically reduced in roots of mycorrhizal barley plants. Soil Biol. Biochem. 39: 727–734.

    CAS  Google Scholar 

  • Klironomos, J.N. & Hart, M.M 2001. Animal nitrogen swap for plant carbon. Nature 410: 651–652.

    CAS  PubMed  Google Scholar 

  • Klironomos, J.N. Bednarczuk E. M., & Neville J. 1999. Reproductive significance of feeding on saprobic and arbuscular mycorrhizal fungi by the collembolan, Folsomia candida Funct. Ecol. 13: 756–761.

    Google Scholar 

  • Koch, K.E. & Johnson, C.R. 1984. Photosynthetic partitioning in split-root citrus seedlings with mycorrhizal and nonmycorrhizal root systems. Plant Physiol. 75: 26–30.

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Koide, R.T. & Schreiner, R.P. 1992. Regulation of the vesicular-arbuscular mycorrhizal symbiosis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43: 557–581.

    CAS  Google Scholar 

  • Koide, R.T., Huenneke, L.F., Hamburg, S.P., & Mooney, H.A. 1988. Effects of applications of fungicide, phosphorus and nitrogen on the structure and productivity of an annual serpentine plant community. Funct. Ecol. 2: 335–344.

    Google Scholar 

  • Kwon, D.-K. & Beevers, H. 1992. Growth of Sesbania rostrata (Brem) with stem nodules under controlled conditions. Plant Cell Environ. 15: 939–945.

    Google Scholar 

  • Lambers, H., Atkin, O.K., & Millenaar, F.F. 2002. Respiratory patterns in roots in relation to their functioning. In: Plant roots: the hidden half, 3rd edition. Y. Waisel, A. Eshel, & U. Kafkaki (eds). Marcel Dekker, New York, pp. 521–552.

    Google Scholar 

  • Lambers, H., Shane, M.W., Cramer, M.D., Pearse, S.J., & Veneklaas, E.J. 2006. Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann. Bot. 98: 693–713.

    PubMed Central  PubMed  Google Scholar 

  • Lambers, H., Shaver, G., Raven, J.A., & Smith, S.E. 2008. N- and P-acquisition change as soils age. Trends Ecol. Evol., in press.

    Google Scholar 

  • Landeweert, R., Hoffland, E., Finlay, R.D., Kuyper, T.W., & Van Breemen, N. 2001. Trends Ecol. Evol. 16: 248–253.

    PubMed  Google Scholar 

  • Leake, J.R. 2004. Myco-heterotroph/epiparasitic plant interactions with ectomycorrhizal and arbuscular mycorrhizal fungi. Curr. Opin. Plant Biol. 7: 422–428.

    CAS  PubMed  Google Scholar 

  • Leake, J.R. & Read, D.J. 1989. The biology of mycorrhiza in the Ericaceae. New Phytol. 112: 69–76.

    CAS  Google Scholar 

  • LePage, B.A., Currah, R.S., Stockey, R.A., & Rothwell, G.W. 1997. Fossil ectomycorrhizae from the middle Eocene. Am. J. Bot. 84: 410–412.

    CAS  PubMed  Google Scholar 

  • Li, H-Y., Smith, S.E., Holloway, R.E., Zhu, Y-G., & Smith, F.A. 2006. Arbuscular mycorrhizal (AM) fungi contribute to phosphorus uptake by wheat grown in a phosphorus-fixing soil even in the absence of positive growth responses. New Phytol. 172: 536–543.

    CAS  PubMed  Google Scholar 

  • Limpens, E. & Bisseling, T. 2003. Signaling in symbiosis. Curr. Opin. Plant Sci. 6: 343–350.

    CAS  Google Scholar 

  • Lindblad, P., Atkins, C.A., & Pate, J.S. 1991. N2-fixation by freshly isolated Nostoc from coralloid roots of the cycad Macrozamia riedlei (Fisch. ex Gaud.) Gardn. Plant Physiol. 95: 753–759.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lodwig, E. & Poole, P. 2003. Metabolism of Rhizobium bacteroids. Crit. Rev. Plant Sci. 22: 37–78.

    CAS  Google Scholar 

  • Martin, F., Duplessis, S., Ditengou, F., Lagrange, H., Voiblet, C., & Lapeyrie, F. 2001. Developmental cross talking in the ectomycorrhizal symbiosis: signals and communication genes. New Phytol. 152: 145–154.

    Google Scholar 

  • Marschner, H. & Dell, B. 1994. Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159: 89–102.

    CAS  Google Scholar 

  • Marulanda, A., Azcon, R., & Ruiz-Lozano, J.M. 2003. Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa plants under drought stress. Physiol. Plant. 119: 526–533.

    CAS  Google Scholar 

  • Massicotte, H.B. , Melville, L.H., Peterson, R.L., Unestam, T. 1999. Comparative studies of ectomycorrhiza formation in Alnus glutinosa and Pinus resinosa with Paxillus involutus. Mycorrhiza 8: 229–240.

    Google Scholar 

  • Maxwell, C.A., Hartwig, U.A., Joseph, C.M., & Phillips, D.A. 1989. A chalcone and two related flavonoids released from alfalfa roots induce nod genes of Rhizobium meliloti. Plant Physiol. 91: 842–847.

    CAS  PubMed Central  PubMed  Google Scholar 

  • McNeill, A.M. & Wood, M. 1990. Fixation and transfer of nitrogen by white clover to ryegrass. Soil Use Manage. 6: 84–86.

    Google Scholar 

  • Mellor, R.B. & Collinge, D.B. 1995. A simple model based on known plant defence reactions is sufficient to explain most aspects of nodulation. J. Exp. Bot. 46: 1–18.

    CAS  Google Scholar 

  • Mergaert, P., Uchiumi T. Uchiumi, Alunni, B., Evanno, G., Cheron, A., Catrice, O., Mausset, A.-E., Barloy-Hubler, F., Galibert, F., Kondorosi, A., & Kondorosi, E. 2006. Eukaryotic control on bacterial cell cycle and differentiation in the rhizobium-legume symbiosis. Proc. Natl. Acad. Sci. USA 103: 5230–5235.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mouritzen, P. & Rosendahl, L. 1997. Identification of a transport mechanism for NH4 + in the symbiosome membrane of pea root nodules. Plant Physiol. 115: 519–526.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Muthukumar, T. Udaiyan, K., & Shanmughavel, P. 2004. Mycorrhiza in sedges—an overview. Mycorrhiza 14: 65–77.

    CAS  PubMed  Google Scholar 

  • Mylona, P., Pawlowski, K., & Bisseling, T. 1995. Symbiotic nitrogen fixation. Plant Cell 7: 869–885.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nadelhoffer, K., Shaver, G., Fry, B., Giblin, A., Johnson, L., & McKane, R. 1996. 15N natural abundances and N use by tundra plants. Oecologia 107: 386–394.

    Google Scholar 

  • Newman, E.I., Eason, W.R., Eissenstat, D.M., & Ramos, M.I.F.R. 1992. Interactions between plants: the role of mycorrhizae. Mycorrhiza 1: 47–53.

    Google Scholar 

  • Nicholson, T. 1975. Evolution of vesicular-arbuscular mycorrhizas. In: Endomycorrhizas, F.E. Sanders, B. Mosse, & P.B. Tinker (eds). Academic Press, London, pp. 25–34.

    Google Scholar 

  • O’Connor, P.J., Smith, S.E., & Smith, F.A. 2002. Arbuscular mycorrhizas influence plant diversity and community structure in a semiarid herbland. New Phytol. 154: 209–218.

    Google Scholar 

  • Oldroyd, G.E.D., Harrison, M.J., & Udvardi, M. 2005. Peace talks and trade deals. Keys to long-term harmony in legume-microbe symbioses. Plant Physiol. 137: 1205–1210.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Palus, J.A., Borneman, J., Ludden, P.W., & Triplett, E.W. 1996. A diazotrophic bacterial endophyte isolated from stems of Zea mays L. and Zea luxurians Iltis and Doebley. Plant Soil 186: 135–142.

    CAS  Google Scholar 

  • Paszkowski, U. 2006. Mutualism and parasitism: the yin and yang of plant symbioses. Curr. Opin. Plant Biol. 9: 364–370.

    PubMed  Google Scholar 

  • Pate, J.S., Lindblad, P., & Atkins, C.A. 1988. Pathway of assimilation and transfer of fixed nitrogen in coralloid roots of cycad-Nostoc symbioses. Planta 176: 461–471.

    CAS  PubMed  Google Scholar 

  • Paynel, F., Murray, P.J., & Cliquet, J.B. 2001. Root exudates: a pathway for short-term N transfer from clover and ryegrass. Plant Soil 229: 235–243.

    CAS  Google Scholar 

  • Penas, J.I., Sanchez-Diaz, M., Aguirreola, J., & Becana, M. 1988. Increased stress tolerance of nodule activity in Medicago-Rhizobium-Glomus symbiosis under drought. J. Plant Physiol. 79: 79–83.

    Google Scholar 

  • Peng, S., Eissenstat, D.M., Graham, J.H., Williams, K., & Hodge, N.C. 1993. Growth depression in mycorrhizal citrus at high-phosphorus supply. Analysis of carbon costs. Plant Physiol. 101: 1063–1071.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Peoples, M.B., Herridge, D.F., & Ladha, J.K. 1995. Biological nitrogen fixation: an efficient source of nitrogen for sustainable agricultural production? Plant Soil 174: 3–28.

    CAS  Google Scholar 

  • Peoples, M.B., Palmer, B., Lilley, D.M., Duc, L.M., & Herridge, D.F. 1996. Application of 15N and xylem ureide methods for assessing N2 fixation of three shrub legumes periodically pruned for forage. Plant Soil 182: 125–137.

    CAS  Google Scholar 

  • Peterson, R.L. & Bonfante, P. 1994. Comparative structure of vesicular-arbuscular mycorrhizas and ectomycorrhizas. Plant Soil 159: 79–88.

    Google Scholar 

  • Pfeffer, P.E., Douds, D.D. Jr, Bücking, H., Schwartz, D.P., & Shachar-Hill, Y. 2004. The fungus does not transfer carbon to or between roots in an arbuscular mycorrhizal symbiosis. New Phytol. 163: 617–627.

    Google Scholar 

  • Phillips, D.A., Dakora, F.D., Sande, E., Joseph, C.M., & Zon, J. 1994. Synthesis, release, and transmission of alfalfa signal to rhizobial symbionts. Plant Soil. 161: 69–80.

    CAS  Google Scholar 

  • Pingret, J.-L., Journet, E.-P., & Barker, D.G. 1998. Rhizobium Nod factor signaling: Evidence for a G protein-mediated transduction mechanism. Plant Cell 10: 659–671.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Radutoiu, S, Madsen, Madsen, E.B., Felle, H.H., Umehara, Y., Gronlund, M., Sato, S., Nakamura, Y., Tabata, S., Dandal, N., & Stougaard, J. 2003. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425: 585–592.

    CAS  PubMed  Google Scholar 

  • 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: 462–466.

    CAS  PubMed  Google Scholar 

  • Read, D.J. 1996. The structure and function of the ericoid mycorrhizal root. Ann. Bot. 77: 365–374.

    CAS  Google Scholar 

  • Read, D.J. & Perez-Moreno, J. 2003. Mycorrhizas and nutrient cycling in ecosystems – a journey towards relevance? New Phytol. 157: 475–492.

    Google Scholar 

  • Reddell, P., Yun, Y., & Shipton, W.A. 1997. Cluster roots and mycorrhizae in Casuarina cunninghamiana: their occurrence and formation in relation to phosphorus supply. Aust. J. Bot. 45: 41–51.

    Google Scholar 

  • 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.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Richardson, A.E., Djordjevic, M.A., Rolfe, B.G., & Simpson, R.J. 1988. Effects of pH, Ca and Al on the exudation from clover seedlings of compounds that induce the expression of nodulation genes in Rhizobium trifolii. Plant Soil 109: 37–47.

    CAS  Google Scholar 

  • Rousseau, J.V.D. & Reid, C.P.P. 1991. Effects of phosphorus fertilization and mycorrhizal development on phosphorus nutrition and carbon balance of loblolly pine. New Phytol. 92: 75–87.

    Google Scholar 

  • Ryle, G.J.A. Powell, C.E., & Gordon, A.J. 1985. Short-term changes in CO2-evolution associated with nitrogenase activity in white clover in response to defoliation and photosynthesis. J. Exp. Bot. 36: 634–643.

    CAS  Google Scholar 

  • Sanchez-Diaz, M., Pardo, M., Antolin, M., Pena, J., & Aguirreola, J. 1990. Effect of water stress on photosynthetic activity in the Medicago-Rhizobium-Glomus symbiosis. Plant. Sci. 71: 215–221.

    Google Scholar 

  • Sanders, I.R. & Koide, R.T. 1994. Nutrient acquisition and community structure in co-occurring mycotrophic and non-mycotrophic old-field annuals. Funct. Ecol. 8: 77–84.

    Google Scholar 

  • Santana, M.A., Pihakaski-Maunschbach, K., Sandal, N., Marcker, K.A., & Smith, A.G. 1998. Evidence that the plant host synthesizes the heme moiety of leghemoglobin in root nodules. Plant Physiol. 116: 1259–1269.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Scervino, J.M., Ponce, M.A., Erra-Bassells, R., Vierheilig, H, Ocampo, J.A., & Godeas, A. 2005. Flavonoids exclusively present in mycorrhizal roots of white clover exhibit a different effect on arbuscular mycorrhizal fungi than flavonoids exclusively present in non-mycorrhizal roots of white clover. J. Plant Interact. 1: 15–22.

    CAS  Google Scholar 

  • Schulze, E.-D., Chapin III, F.S., & Gebauer, G. 1995. Nitrogen nutrition and isotope differences among life forms at the northern treeline of Alaska. Oecologia 100: 406–412.

    Google Scholar 

  • Selosse, M.-A., Richard, F., He, X., & Simard, S.W. 2006. Mycorrhizal networks: des liaisons dangereuses? Trends Ecol Evol. 21: 621–628.

    PubMed  Google Scholar 

  • Shirtliffe, S.J. & Vessey J.K. 1996. A nodulation (Nod+/Fix-) mutant of Phaseolus vulgaris L. has nodules lacking peripheral vascular bundles (Pvb) and is resistant to mycorrhizal infection (Myc). Plant Sci. 118: 209–220.

    CAS  Google Scholar 

  • Smith, S.E. & Gianinazzi-Pearson, V. 1988. Physiological interactions between symbionts in vesicular-arbuscular mycorrhizal plants. Annu. Rev. Plant Physiol. Mol. Biol. 39: 221–244.

    CAS  Google Scholar 

  • Smith, S.E. & Read, D.J. 2008. Mycorrhizal symbiosis, 3rd edition. Elsevier, City.

    Google Scholar 

  • Smith, S.E., Smith, F.A., & Jakobsen, I. 2003. Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol. 133: 16–20.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Smith, S.E., Smith, F.A., & 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: 511–524.

    Google Scholar 

  • Snellgrove, R.C., Splittstoesser, W.E., Stribley, D.P., & Tinker, P.B. 1982. The distribution of carbon and the demand of the fungal symbiont in leek plants with vesicular-arbuscular mycorrhizas. New Phytol. 92: 75–87.

    Google Scholar 

  • Spaink, H.P. 1995. The molecular basis of infection and nodulation by rhizobia: the ins and outs of sympathogenesis. Annu. Rev. Phytopathol. 33: 345–368.

    CAS  PubMed  Google Scholar 

  • Sprent, J.I. 1999. Nitrogen fixation and growth of npn-crop legume species in diverse environments. Persp. Plant Ecol. Evol. Syst. 2: 149–162.

    Google Scholar 

  • Sprent, J.I. 2007. Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytol. 174: 11–25.

    CAS  PubMed  Google Scholar 

  • Sprent, J.I. & James, E.K. 2007. Legume evolution: where do nodules and mycorrhizas fit in? Plant Physiol. 144: 575–581.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sprent, J.I., Geoghegan, I.E., Whitty, P.W., & James, E.K. 1996. Natural abundance of 15N and 13C in nodulated legumes and other plants in the cerrado and neighbouring regions of Brazil. Oecologia 105: 440–446.

    Google Scholar 

  • Sturz, A.V. 1995. The role of endophytic bacteria during seed piece decay and potato tuberization. Plant Soil 172: 257–263.

    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 

  • Temperton, V.M., Mwangi, P.N., Scherer-Lorenzen, M., Schmid, B., & Buchmann, N. 2007. Positive interactions between nitrogen-fixing legumes and four different neighbouring species in a biodiversity experiment. Oecologia 151: 190–205.

    PubMed  Google Scholar 

  • Thingstrup, I., Rubaek, G., Sibbesen, E., & Jakomsen, I. 1998. Flax (Linum usitatissimum L.) depends on arbuscular mycorrhizal fungi for growth and P uptake at intermediate but not high soil P levels. Plant Soil 203: 37–46.

    CAS  Google Scholar 

  • Thompson, B.D., Robson, A.D., & Abbott, L.K. 1986. Effects of phosphorus on the formation of mycorrhizas by Gigaspora calospora and Glomus fasciculatum in relation to root carbohydrates. New Phytol. 103: 751–765.

    Google Scholar 

  • Tisdall, J.M. 1994. Possible role of soil microorganisms in aggregation in soils. Plant Soil 159: 115–121.

    Google Scholar 

  • Tobar, R., Azcón, R., & Barea, J.-M. 1994. Improved nitrogen uptake and transport from 15N-labelled nitrate by external hyphae of arbuscular mycorrhiza under water-stressed conditions. New Phytol. 126: 119–122.

    Google Scholar 

  • Triplett, E.W. 1996. Diazotrophic endophytes: progress and prospects for nitrogen fixation in monocots. Plant Soil 186: 29–38.

    CAS  Google Scholar 

  • Turnbull, M.H., Goodall, R., & Stewart, G.R. 1995. The impact of mycorrhizal colonization upon nitrogen source utilization and metabolism in seedlings of Eucalyptus grandis Hill ex Maiden and Eucalyptus maculata Hook. Plant Cell Environ. 18: 1386–1394.

    CAS  Google Scholar 

  • Van Brussel, A.A.N., Tak, T., Boot, K.J.M., & Kijne, J.W. 2002. Autoregulation of root nodule formation: signals of both symbiotic partners studied in a split-root system of Vicia sativa subsp. nigra. Mol. Plant-Microbe Interact. 15: 341–349.

    Google Scholar 

  • Van Groenigen, K.-J., Six, J., Hungate, B.A., De Graaff, M.-A., Van Breemen, N., & Van Kessel, C. 2006. Element interactions limit soil carbon storage. Proc. Natl. Acad. Sci. USA 103: 6571–6574.

    PubMed Central  PubMed  Google Scholar 

  • Vance, C.P. 2002. Root-bacteria interactions. Symbiotic nitrogen fixation. In: Plant roots: the hidden half, 3rd edition, Y. Waisel, A. Eshel, & U. Kafkaki (eds). Marcel Dekker, New York, pp. 839–868.

    Google Scholar 

  • Van der Heijden, M.G.A., Klironomos, J.N., Ursic, M., Moutoglis, P., Streitwolf-Engel, R., Boller, T., Wiemken, A., & Sanders, I.R. 1998a. Mycorrhizal fungal diversity determines plant diversity, ecosystem variability and productivity. Nature 396: 69–72.

    Google Scholar 

  • Van der Heijden, M.G.A., Boller, T., Wiemken, A., & Sanders, I.R. 1998b Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79: 2082–2091.

    Google Scholar 

  • Van Ghelue, M., Løvaas, E., Ringø, E. & Solheim, B. 1997. Early interactions between Alnus glutinosa and Frankia strain ArI3. Production and specificity of root hair deformation factor(s). Physiol. Plant. 99: 579–587.

    Google Scholar 

  • Van Hees, P.A.W., Rosling, A., Essén, S., Godbold D.L., Jones, D.L., & Finlay R.D. 2006. Oxalate and ferricrocin exudation by the extramatrical mycelium of an ectomycorrhizal fungus in symbiosis with Pinus sylvestris. New Phytol. 169: 367–378.

    PubMed  Google Scholar 

  • Van Leerdam, D. M., Williams, P. A., & Cairne, J. W. G. 2001. Phosphate-solubilising abilities of ericoid mycorrhizal endophytes of Woollsia pungens (Epacridaceae). Aust. J. Bot. 49: 75–80.

    Google Scholar 

  • Van Rhijn, P & Vanderleyden, J. 1995. The Rhizobium-plant symbiosis. Microbiol. Rev. 59: 124–142.

    PubMed Central  PubMed  Google Scholar 

  • Vessey, J.K. 1994. Measurement of nitrogenase activity in legume root nodules: in defence of the acetylene reduction assay. Plant Soil 158: 151–162.

    CAS  Google Scholar 

  • Vessey, J.K., Pawlowski, K., & Bergman, B. 2005. N2-fixing symbiosis: legumes, actinorhizal plants, and cycads. Plant Soil 274: 51–78.

    CAS  Google Scholar 

  • Vierheilig, H., Iseli, B., Alt, M., Raikhel, N., Wiemken, A., & Boller, T. 1996. Resistance of Urtica dioica to mycorrhizal colonization: a possible involvement of Urtica dioica agglutinin. Plant Soil 183: 131–136.

    CAS  Google Scholar 

  • Vierheilig, H., Bago, B., Albrecht, C., Poulin, M.-J., & Piché, Y. 1998. Flavonoids and arbuscular-mycorrhizal fungi. In: Flavonoids in the living system, J. Manthey & B. Buslig (eds). Plenum Press, New York, pp. 9–33.

    Google Scholar 

  • Vierheilig, H. Garcia-Garrido, J.M., Wyss, U., & Piché, Y. 2000. Systemic suppression of mycorrhizal colonization of barley roots already colonized by AM fungi. Soil Biol. Biochem. 32: 589–595.

    CAS  Google Scholar 

  • Volpin, H., Elkind, Y., Okon, Y., & Kapulnik, Y. 1994. A vesicular arbuscular mycorrhizal fungus (Glomus intraradices) induces a defense response in alfalfa roots. Plant Physiol. 104: 683–689.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wallander, H. 2000. Uptake of P from apatite by Pinus sylvestris seedlings colonised by different ectomucorrhizal fungi. Plant Soil 218: 249–256.

    CAS  Google Scholar 

  • Wang, B. & Qiu, Y.-L. 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16: 299–363.

    CAS  PubMed  Google Scholar 

  • Webster, G., Gough, C., Vasse, J., Batchelor, C.A., O’Callaghan, K.J., Kothari, S.L., Davey, M.R., Dénarié, J., Cocking, E.C. 1997. Interactions of rhizobia with rice and wheat. Plant Soil 194: 115–122.

    CAS  Google Scholar 

  • Wei, H. & Layzell, D.B. 2006. Adenylate-coupled ion movement. A mechanism for the control of nodule permeability to O2 diffusion. Plant Physiol. 141: 280–287.

    CAS  PubMed Central  PubMed  Google Scholar 

  • White, J., Prell, J., James, E.K., Poole, P. 2007. Nutrient sharing between symbionts. Plant Physiol. 144: 604–614.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Whitehead, L.F., Tyerman, S.D., Salom, C.L., & Day, D.A. 1995. Transport of fixed nitrogen across symbiotic membranes of legume nodules. Symbiosis 19: 141–154.

    Google Scholar 

  • Wilson, D. 1993. Fungal endophytes: out of sight but should not be out of mind. Oikos 68: 279–384.

    Google Scholar 

  • Wright, D.P., Scholes, J.D., & Read, D.J. 1998a. Effects of VA mycorrhizal colonization on photosynthesis and biomass production of Trifolium repens L. Plant Cell Environ. 21: 209–216.

    Google Scholar 

  • Wright, D.P., Read, D.J., & Scholes, J.D. 1998b. Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L. Plant Cell Environ. 21: 881–891.

    Google Scholar 

  • Wright, D.P., Scholes, J.D., Read, D.J., Rolfe, S.A. 2005. European and African maize cultivars differ in their physiological and molecular responses to mycorrhizal infection. New Phytol. 167: 881–896.

    CAS  PubMed  Google Scholar 

  • Yao, Q., Li, X., Feng, G., & Christie, P. 2001. Mobilization of sparingly soluble inorganic phosphates by the external mycelium of an arbuscular mycorrhizal fungus. Plant Soil 230: 279–285.

    CAS  Google Scholar 

  • Yoneyama, T., Muraoka, T., Kim, T.H., Decanay, E.V., & Nakanishi, Y. 1997. The natural 15N abundance of sugarcane and neigbouring plants in Brazil, the Philippines and Miyako (Japan). Plant Soil 189: 239–244.

    CAS  Google Scholar 

  • Yoneyama, K., Yoneyama, K., Takeuchi, Y., & Sekimoto, H. 2007a. Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta 225: 1031–1038.

    CAS  Google Scholar 

  • Yoneyama, K., Sekimoto, H., Takeuchi ,Y., & Yoneyama, K. 2007b. Regulation of strigolactone exudation by plant nutrients. Abstract 19th Annual Meeting International Plant Growth Substances Association, Puerto Rico, Mexico.

    Google Scholar 

  • Zabinskey, C.A., Quinn, L., & Callaway, R.M. 2002. Phosphorus uptake, not carbon transfer, explains arbuscular mycorrhizal enhancement of Centaurea maculosa in the presence of native grassland species. Funct. Ecol. 16: 758–765.

    Google Scholar 

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Lambers, H., Chapin, F.S., Pons, T.L. (2008). Symbiotic Associations. In: Plant Physiological Ecology. Springer, New York, NY. https://doi.org/10.1007/978-0-387-78341-3_12

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