Mycorrhiza pp 113-132 | Cite as

Mycorrhiza Helper Bacteria

Mycorrhizal symbiosis should not be considered merely as a bipartite plant-fungus interaction, but should instead incorporate the associated organisms. These mycorrhiza-associated organisms are known to influence each other mutually, the outcome of which is described as the “mycorrhizosphere” (Foster and Marks 1966; Meyer and Linderman 1986; Frey-Klett and Garbaye 2005). The mycorrhizosphere comprises mycorrhizas, extramatrical mycelium and the associated microorganisms. In the same way the rhizospheres exert a pressure on microbial populations (Barea et al. 2005), the mycorrhizal roots and hyphae of mycorrhizal fungi (MF) shape the bacterial species composition due to root and hyphal exudation and turnover (Bowen 1993; Morgan et al. 2005). This “mycorrhizosphere effect” may lead to improved plant nutrition, growth and disease resistance (Linderman 1988; Frey-Klett et al. 2005). Determining the functional significance of the mycorrhizosphere organisms for plant productivity presents a major challenge for the future (Artursson et al. 2006).

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abdel-Fattah GM, Mohamedin AH (2000) Interactions between a vesicular-arbuscular mycorrhizal fungus (Glomus intraradices) and Streptomyces coelicolor and their effects on sorghum plants grown in soil amended with chitin of brawn scales. Biol Fertil Soils 32:401-409Google Scholar
  2. Ali NA, Jackson RM (1989) Stimulation of germination of spores of some ectomycorrhizal fungi by other micro-organisms. Mycol Res 93:182-186Google Scholar
  3. Ames BN (1989) Mycorrhiza development in onion in response to chitin-decomposing actino- mycetes. New Phytol 112:423-427Google Scholar
  4. Artursson V, Finlay RD, Jansson JK (2005) Combined bromodeoxyuridine immunocapture and terminal-restriction fragment length polymorphism analysis highlights differences in the active soil bacterial metagenome due to Glomus mosseae inoculation or plant species. Environ Microbiol 7:1952-1966PubMedGoogle Scholar
  5. Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8: 1-10PubMedGoogle Scholar
  6. Asiegbu F, Daniel G, Johansson M (1993) Studies on the infection of Norway spruce roots by Heterobasidion annosum. Can J Bot 71:1552-1561Google Scholar
  7. Aspray TJ, Frey-Klett P, Jones JE, Whipps JM, Garbaye J, Bending GD (2006a) Mycorrhization helper bacteria: a case of specificity for altering ectomycorrhiza architecture but not ectomycorrhiza formation. Mycorrhiza 10.1007/s00572-006-0068-3 (in press)Google Scholar
  8. Aspray TJ, Eirian Jones E, Whipps JM, Bending GD (2006b) Importance of mycorrhization helper bacteria cell density and metabolite localization for the Pinus sylvestris-Lactarius rufus symbiosis. FEMS Microbiol Ecol 56:25-33PubMedGoogle Scholar
  9. Azcon-Aguilar C, Diaz-Rodriguez RM, Barea JM (1986) Effect of soil microorganisms on spore germination of the vesicular-arbuscular mycorrhizal fungus Glomus mosseae. Trans Br Mycol Soc 86:337-340Google Scholar
  10. Barbieri E, Potenza L, Rossi I, Sisti D, Giomaro G, Rossetti S, Beimfohr C, Stocchi V (2000) Phylogenetic characterization and in situ detection of a Cytophaga-Flexibacter-Bacteroides phylogroup bacterium in Tuber borchii Vittad ectomycorrhizal mycelium. Appl Environ Microbiol 66:5035-5042PubMedGoogle Scholar
  11. Barbieri E, Gioacchini AM, Zambonelli A, Bertini I, Stocchi V (2005) Determination of microbial volatile organic compounds from Staphylococcus pasteuri against Tuber borchii using solid phase microextraction and gas chromatography/ion trap mass spectrometry. Rapid Comm Mass Spectrom 15:3411-3415Google Scholar
  12. Barea JM, Andrade G, Bianciotto V, Dowling D, Lohrke S, Bonfante P, O’Gara F, Azcon-Aguilar C (1998) Impact on arbuscular mycorrhiza formation of pseudomonas strains used as inoculants for biocontrol of soil-borne fungal plant pathogens. Applied Environ Microbiol 64:2304-2307Google Scholar
  13. Barea JM, Pozo MJ, Azcon R, Azcon-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761-1778PubMedGoogle Scholar
  14. Becker DM, Bagley ST, Podila GK (1999) Effects of mycorrhiza-associated streptomycetes on growth of Laccaria bicolor, Cenococcum geophilum, and Armillaria species and on gene expression in Laccaria bicolor. Mycologia 91:33-40Google Scholar
  15. Bedini, S, Bagnoli G, Sbrana C, Leporini C, Tola E, Dunne C, Filippi C, D’Andrea F, O’Gara F, Nuti MP (1999) Pseudomonads isolated from within fruit bodies of Tuber borchii are capable of producing biological control or phytostimulatory compounds in pure culture. Symbiosis 26:223-236Google Scholar
  16. Bending GD, Poole EJ, Whipps JM, Read DJ (2002) Characterisation of bacteria from Pinus sylvestris-Suillus luteus mycorrhizas and their effects on root-fungus interactions and plant growth. FEMS Microbiol Ecol 39:219-227PubMedGoogle Scholar
  17. Bertaux J, Schmid M, Prevost-Boure NC, Churin JL, Hartmann A, Garbaye J, Frey-Klett P (2003) In situ identification of intracellular bacteria related to Paenibacillus spp. in the mycelium of the ectomycorrhizal fungus Laccaria bicolor S238N. Appl Environ Microbiol 69:4243-4248PubMedGoogle Scholar
  18. Bianciotto V, Bonfante P (2002) Arbuscular mycorrhizal fungi: a specialised niche for rhizospheric and endocelluar bacteria. Antonie Van Leeuwenhoek Int J Gen Mol Microbiol 81:365-371Google Scholar
  19. Bianciotto V, Bandi C, Minerdi D, Sironi M, Tichy HV, Bonfante P (1996) An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria. Appl Environ Microbiol 62:3005-3010PubMedGoogle Scholar
  20. Bowen GB (1993) The ecology of ectomycorrhiza formation and functioning. Plant Soil 159:61-67Google Scholar
  21. Bowen GD, Theodorou C (1979) Interactions between bacteria and ectomycorrhizal fungi. Soil Biol Biochem 11:119-126Google Scholar
  22. Brulé C, Frey-Klett P, Pierrat JC, Courrier S, Gérard F, Lemoine MC, Rousselet JL, Sommer J, Garbaye J (2001) Survival in the soil of the ectomycorrhizal fungus Laccaria bicolor and effect of a mycorrhiza helper Pseudomonas fluorescens. Soil Biol Biochem 33: 1683-1694Google Scholar
  23. Budi SW, van Tuinen D, Martinotti MG, Gianinazzi S (1999) Isolation from the Sorghum bicolor mycorrhizosphere of a bacterium compatible with arbuscular mycorrhiza development and antagonistic towards soil-borne fungal pathogens. Appl Environ Microbiol 65:5148-5150PubMedGoogle Scholar
  24. Calvaruso C, Turpault MP, Frey-Klett P (2006) Root-associated bacteria contribute to mineral weathering and to mineral nutrition in trees: a budgeting analysis. Applied and Environmental Microbiology 72:1258-1266PubMedGoogle Scholar
  25. Coleman ST, Fang TK, Rovinsky SA, Turano FJ, Moye-Rowley WS (2001) Expression of a glutamate decarboxylase homologue is required for normal oxidative stress tolerance in Saccharomyces cerevisiae. J Biol Chem 276:244-250PubMedGoogle Scholar
  26. Danell E, Alström S, Ternström A (1993) Pseudomonas fluorescens in association with fruit bodies of the ectomycorrhizal mushroom Cantharellus cibarius. Mycol Res 97:1148-1152Google Scholar
  27. De Oliveira VL, Garbaye J (1989) Les microorganismes auxiliaires de l’etablissement des symbioses ectomycorrhiziennes. Eur J For Pathol 19:54-64Google Scholar
  28. Deveau A, Palin B, Delaruelle C, Peter M. Kohler A, Pierrat JC, Sarniguet A, Garbaye J, Martin F, Frey-Klett P (2007) The mycorrhiza helper Pseudomonas fluorescens BBc6R8 has a specific priming effect on the growth, morphology and gene expression of the ectomycorrhizal fungus Laccaria bicolor S238N. New Phytologist 175:743-755PubMedGoogle Scholar
  29. Dunstan WA, Malajczuk N, Dell B (1998) Effects of bacteria on mycorrhizal development and growth of container grown Eucalyptus diversicolor F. Muell. seedlings. Plant Soil 201:241-249Google Scholar
  30. Duponnois R (2006) Bacteria helping mycorrhiza development. In: Mukerji KG, Manoharachary C, Singh J (eds) Microbial activity in the rhizosphere. Springer, Heildelberg, pp 297-310Google Scholar
  31. Duponnois R, Garbaye J (1990) Some mechanisms involved in growth stimulation of ectomycorrhizal fungi by bacteria. Can J Bot 68:2148-2152Google Scholar
  32. Duponnois R, Garbaye J (1991) Mycorrhization helper bacteria associated with the Douglas fir Laccaria laccata symbiosis: effects in vitro and in glasshouse conditions. Ann Sci For 48:239-251Google Scholar
  33. Duponnois R, Kisa M (2006) The possible role of trehalose in the mycorrhiza helper effect. Can J Bot 84:1005-1008Google Scholar
  34. Duponnois R, Garbaye J, Bouchard D, Churin JL (1993) The fungus-specificity of mycorrhization helper bacteria (MHBs) used as an alternative to soil fumigation for ectomycorrhizal inoculation of bare-root Douglasfir planting stocks with Laccaria laccata. Plant Soil 157:257-262Google Scholar
  35. Duponnois R, Assikbetse K, Ramanankierana H, Kisa M, Thioulouse J, Lepage M (2006) Litter-forager termite mounds enhance the ectomycorrhizal symbiosis between Acacia holo-sericea A. Cunn. Ex G. Don and Scleroderma dictyosporum isolates. FEMS Microbiol Ecol 56:292-303PubMedGoogle Scholar
  36. Fossdal CG, Sharma P, Lönneborg A (2001) Isolation of the first putative peroxidase cDNA from a conifer and the local and systemic accumulation of related proteins upon pathogen infection. Plant Mol Biol 47:423-435PubMedGoogle Scholar
  37. Foster RC, Marks GC (1966) The fine structure of the mycorrhizas of Pinus radiata. Australian J Biol Sci 19:1027-1038Google Scholar
  38. Founoune H, Duponnois R, Ba AM, Sall S, Branget I, Lorquin J, Neyra M, Chotte JL (2002) Mycorrhiza helper bacteria stimulated ectomycorrhizal symbiosis of Acacia holosericea with Pisolithus alba. New Phytol 153:81-89Google Scholar
  39. Frey-Klett P, Garbaye J (2005) Mycorrhiza helper bacteria: a promising model for the genomic analysis of fungal-bacterial interactions. New Phytol 168:4-8PubMedGoogle Scholar
  40. Frey-Klett P, Pierrat JC, Garbaye J (1997) Location and survival of mycorrhiza helper Pseudomonas fluorescens during establishment of ectomycorrhizal symbiosis between Laccaria bicolor and Douglas fir. Appl Environ Microbiol 63:139-144PubMedGoogle Scholar
  41. Frey-Klett P, Churin J-L, Pierrat J-C, Garbaye J (1999) Dose effect in the dual inoculation of an ectomycorrhizal fungus and a mycorrhiza helper bacterium in two forest nurseries. Soil Biol Biochem 31:1555-1562Google Scholar
  42. Frey-Klett P, Chavatte M, Clausse M-L, Courrier S, Le Roux C, Raaijmakers J, Martinotti MG, Pierrat J-C, Garbaye J (2005) Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonads. New Phytol 165:317-328PubMedGoogle Scholar
  43. Frey-Klett P, Garbaye J, Tarkka M (2007) Tansley Review: The mycorrhiza helper bacteria revisited. New Phytologist 176:22-36PubMedGoogle Scholar
  44. Fries N (1987) Ecological and evolutionary aspects of spore germination in the higher basidiomycetes. Trans Br Mycol Soc 88:1-7Google Scholar
  45. Gamalero E, Fracchia L, Cavaletto M, Garbaye J, Frey-Klett P, Varese GC, Martinotti MG (2003) Characterization of functional traits of two fluorescent pseudomonads isolated from basidiomes of ectomycorrhizal fungi. Soil Biol Biochem 35:55-65Google Scholar
  46. Gamalero E, Trotta A, Massa N, Copetta A, Martinotti MG, Berta G (2004) Impact of two fluorescent pseudomonads and an arbuscular mycorrhizal fungus on tomato plant growth, root architecture and P acquisition. Mycorrhiza 14:229-234Google Scholar
  47. Garbaye J (1991) Biological interactions in the mycorhizospere. Experientia 47:370-375Google Scholar
  48. Garbaye J (1994) Mycorrhiza helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197-210Google Scholar
  49. Garbaye J, Bowen GD (1987) Effect of different microflora on the success of ectomycorrhizal inoculation of Pinus radiata. Can J For Res 17:941-943Google Scholar
  50. Garbaye J, Bowen GD (1989) Stimulation of mycorrhizal infection of Pinus radiata by some microorganisms associated with the mantle of ectomycorrhizas. New Phytol 112:383-388Google Scholar
  51. Garbaye J, Churin JL, Robin Duponnois R (1992) Effects of substrate sterilization, fungicide treatment, and mycorrhization helper bacteria on ectomycorrhizal formation of pedunculate oak (Quercus robur) inoculated with Laccaria laccata in two peat bare-root nurseries. Biol Fertil Soils 13:55-57Google Scholar
  52. Garbaye J, Churin JL, Robin Duponnois R (1992) Effects of substrate sterilization, fungicide treatment, and mycorrhization helper bacteria on ectomycorrhizal formation of pedunculate oak (Quercus robur) inoculated with Laccaria laccata in two peat bare-root nurseries. Biol Fertil Soils 13:55-57Google Scholar
  53. Garbaye J, Duponnois R (1992) Specificity and function of mycorrhization helper bacteria (MHB) associated with the Pseudotsuga menziesii-Laccaria laccata symbiosis. Symbiosis 14:335-344Google Scholar
  54. Gazzanelli G, Malatesta M, Pianetti A, Baffone W, Stocchi V, Citterio B (1999) Bacteria associated to fruit bodies of the ectomycorrhizal fungi Tuber borchii Vittad. Symbiosis 26:211-222Google Scholar
  55. Giovannetti M, Azzolini D, Citernesi AS (1999) Anastomosis formation and nuclear and protoplasmic exchange in arbuscular mycorrhizal fungi. Appl Environ Microbiol 65: 5571-5575PubMedGoogle Scholar
  56. Grimaldi B, de Raaf MA, Filetici P, Ottonello S, Ballario P (2005) Agrobacterium-mediated gene transfer and enhanced green fluorescent protein visualization in the mycorrhizal ascomycete Tuber borchii: a first step towards truffle genetics. Curr Genet 48:69-74PubMedGoogle Scholar
  57. Gryndler M, Vosatka M (1996) The response of Glomus fistulosum-maize mycorrhiza to treatments with culture fractions from Pseudomonas putida. Mycorrhiza 6:207-211Google Scholar
  58. Heinonsalo J, Frey-Klett P, Pierrat J-C, Churin J-L, Vairelles D, Garbaye J (2004) Fate, tree growth effect and potential impact on soil microbial communities of mycorrhizal and bacterial inoculation in a forest plantation. Soil Biol Biochem 36:211-216Google Scholar
  59. Helber N, Requena N (2008) Expression of the fluorescence markers DsRed and GFP fused to a nuclear localization signal in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 177:537-548PubMedGoogle Scholar
  60. Hildebrandt U, Janetta K, Bothe H (2002) Towards growth of arbuscular mycorrhizal fungi independent of a plant host. Appl Environ Microbiol 68:1919-1924PubMedGoogle Scholar
  61. Hildebrandt U, Ouziad F, Marner FJ, Bothe H (2006) The bacterium Paenibacillus validus stimulates growth of the arbuscular mycorrhizal fungus Glomus intraradices up to the formation of fertile spores. FEMS Microbiol Lett 254:258-267PubMedGoogle Scholar
  62. Keller S, Schneider K, Sussmuth RD (2006) Structure elucidation of auxofuran, a metabolite involved in stimulating growth of fly agaric, produced by the mycorrhiza helper bacterium Streptomyces AcH 505. J Antibiot (Tokyo) 59:801-803Google Scholar
  63. Krishna KR, Balakrishna AN, Bagyaraj DJ (1982) Interaction between a vesicular arbuscular mycorrhizal fungus and Streptomyces cinnamomeus and their effects on finger millet. New Phytol 93:401-405Google Scholar
  64. Lagrange H, Jay-Allgmand C, Lapeyrie F (2001) Rutin, the phenylglycoside from eucalyptus root exudates, stimulates Pisolithus hyphal growh at picomolar concentrations. New Phytol 149:349-355Google Scholar
  65. Lehr NA, Schrey SD, Bauer R, Hampp R, Tarkka MT (2007) Suppression of plant defense response by a mycorrhiza helper bacterium. New Phytol 174:892-903PubMedGoogle Scholar
  66. Linderman RG (1988) Mycorrhizal interactions with the rhizosphere microflora - the mycorrhizosphere effect. Phytopathology 78:366-371Google Scholar
  67. Maier A (2003) Einfluss bakterieller Stoffwechselprodukte auf Wachstum und Proteom des Ektomykorrhizapilzes Amanita muscaria. PhD thesis, University of Tübingen, Tübingen, GermanyGoogle Scholar
  68. Maier A, Riedlinger J, Fiedler H-P, Hampp R (2004) Actinomycetales bacteria from a spruce stand: characterization and effects on growth of root symbiotic, and plant parasitic soil fungi in dual culture. Mycol Progress 3:129-136Google Scholar
  69. Marschner P, Timonen S (2006) Bacterial community composition and activity in rhizospheres of roots colonised by arbuscular mycorrhizal fungi. In: Mukerji KG, Manoharachary C, Singh J (eds) Microbial activity in the rhizosphere Springer, Heidelberg, pp 139-154Google Scholar
  70. Mayo K, Davis R, Motta J (1986) Stimulation of germination of spores of Glomus versiforme by spore-associated bacteria. Mycologia 78:426-431Google Scholar
  71. Meyer JR, Linderman RG (1986) Response of subterranean clover to dual inoculation with vesicular-arbuscular fungi and a plant growth promoting bacterium. Soil Biol Biochem 18:185-190Google Scholar
  72. Mogge B, Loferer C, Agerer R, Hutzler P, Hartmann A (2000) Bacterial community structure and colonization patterns of Fagus sylvatica L. ectomycorrhizospheres as determined by fluorescence in situ hybridization and confocal laser scanning microscopy. Mycorrhiza 9:271-278Google Scholar
  73. Morgan JAW, Bending GD, White PJ (2005) Biological costs and benefits to plant-microbe interactions in the rhizosphere. J Exp Bot 56:1729-1739PubMedGoogle Scholar
  74. Mosse B (1962) The establishment of vesicular-arbuscular mycorrhiza under aseptic conditions. J Gen Microbiol 27:509-520PubMedGoogle Scholar
  75. Mugnier J, Mosse B (1987) Spore germination and viability of a vesicular-arbuscular mycorrhizal fungus, Glomus mosseae. Trans Br Mycol Soc 88:411-413Google Scholar
  76. Muller T, Benjdia M, Avolio M, Voigt B, Menzel D, Pardo A, Frommer WB, Wipf D (2006) Functional expression of the green fluorescent protein in the ectomycorrhizal model fungus Hebeloma cylindrosporum. Mycorrhiza 16:437-442PubMedGoogle Scholar
  77. Paula MA, Urquiaga S, Siqueira JO, Döbereiner J (1992) Synergistic effects of vesicular-arbuscular mycorrhizal fungi and diazotrophic bacteria on nutrition and growth of sweet potato (Ipomoea batatas). Biol Fertil Soils 14:61-66Google Scholar
  78. Poole EJ, Bending GD, Whipps JM, Read DJ (2001) Bacteria associated with Pinus sylvestris- Lactarius rufus ectomycorrhizas and their effects on mycorrhiza formation in vitro. New Phytol 151:743-751Google Scholar
  79. Rao NSS, Tilak KVBR, Singh CS (1985) Synergistic effect of vesicular-arbuscular mycorrhizae and Azospirillum brasiliense on the growth of barley in pots. Soil Biol Biochem 1:121-129Google Scholar
  80. Reddy MS, Satyanarayana T (2006) Interactions between ectomycorrhizal fungi and rhizospheric microbes In: Mukerji KG, Manoharachary C, Singh J (eds) Microbial activity in the rhizosphere. Springer, Heidelberg, pp 245-264Google 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 136:667-677Google Scholar
  82. Riedlinger J (2006) Die stofflichen Grundlagen der Modulation des Myzelwachstums von symbiotischen und pathogenen Pilzen durch Streptomyzeten. PhD thesis, University of Tübingen, Tübingen, GermanyGoogle Scholar
  83. Riedlinger J, Schrey SD, Tarkka MT, Hampp R, Kapur M, Fiedler HP (2006) Auxofuran, a novel substance stimulating growth of fly agaric, produced by the mycorrhiza helper bacterium Streptomyces AcH 505. Appl Environ Microbiol 72:3550-3557PubMedGoogle Scholar
  84. Rincon A, Ruiz-Diez B, Garcia-Fraile S, Garcia JA, Fernandez-Pascual M, Pueyo JJ, de Felipe MR (2005) Colonisation of Pinus halepensis roots by Pseudomonas fluorescens and interaction with the ectomycorrhizal fungus Suillus granulatus. FEMS Microbiol Ecol 51:303-311PubMedGoogle Scholar
  85. Sarand I, Timonen S, Nurmiaho-Lassila E-L, Koivula T, Haahtela K, Romantschuk M, Sen R (1998) Microbial biofilms and catabolic plasmid harbouring degradative fluorescent pseu-domonads in Scots pine mycorrhizospheres developed on petroleum contaminated soil. FEMS Microbiol Ecol 27:112-115Google Scholar
  86. Schelkle M, Peterson RL (1996) Suppression of common root pathogens by helper bacteria and ectomycorrhizal fungi in vitro. Mycorrhiza 6:481-485Google Scholar
  87. Schrey SD, Schellhammer M, Ecke M, Hampp R, Tarkka MT (2005) Mycorrhiza helper bacterium Streptomyces AcH 505 induces differential gene expression in the ectomycorrhizal fungus Amanita muscaria. New Phytol 168:205-216PubMedGoogle Scholar
  88. Schrey SD, Salo V, Raudaskoski M, Hampp R, Nehls U, Tarkka MT (2007) Interaction with mycorrhiza helper bacterium Streptomyces sp. AcH 505 modifies organisation of actin cytoskeleton in the ectomycorrhizal fungus Amanita muscaria (fly agaric). Curr Genet 52:77-85PubMedGoogle Scholar
  89. Tarkka MT, Schrey S, Nehls U (2006) The alpha-tubulin gene AmTuba1: A marker for rapid mycelial growth in the ectomycorrhizal basidiomycete Amanita muscaria. Curr Genet 49:294-301PubMedGoogle Scholar
  90. Toro M, Azcon R, Barea JM (1997) Improvement of arbuscular mycorrhiza development by inoculation of soil with phosphate-solubilizing rhizobacteria to improve rock phosphate bioavailability (32P) and nutrient cycling. Appl Environ Microbiol 63:4408-4412PubMedGoogle Scholar
  91. Torsvik, V, Salte, K, Sorheim, R, Goksoyr, J (1990) Comparison of phenotypic diversity and DNA heterogeneity in a population of soil bacteria. Appl Environ Microbiol 56:776-781PubMedGoogle Scholar
  92. Vivas A, Azcón R, Biró B, Barea JM, Ruiz-Lozano JM (2003a) Influence of bacterial strains isolated from lead-polluted soil and their interactions with arbuscular mycorrhizae on the growth of Trifolium pratense L. under lead toxicity. Can J Microbiol 49:577-588PubMedGoogle Scholar
  93. Vivas A, Marulanda A, Gomez M, Barea JM, Azcon R (2003b) Physiological characteristics (SDH and ALP activities) of arbuscular mycorrhizal colonization as affected by Bacillus thuringiensis inoculation under two phosphorus levels. Soil Biol Biochem 35:987-996Google Scholar
  94. Vivas A, Marulanda A, Ruiz-Lozano JM, Barea JM, Azcon R (2003c) Influence of a Bacillus sp. on physiological activities of two arbuscular mycorrhizal fungi and on plant responses to PEG-induced drought stress. Mycorrhiza 13:249-256PubMedGoogle Scholar
  95. Vivas A, Voros I, Biro B, Campos E, Barea JM, Azcon R (2003d) Symbiotic efficiency of autochthonous arbuscular mycorrhizal fungus (G. mosseae) and Brevibacillus sp. isolated from cadmium polluted soil under increasing cadmium levels. Environ Pollut 126:179-189PubMedGoogle Scholar
  96. Vivas A, Barea JM, Azcon R (2005) Brevibacillus brevis isolated from cadmium- or zinc-contaminated soils improves in vitro spore germination and growth of Glomus mosseae under high Cd or Zn Concentrations. Microbial Ecol 49:416-424Google Scholar
  97. Vosatka 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 11:245-251Google Scholar
  98. Wilkinson KG, Dixon KW, Sivasithamparam K (1989) Interaction of soil bacteria, mycorrhizal fungi and orchid seed in relation to germination of Australian orchids. New Phytol 112:429-435Google Scholar
  99. Wilkinson KG, Dixon KW, Sivasithamparam K, Ghisalberti EL (1994) Effect of IAA on symbiotic germination of an Australian orchid and its production by orchid-associated bacteria. Plant Soil 159:291-295Google Scholar
  100. Will ME, Sylvia DM (1990) Interaction of rhizosphere bacteria, fertilizer, and vesicular-arbuscular mycorrhizal fungi with sea oats. Appl Environ Microbiol 56:2073-2079PubMedGoogle Scholar
  101. Xavier LJC, Germida JJ (2003) Bacteria associated with Glomus clarum spores influence mycorrhizal activity. Soil Biol Biochem 35:471-478Google Scholar
  102. Xie ZP, Staehelin C, Vierheilig H, Wiemken A, Jabbouri S, Broughton WJ, Vogeli-Lange R, Boller T (1995) Rhizobial nodulation factors stimulate mycorrhizal colonization of nodulating and nonnodulating soybeans. Plant Physiol 108:1519-1525PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  1. 1.Department of Soil EcologyUFZ, Helmholtz-Centre for Environmental ResearchHalleGermany
  2. 2.UMRINRA-UHP 1136 (Interactions Arbres-Microorganismes)Centre INRA de NancyFrance

Personalised recommendations