Antonie van Leeuwenhoek

, Volume 81, Issue 1–4, pp 343–351 | Cite as

Mycorrhizosphere interactions to improve plant fitness and soil quality

  • José-Miguel Barea
  • Rosario Azcón
  • Concepción Azcón-Aguilar


Arbuscular mycorrhizal fungi are key components of soil microbiota and obviously interact with other microorganisms in the rhizosphere, i.e. the zone of influence of plant roots on microbial populations and other soil constituents. Mycorrhiza formation changes several aspects of plant physiology and some nutritional and physical properties of the rhizospheric soil. These effects modify the colonization patterns of the root or mycorrhizas (mycorrhizosphere) by soil microorganisms. The rhizosphere of mycorrhizal plants, in practice a mycorrhizosphere, harbors a great array of microbial activities responsible for several key ecosystem processes. This paper summarizes the main conceptual principles and accepted statements on the microbial interactions between mycorrhizal fungi and other members of rhizosphere microbiota and discusses current developments and future trends concerning the following topics: (i) effect of soil microorganisms on mycorrhiza formation; (ii) mycorrhizosphere establishment; (iii) interactions involved in nutrient cycling and plant growth; (iv) interactions involved in the biological control of plant pathogens; and (v) interactions to improve soil quality. The main conclusion is that microbial interactions in the rhizosphere of mycorrhizal plants improve plant fitness and soil quality, critical issues for a sustainable agricultural development and ecosystem functioning.

arbuscular mycorrhiza biocontrol N-fixing bacteria PGPR phosphate-solubilizing microorganisms soil aggregation 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alabouvette C, Schippers B, Lemanceau P & Bakker PAHM (1997) Biological control of fusarium-wilts: towards development of commercial product. In: Boland GJ & Kuykendall LD (Eds) Plant Microbe Interactions and Biological Control (pp 15–36). Marcel Dekker, Inc., New York.Google Scholar
  2. Amora-Lazcano E, Vázquez MM & Azcón R (1998) Response of nitrogen-transforming microorganisms to arbuscular mycorrhizal fungi. Biol. Fertil. Soil. 27: 65–70.CrossRefGoogle Scholar
  3. Andrade G, Azcón R & Bethlenfalvay GJ (1995) A rhizobacterium modifies plant and soil responses to the mycorrhizal fungus Glomus mosseae. Appl. Soil Ecol. 2: 195–202.CrossRefGoogle Scholar
  4. Andrade G, Linderman RG & Bethlenfalvay GJ (1998a) Bacterial associations with the mycorrhizosphere and hyphosphere of the arbuscular mycorrhizal fungus Glomus mosseae. Plant Soil 202: 79–87.CrossRefGoogle Scholar
  5. Andrade G, Mihara KL, Linderman RG & Bethlenfalvay GJ (1998b) Soil aggregation status and rhizobacteria in the mycorrhizosphere. Plant Soil 202: 89–96.CrossRefGoogle Scholar
  6. Andrade G, Mihara KL, Linderman RG & Bethlenfalvay GJ (1997) Bacteria from rhizosphere and hyphosphere soils of different arbuscular mycorrhizal fungi. Plant Soil 192: 71–79.CrossRefGoogle Scholar
  7. Atkinson S, Berta G & Hooker JE (1994) Impact of mycorrhizal colonisation on root architecture, root longevity and the formation of growth regulators. In: Gianinazzi S & Schüepp H (Eds) Impact of Arbuscular Mycorrhizas on Sustainable Agriculture and Natural Ecosystems (pp 47–60). ALS, Birkhäuser Verlag, Basel, SwitzerlandGoogle Scholar
  8. Azcón R, Vivas A, Ruíz-Lozano JM & Barea JM (2001) Effectiveness of indigenous arbuscular mycorrhizal (AM) fungi and bacterial isolates on plant growth and nutrition in Zn and Cd artificially contaminated soils. Book of abstracts, COST Action 838, Workshop on Managing arbuscular mycorrhizal fungi for improving soil quality and plant health in agriculture. June 7-9. University of Çukurova, Adana, Turkey. pp 50.Google Scholar
  9. Azcón R, Rubio R & Barea JM (1991) Selective interactions between different species of mycorrhizal fungi and Rhizobium meliloti strains, and their effects on growth, N2-fixation (15N) and nutrition of Medicago sativa L. New Phytol. 117: 399–404.CrossRefGoogle Scholar
  10. Azcón-Aguilar C, Azcón R & Barea JM (1979) Endomycorrhizal fungi and Rhizobium as biological fertilizers for Medicago sativa in normal cultivation. Nature 27: 235–237.Google Scholar
  11. Azcón-Aguilar C & Bago B (1994) Physiological characteristics of the host plant promoting an undisturbed functioning of the mycorrhizal symbiosis. In: Gianinazzi S & Schüepp H (Eds) Impact of Arbuscular Mycorrhizas on Sustainable Agriculture and Natural Ecosystems (pp 47–60). ALS, Birkhäuser Verlag, Basel, Switzerland.Google Scholar
  12. Azcón-Aguilar C & Barea JM (1992) Interactions between mycorrhizal fungi and other rhizosphere microorganisms. In: Allen MJ (Ed) Mycorrhizal Functioning. An Integrative Plant-fungal Process (pp 163–198). Routledge, Chapman & Hall Inc., New York.Google Scholar
  13. Azcón-Aguilar C & Barea JM (1995) Saprophytic growth of arbuscular-mycorrhizal fungi. In: Hock B & Varma A (Eds) Mycorrhiza Structure Function, Molecular Biology and Biotechnology (pp 391–407). Springer-Verlag, Heidelberg.Google Scholar
  14. Azcón-Aguilar C & Barea JM (1996) Arbuscular mycorrhizas and biological control of soil-borne plant pathogens. An overview of the mechanisms involved. Mycorrhiza 6: 457–464.CrossRefGoogle Scholar
  15. Barea JM (1997) Mycorrhiza/bacteria interactions on plant growth promotion. In: Ogoshi A, Kobayashi L, Homma Y, Kodama F, Kondon N & Akino S (Eds) Plant Growth-promoting Rhizobacteria, Present Status and Future Prospects (pp 150–158). OECD, Paris.Google Scholar
  16. Barea JM (2000) Rhizosphere and mycorrhiza of field crops. In: Toutant JP, Balazs E, Galante E, Lynch JM, Schepers JS, Werner D & Werry PA (Eds) Biological Resource Management: Connecting Science and Policy (OECD) (pp 110-125) INRA, Editions and Springer.Google Scholar
  17. Barea JM, Andrade G, Bianciotto V, Dowling D, Lohrke S, Bonfante P, O'Gara F & Azcón-Aguilar C (1998) Impact on arbuscular mycorrhiza formation of Pseudomonas strains used as inoculants for the biocontrol of soil-borne plant fungal pathogens. Appl. Environ. Microbiol. 64: 2304–2307.PubMedGoogle Scholar
  18. Barea JM, Azcón R & Azcón-Aguilar C (1992) Vesicular-arbuscular mycorrhizal fungi in nitrogen-fixing systems. In: Norris JR, Read DJ & Varma AK (Eds) Methods in Microbiology (pp 391–416). Academic Press, London.Google Scholar
  19. Barea JM, Azcón-Aguilar C & Azcón R (1997) Interactions between mycorrhizal fungi and rhizosphere microorganisms within the context of sustainable soil-plant systems. In: Gange AC & Brown VK (Eds) Multitrophic Interactions in Terrestrial Systems (pp 65–77). Blackwell Science, Oxford.Google Scholar
  20. Barea JM & Jeffries P (1995) Arbuscular mycorrhizas in sustainable soil plant systems. In: Hock B & Varma A (Eds) Mycorrhiza Structure Function, Molecular Biology and Biotechnology (pp 521–559). Springer-Verlag, Heidelberg.Google Scholar
  21. Barea JM, Tobar RM & Azcón-Aguilar C (1996) Effect of a genetically-modified Rhizobium meliloti inoculant on the development of arbuscular mycorrhizas, root morphology, nutrient uptake and biomass accumulation in Medicago sativa L. New Phytol 134: 361–369.CrossRefGoogle Scholar
  22. Barea JM, Toro M, Orozco MO, Campos E & Azcón R (2002) 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 (in press).Google Scholar
  23. Bashan Y (1999) Interactions of Azospirillum spp. in soils: a review. Biol. Fertil. Soils 29: 246–256.CrossRefGoogle Scholar
  24. Bashan Y & Holguin G (1998) Proposal for the division of plant growth-promoting rhizobacteria into two classifications: biocontrol-PGPB (plant growth-promoting bacteria) and PGPB. Soil Biol. Biochem. 30: 1225–1228.CrossRefGoogle Scholar
  25. Berta G, Trotta A, Fusconi A, Hooker JE, Munro M, Atkinson D, Giovannetti M, Morini S, Fortuna P, Tisserant B, Gianinazzi-Pearson V & Gianinazzi S (1995) Arbuscular mycorrhizal induced changes to plant growth and root system morphology in Prunus cerasifera. Tree Physiol. 15: 281–293.PubMedGoogle Scholar
  26. Bethlenfalvay GJ, Cantrell IC, Mihara KL & Schreiner RP (1999) Relationships between soil aggregation and mycorrhizae as influenced by soil biota and nitrogen nutrition. Biol. Fertil. Soils 28: 356–363.CrossRefGoogle Scholar
  27. Bethlenfalvay GJ & Linderman RG (1992) Mycorrhizae in Sustainable Agriculture. ASA Special publication No. 54, Madison, Wisconsin.Google Scholar
  28. Bethlenfalvay GJ & Schüepp H (1994) Arbuscular mycorrhizas and agrosystem stability. In: Gianinazzi S & Schüepp H (Eds) Impact of Arbuscular Mycorrhizas on Sustainable Agriculture and Natural Ecosystems. (pp 117–131). Birkhäuser, Basel.Google Scholar
  29. Bianciotto V, Andreotti S, Balestrini R, Bonfante P & Perotto S (2001) Mucoid mutants of the biocontrol strain Pseudomonas fluorescens CHA0 show increased ability in biofilm formation on mycorrhizal and nonmycorrhizal carrot roots. Mol. Plant. Microbe Interac. 14: 255–260.Google Scholar
  30. Bianciotto V, Lumini E, Lanfranco L, Minerdi D, Bonfante P & Perotto S (2000) Detection and identification of bacterial endosymbionts in arbuscular mycorrhizal fungi belonging to the family Gigasporaceae. Appl. Environ. Microbiol. 66: 4503–4509.PubMedCrossRefGoogle Scholar
  31. Bonfante P & Perotto S (2000) Outside and inside the roots: Cell-to-cell interactions among arbuscular mycorrhizal fungi, bacteria and host plants. Curr. Adv. Mycorrhizae Res. 141-155.Google Scholar
  32. Bowen GD & Rovira AD (1999) The rhizosphere and its management to improve plant growth. Adv. Agron. 66: 1–102.Google Scholar
  33. Broek AV & Vanderleyden J (1995) Genetics of the Azospirillum plant root association. Crit. Rev. Plant Sci. 14: 445–466.Google Scholar
  34. Budi SW, Van Tuinen D, Martinotti G & Gianinazzi S (1999) Isolation from Sorghum bicolor mycorrhizosphere of a bacterium compatible with arbuscular mycorriza development and antagonistic towards soilborne fungal pathogens. Appl. Environ. Microbiol. 65: 5148–5150.PubMedGoogle Scholar
  35. Calvet C, Pera J & Barea JM (1993) Growth response of marigold (Tagetes erecta L.) to inoculation with Glomus mosseae, Trichoderma aureoviride and Phythium ultimum in a peat-perlite mixture. Plant Soil 148: 1–6.CrossRefGoogle Scholar
  36. Christensen H & Jakobsen I (1993) Reduction of bacterial growth by a vesicular-arbuscular mycorrhizal fungus in the rhizosphere of cucumber (Cucunis sativus L). Biol. Fertil. Soils 15: 253–258.CrossRefGoogle Scholar
  37. Cordier C, Lemoine MC, Lemanceau P, Gianinazzi-Pearson V & Gianinazzi S (1999) The beneficial rhizosphere: a necessary strategy for microplant production. Acta Horticulturae 530: 259–265.Google Scholar
  38. Duijff BJ, Gianinazzi-Pearson V & Lemanceau P (1997) Involvement of the outermembrane lipopolysaccharides in the endophytic root colonization of tomato roots by biocontrol Pseudomonas fluorescens strain WCS417r. New Phytol. 135: 325–334.CrossRefGoogle Scholar
  39. Edwards SG, Young JPW & Fitter AH (1998) Interactions between Pseudomonas fluorescens biocontrol agents and Glomus mosseae, an arbuscular mycorrhizal fungus, within the rhizosphere. FEMS Microbiol. Lett. 116: 297–303.CrossRefGoogle Scholar
  40. Filippi C, Bagnoli G, Citernesi AS & Giovannetti M (1998) Ultrastructural spatial distribution of bacteria associated with sporocarps of Glomus mosseae. Symbiosis 24: 1–12.Google Scholar
  41. Franken P & Requena, N (2001) Analysis of gene expression in arbuscular mycorrhizas: new approaches and challenges. New Phytol. 150: 517–523.CrossRefGoogle Scholar
  42. Frey-Klett P, Garbaye J, Berge O & Heulin T (1997) Metabolic and genotypic fingerprinting of fluorescent Pseudomonads associated with the Douglas Fir-Laccaria bicolor mycorrhizosphere. Appl. Environ. Microbiol. 63: 1852–1860.PubMedGoogle Scholar
  43. Galleguillos C, Aguirre C, Barea JM & Azcón R (2000) Growth promoting effect of two Sinorhizobium meliloti strains (a wild type and its genetically modified derivative) on a non-legume plant species in specific interaction with two arbuscular mycorrhizal fungi. Plant Sci. 159: 57–63.PubMedCrossRefGoogle Scholar
  44. Garbaye J (1994) Helper bacteria: A new dimension to the mycorrhizal symbiosis. New Phytol. 128: 197–210.CrossRefGoogle Scholar
  45. Germida JJ & Walley FL (1996) Plant growth-promoting rhizobacteria alter rooting patterns and arbuscular mycorrhizal fungi colonization of field-grown spring wheat. Biol. Fertil. Soils 23: 113–120.Google Scholar
  46. Gianinazzi S & Schüepp H (1994) Impact of Arbuscular Mycorrhizas on Sustainable Agriculture and Natural Ecosystems. ALS, Birkhäuser Verlag, Basel.Google Scholar
  47. Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can. J. Microbiol. 41: 109–117.CrossRefGoogle Scholar
  48. Giovannetti M (2000) Spore germination and pre-symbiotic mycelial growth. In: Kapulnik Y & Douds DD Jr (Ed) Arbuscular Mycorrhizas: Physiology and Function (pp 3–18). Kluwer Academic Publishers, Dordrecht, The Netherlands.Google Scholar
  49. Goicoechea N, Antolín MC & Sánchez-Díaz M (1997) Influence of arbuscular mycorrhizae and Rhizobium on nutrient content and water relations in drought stressed alfalfa. Plant Soil 192: 261–268.CrossRefGoogle Scholar
  50. Goicoechea N, Szalai G, Antolín MC, Sánchez-Díaz M & Paldi E (1998) Influence of arbuscular mycorrhizae and Rhizobium on free polyamines and proline levels in water-stressed alfalfa. J. Plant Physiol. 153: 706–711.Google Scholar
  51. Gryndler M (2000) Interactions of arbuscular mycorrhizal fungi with other soil organisms. In: Kapulnik Y & Douds DD Jr (Ed) Arbuscular Mycorrhizas: Physiology and Function (pp 239–262). Kluwer Academic Publishers, Dordrecht, The Netherlands.Google Scholar
  52. Gryndler M & Hrselova H (1998) Effect of diazotrophic bacteria isolated from a mycelium of arbuscular mycorrhizal fungi on colonization of maize roots by Glomus fistulosum. Biol. Plant 41: 617–621.CrossRefGoogle Scholar
  53. Gryndler M, Hrselová H & Stríteská D (2000) Effect of soil bacteria on growth of hyphae of the arbuscular mycorrhizal (AM) fungus Glomus claroideum. Folia Microbiol. 45: 545–551.Google Scholar
  54. Haas D, Keel C, Laville J, Maurhofer M, Oberliansli T, Schnider U, Voisard C, Wüthrich B & Defago G (1991) Secondary metabolites of Pseudomonas fluorescens strain CHA0 involved in the suppression of root diseases. In: Hennecke H & Verma DPS (Eds) Advances in Molecular Genetics of Plant-microbe Interactions (pp 450–456). Kluwer Academic Publisher, Dordrecht.Google Scholar
  55. Harley JL & Smith SE (1983) Mycorrhizal Symbiosis. Academic Press, New York.Google Scholar
  56. Herrera MA, Salamanca CP & Barea JM (1993) Inoculation of woody legumes with selected arbuscular mycorrhizal fungi and rhizobia to recover desertified mediterranean ecosystems. Appl. Environ. Microbiol. 59: 129–133.PubMedGoogle Scholar
  57. Jeffries P (1997) Mycoparasitism. In: Wicklow Södertröm (Eds) The Mycota IV Environmental and Microbial Relationships (pp. 149–164). Springer-Verlag, Berlin, Heidelberg.Google Scholar
  58. 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 (pp 95–113). Springer-Verlag, Berlin, Heidelberg.Google Scholar
  59. Kennedy AC (1998) The rhizosphere and spermosphere In: Sylvia DM, Fuhrmann JJ, Hartel PG & Zuberer DA (Eds) Principles and Applications of Soil Microbiology (pp 389–407). Prentice Hall, Upper Saddle River, New Jersey.Google Scholar
  60. Kennedy AC & Smith KL (1995) Soil microbial diversity and the sustainability of agricultural soils. Plant Soil 170: 75–86.CrossRefGoogle Scholar
  61. Kim KY, Jordan D & McDonald GA (1998) Effect of phosphate-solubilizing bacteria and vesicular-arbuscular mycorrhizae on tomato growth and soil microbial activity. Biol. Fertil. Soils 26: 79–87.CrossRefGoogle Scholar
  62. Kloepper JW (1994) Plant growth-promoting rhizobacteria (other systems) In: Okon Y (Ed) Azospirillum/plant associations (pp 111–118). CRC Press, Boca Raton.Google Scholar
  63. Kloepper JW (1996) Host specificity in microbe-microbe interactions. BioScience 46: 406–409.CrossRefGoogle Scholar
  64. Kloepper JW, Zablotowick RM, Tipping EM & Lifshitz R (1991) Plant growth promotion mediated by bacterial rhizosphere colonizers. In: Keister DL & Cregan PB (Eds) The Rhizosphere and Plant Growth (pp 315–326). Kluwer Academic Publishers, Dordrecht.Google Scholar
  65. Lemanceau P & Alabouvette C (1993) Suppression of Fusarium-wilts by fluorescent pseudomonads: mechanisms and applications. Biocontrol Sci. Technol. 3: 219–234.Google Scholar
  66. Linderman RG (1992) Vesicular-arbuscular mycorrhizae and soil microbial interactions. In: Bethlenfalvay GJ & Linderman RG (Eds) Mycorrhizae in Sustainable Agriculture (pp 45–70). ASA Spec. Publ., Madison, Wisconsin.Google Scholar
  67. Linderman RG (1994) Role of VAM fungi in biocontrol. In: Pfleger FL & Linderman RG (Eds) Mycorrhizae and Plant Health (pp 1–26). APS Press, St Paul.Google Scholar
  68. Linderman RG (2000) Effects of mycorrhizas on plant tolerance to diseases. In: Kapulnik Y & Douds DD Jr (Ed) Arbuscular Mycorrhizas: Physiology and Function (pp 345–365). Kluwer Academic Publishers, Dordrecht, The Netherlands.Google Scholar
  69. Lugtenberg BJJ, Weger de LA & Bennett JW (1991) Microbial stimulation of plant growth and protection from disease. Curr. Opin. Microbiol. 2: 457–464.Google Scholar
  70. Lynch JM (1990) The Rhizosphere. John Wiley, New York.Google Scholar
  71. Meyer JR & Linderman RG (1986) Response of subterranean clover to dual inoculation with vesicular arbuscular mycorrhizal fungi and a plant growth promoting bacterium, Pseudomonas putida. Soil Biol. B 18: 185–190.CrossRefGoogle Scholar
  72. Miller RM & Jastrow JD (1994) Vesicular-arbuscular mycorrhizae and biogeochemical cycling. In: Pfleger FL & Linderman RG (Eds) Mycorrhizae and Plant Health (pp 189–212). APS Press, St. Paul, MN.Google Scholar
  73. Miller RM & Jastrow JD (2000) Mycorrhizal fungi influence soil structure. In: Kapulnik Y & Douds DD Jr (Eds) Arbuscular Mycorrhizas: Physiology and Function (pp 3–18). Kluwer Academic Publishers, Dordrecht, The Netherlands.Google Scholar
  74. Monzón A & Azcón R (1996) Relevance of mycorrhizal fungal origin and host plant genotype to inducing growth and nutrient uptake in Medicago species. Agric. Ecosyst. Environ. 60: 9–15.CrossRefGoogle Scholar
  75. Nehl DB, Allen SJ & Brown JF (1996) Deleterious rhizosphere bacteria: An integrating perspective. Appl. Soil Ecol. 5: 1–20.CrossRefGoogle Scholar
  76. Nemec S (1997) Longevity of microbial biocontrol agents in a planting mix amended with Glomus intraradices. Biocontrol Sci. Technol. 7: 183–192.CrossRefGoogle Scholar
  77. O'Gara F, Dowling DN & Boesten B (1994) Molecular Ecology of Rhizosphere Microorganisms. VCH, Weinheim, Germany.Google Scholar
  78. Okon Y (1994) Azospirillum/plant Associations. CRC Press, Boca Raton.Google Scholar
  79. Puppi G, Azcón R & Höflich G (1994) Management of positive interactions of arbuscular mycorrhizal fungi with essential groups of soil microorganisms. In: Gianinazzi S & Schüepp H (Eds) Impact of Arbuscular Mycorrhizas on Sustainable Agriculture and Natural Ecosystems (pp 201–215). ALS, Birkhäuser Verlag, Basel Switzerland.Google Scholar
  80. Ravnskov S, Nybroe O & Jakobsen I (1999) Influence of an arbuscular mycorrhizal fungus on Pseudomonas fluorescens DF57 in rhizosphere and hyphosphere soil. New Phytol. 142: 113–122.CrossRefGoogle Scholar
  81. Requena N, Jimenez I, Toro M & Barea JM (1997) Interactions between plant-growth-promoting rhizobacteria (PGPR), arbuscular mycorrhizal fungi and Rhizobium spp. in the rhizosphere of Anthyllis cytisoides, a model legume for revegetation in mediterranean semi-arid ecosystems. New Phytol. 136: 667–677.CrossRefGoogle Scholar
  82. Requena N, Perez-Solis E, Azcón-Aguilar C, Jeffries P & Barea JM (2001) Management of indigenous plant-microbe symbioses aids restoration of desertified ecosystems. Appl. Environ. Microbiol. 67: 495–498.PubMedCrossRefGoogle Scholar
  83. Ruiz-Lozano JM & Bonfante P (2000) A Burkholderia strain living inside the arbuscular mycorrhizal fungus Gigaspora margarita possesses the vacB gene, which is involved in host cell colonization by bacteria. Microbial Ecol. 39: 137–144.CrossRefGoogle Scholar
  84. Ruiz-Lozano JM & Azcón R (1993) Specificity and functional compatibility of VA mycorrhizal endophytes in association with Bradyrhizobium strains in Cicer arietinum. Symbiosis 15: 217–226.Google Scholar
  85. Ruiz-Lozano JM, Collados C, Barea JM & Azcón R (2001) Arbuscular mycorrhizal symbiosis can alleviate drought-induced nodule senescence in soybean plants. New Phytol. 151: 493–502.CrossRefGoogle Scholar
  86. Sanjuan J & Olivares J (1991) Multicopy plasmids carrying the Klebsiella pneumoniae nifA gene enhance Rhizobium meliloti nodulation competitiveness on alfalfa. Mol. Plant Micr. Interact. 4: 365–369.Google Scholar
  87. Schreiner RP, Mihara KL, McDaniel H & Bethlenfalvay GJ (1997) Mycorrhizal fungi influence plant and soil functions and interactions. Plant Soil 188: 199–209.CrossRefGoogle Scholar
  88. Secilia J & Bagyaraj DJ (1987) Bacteria and actinomycetes associated with pot cultures of vesicular arbuscular mycorrhizas. Can. J. Micro. 33: 1069–1073.CrossRefGoogle Scholar
  89. Smith SE, Gianinazzi-Pearson V, Koide R & Cairney JWG (1994) Nutrient transport in mycorrhizas: structure, physiology and consequences for efficiency of the symbiosis. In: Robson AD, Abbott LK & Malajczuk N (Eds) Management of Mycorrhizas in Agriculture, Horticulture and Forestry (pp 103–113). Kluwer Academic Publishers, Dordrecht.Google Scholar
  90. Smith DE & Read DJ (1997) Mycorrhizal Symbiosis. Academic Press, London.Google Scholar
  91. Sturz AV & Nowak J (2000) Endophytic communities of rhizobacteria and the strategies required to create yield enhancing associations with crops. Appl. Soil Ecol. 15: 183–190.CrossRefGoogle Scholar
  92. Toal ME, Yeomans C, Killham K & Meharg AA (2000) A review of rhizosphere carbon flow modelling. Plant Soil 222: 263–281.CrossRefGoogle Scholar
  93. Tobar RM, Azcón-Aguilar C, Sanjuán J & Barea JM (1996) Impact of a genetically modified Rhizobium strain with improved nodulation competitiveness on the early stages of arbuscular mycorrhiza formation. Appl. Soil Ecol. 4: 15–21.CrossRefGoogle Scholar
  94. Toro M, Azcón R & Barea JM (1997) Improvement of arbuscular mycorrhizal development by inoculation with phosphatesolubilizing rhizobacteria to improve rock phosphate bioavailability (32P) and nutrient cycling. Appl. Environ. Microbiol. 63: 4408–4412.PubMedGoogle Scholar
  95. Toro M, Azcón R & Barea JM (1998) The use of isotopic dilution techniques to evaluate the interactive effects of Rhizobium genotype, mycorrhizal fungi, phosphate-solubizing rhizobacteria and rock phosphate on nitrogen and phosphorus acquisition by Medicago sativa. New Phytol. 138: 265–273.CrossRefGoogle Scholar
  96. Valdenegro M, Barea JM & Azcón R (2001) Influence of arbuscularmycorrhizal fungi, Rhizobium meliloti strains and PGPR inoculation on the growth of Medicago arborea used as model legume for re-vegetation and biological reactivation in a semi-arid mediterranean area. Plant Growth Regulation 34: 233–240.CrossRefGoogle Scholar
  97. Van Loon LC, Bakker PAHM & Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36: 453–483.PubMedCrossRefGoogle Scholar
  98. Vázquez MM, Cesar S, Azcón R & Barea JM (2000) Interactions between arbuscular mycorrhizal fungi and other microbial inoculants (Azospirillum, Pseudomonas, Trichoderma) and their effects on microbial population and enzyme activities in the rhizosphere of maize plants. Appl. Soil Ecol. 15: 261–272.CrossRefGoogle Scholar
  99. Volpin H & Kapulnik Y (1994) Interaction of Azospirillum with beneficial soil microorganisms. In: Okon Y (Ed) Azospirillum/Plant Associations (pp 111–118). CRC Press, Boca RatonGoogle Scholar
  100. Vosátka M (1996) Soil bacteria - a component of plant, soil and arbuscular mycorrhizal fungal interactions. In: Azcon-Aguilar C & Barea JM (Eds) Mycorrhizas in Integrated Systems - From Genes to Plant Development (pp 613-618). European Commission Report EUR 16728, Brussels, Luxembourg.Google Scholar
  101. Vosátka M & Gryndler M (1999) Treatment with culture fractions from Pseudomonas putida modifies the development of Glomus fistulosum mycorrhiza and the response of potato and maize plants to inoculation. Appl. Soil Ecol. 11: 245–251.CrossRefGoogle Scholar
  102. Weller DM & Thomashow LS (1994) Current challanges in introducing beneficial microorganisms into the rhizosphere. In: O'Gara F, Dowling DN, Boesten B & Weinheim VCH (Eds) Molecular Ecology of Rhizosphere Microorganisms Biotechnology and the Release of GMOs (pp 1-18). Germany.Google Scholar
  103. Werner D (1998) Organic signals between plants and microorganisms. In: Pinton R, Varanini Z & Nannipieri P (Eds) The Rhizosphere: Biochemistry and Organic Substances at the Soil-Plant Interfaces. Marcel Dekker Inc., New York.Google Scholar
  104. Whitelaw MA (2000) Growth promotion of plants inoculated with phosphate-solubilizing fungi. Adv. Agron. 69: 99–151.CrossRefGoogle Scholar
  105. 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.CrossRefGoogle Scholar
  106. Wise DL, Trantolo DJ, Cichon EJ, Inyang HI & Stottmeister U (2000) Bioremediation of Contaminated Soils. Marcel Dekker, New York.Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • José-Miguel Barea
    • 1
  • Rosario Azcón
    • 1
  • Concepción Azcón-Aguilar
    • 1
  1. 1.Departamento de Microbilogía del Suelo y Sistemas Simbióticos, Estación Experimental del ZaidínCSICGranadaSpain

Personalised recommendations