Plant and Soil

, Volume 321, Issue 1–2, pp 235–257

Plant-driven selection of microbes

  • Anton Hartmann
  • Michael Schmid
  • Diederik van Tuinen
  • Gabriele Berg
Review Article


The rhizodeposition of plants dramatically influence the surrounding soil and its microflora. Root exudates have pronounced selective and promoting effects on specific microbial populations which are able to respond with chemotaxis and fast growth responses, such that only a rather small subset of the whole soil microbial diversity is finally colonizing roots successfully. The exudates carbon compounds provide readily available nutrient and energy sources for heterotrophic organisms but also contribute e.g. complexing agents, such as carboxylates, phenols or siderophores for the mobilization and acquisition of rather insoluble minerals. Root exudation can also quite dramatically alter the pH- and redox-milieu in the rhizosphere. In addition, not only specific stimulatory compounds, but also antimicrobials have considerable discriminatory effect on the rhizosphere microflora. In the “biased rhizosphere” concept, specific root associated microbial populations are favored based on modification of the root exudation profile. Rhizosphere microbes may exert specific plant growth promoting or biocontrol effects, which could be of great advantage for the plant host. Since most of the plant roots have symbiotic fungi, either arbuscular or ectomycorrhizal fungi, the impact of plants towards the rhizosphere extends also to the mycorrhizosphere. The selective effect of the roots towards the selection of microbes also extends towards the root associated and symbiotic fungi. While microbes are known to colonize plant roots endophytically, also mycorrhiza are now known to harbor closely associated bacterial populations even within their hyphae.

The general part of the manuscript is followed by the more detailed presentation of specific examples for the selection and interaction of roots and microbes, such as in the rhizosphere of strawberry, potato and oilseed rape, where the soil-borne plant pathogen Verticillium dahliae can cause high yield losses; the potential of biocontrol by specific constituents of the rhizosphere microbial community is demonstrated. Furthermore, plant cultivar specificity of microbial communities is described in different potato lines including the case of transgenic lines. Finally, also the specific selective effect of different Medicago species on the selection of several arbuscular mycorrhizal taxa is presented.


Root exudation Rhizodeposition Microbial diversity Rhizosphere bacteria Mycorrhizal fungi Arbuscular mycorrhiza Ectomycorrhiza Antimicrobials Signalling compounds Plant growth promotion Biological control “Biased rhizosphere concept” 


  1. Agerer R (2001) Exploration types of ectomycorrhizal mycelial systems: A proposal to classify mycorrhizal mycelial systems with respect to their ecologically important contact area with the substrate. Mycorrhiza 11:107–114. doi:10.1007/s005720100108 CrossRefGoogle Scholar
  2. Ahrenholtz I, Harms K, de Vries J, Wackernagel W (2000) Increased killing of Bacillus subtilis on the hair roots of transgenic T4 lysozyme-producing potatoes. Appl Environ Microbiol 66:1862–1865. doi:10.1128/AEM.66.5.1862-1865.2000 PubMedCrossRefGoogle Scholar
  3. Akiyama K, Matsuzaki K-i, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827. doi:10.1038/nature03608 PubMedCrossRefGoogle Scholar
  4. Alkan N, Gadkar V, Coburn J, Yarden O, Kapulnik Y (2004) Quantification of the arbuscular mycorrhizal fungus Glomus intraradices in host tissue using real-time polymerase chain reaction. New Phytol 161:877–885. doi:10.1046/j.1469-8137.2004.00975.x CrossRefGoogle Scholar
  5. Alkan N, Gadkar V, Yarden O, Kapulnik Y (2006) Analysis of quantitative interactions between two species of arbuscular mycorrhizal fungi, Glomus mosseae and G. intraradices, by Real-Time PCR. Appl Environ Microbiol 72:4192–4199. doi:10.1128/AEM.02889-05 PubMedCrossRefGoogle Scholar
  6. Andrade G, Mihara KL, Linderman RG, Bethlenfalvay GJ (1997) Bacteria from the rhizosphere and hyphoshere soils of different arbuscular-mycorrhizal fungi. Plant Soil 192:71–79. doi:10.1023/A:1004249629643 CrossRefGoogle Scholar
  7. Apel K, Hirt H (2004) Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. doi:10.1146/annurev.arplant.55.031903.141701 PubMedCrossRefGoogle Scholar
  8. 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 Microbio l7:1952–1966. doi:10.1111/j.1462-2920.2005.00868.x PubMedCrossRefGoogle Scholar
  9. Bais HP, Prithiviraj B, Jha AK, Ausubel FM, Vivanco JM (2005) Mediation of pathogen resistance by exudation of antimicrobials from roots. Nature 434:217–221. doi:10.1038/nature03356 PubMedCrossRefGoogle Scholar
  10. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266. doi:10.1146/annurev.arplant.57.032905.105159 PubMedCrossRefGoogle Scholar
  11. 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. Appl Environ Microbiol 64:2304–2307PubMedGoogle Scholar
  12. Bauer WD, Mathesius U (2004) Plant responses to bacterial quorum sensing signals. Curr Opin Plant Biol 7:429–433. doi:10.1016/j.pbi.2004.05.008 PubMedCrossRefGoogle Scholar
  13. Bérczi A, Møller IM (2000) Redox enzymes in the plant plasma membrane and their possible roles. Plant Cell Environ 23:1287–1302. doi:10.1046/j.1365-3040.2000.00644.x CrossRefGoogle Scholar
  14. Berg G, Smalla K (2008) Plant species versus soil type: which factors influence the structure and function of the microbial communities in the rhizosphere? FEMS Microbiol Ecol (submitted)Google Scholar
  15. Berg G, Roskot N, Steidle A, Eberl L, Zock A, Smalla K (2002) Plant-dependent genotypic and phenotypic diversity of antagonistic rhizobacteria isolated from different Verticillium host plants. Appl Environ Microbiol 68:3328–3338. doi:10.1128/AEM.68.7.3328-3338.2002 PubMedCrossRefGoogle Scholar
  16. Berg G, Zachow C, Lottmann J, Gotz M, Costa R, Smalla K (2005) Impact of plant species and site on rhizosphere-associated fungi antagonistic to Verticillium dahliae Kleb. Appl Environ Microbiol 71:4203–4213. doi:10.1128/AEM.71.8.4203-4213.2005 PubMedCrossRefGoogle Scholar
  17. Berg G, Opelt K, Zachow C, Lottmann J, Gotz M, Costa R, Smalla K (2006) The rhizosphere effect on bacteria antagonistic towards the pathogenic fungus Verticillium differs depending on plant species and site. FEMS Microbiol Ecol 56:250–261. doi:10.1111/j.1574-6941.2005.00025.x PubMedCrossRefGoogle Scholar
  18. 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 69:4243–4248. doi:10.1128/AEM.69.7.4243-4248.2003 PubMedCrossRefGoogle Scholar
  19. Bertaux J, Schmid M, Hutzler P, Hartmann A, Garbaye J, Frey-Klett P (2005) Occurrence and distribution of endobacteria in the plant-associated mycelium of the ectomycorrhizal fungus Laccaria bicolor S238N. Environ Microbio l7:1786–1795. doi:10.1111/j.1462-2920.2005.00867.x PubMedCrossRefGoogle Scholar
  20. Bohm M, Hurek T, Reinhold-Hurek B (2007) Twitching motility is essential for endophytic rice colonization by the N2-fixing endophyte Azoarcus sp. Strain BH72. Mol Plant Microbe Interact 20:526–533. doi:10.1094/MPMI-20-5-0526 PubMedCrossRefGoogle Scholar
  21. Bruinsma M, Kowalchuk GA, van Veen JA (2003) Effects of genetically modified plants on microbial communities and processes in soil. Biol Fertil Soils 37:329–337Google Scholar
  22. Budi SW, van Tuinen D, Martinotti G, Gianinazzi S (1999) Isolation from the Sorghum bicolor mycorrhizosphere of a bacterium compatible with arbuscular mycorrhiza development and antagonistic towards soilborne fungal pathogens. Appl Environ Microbiol 65:5148–5150PubMedGoogle Scholar
  23. Butler JL, Williams MA, Bottomley PJ, Myrold DD (2003) Microbial community dynamics associated with rhizosphere carbon flow. Appl Environ Microbiol 69:6793–6800. doi:10.1128/AEM.69.11.6793-6800.2003 PubMedCrossRefGoogle Scholar
  24. Butler JL, Bottomley PJ, Griffith SM, Myrold DD (2004) Distribution and turnover of recently fixed photosynthate in ryegrass rhizospheres. Soil Biol Biochem 36:371–382. doi:10.1016/j.soilbio.2003.10.011 CrossRefGoogle Scholar
  25. Chishaki N, Horiguchi T (1997) Responses of secondary metabolism in plants to nutrient deficiency. Soil Sci Plant Nutr 43:987–991Google Scholar
  26. Cook RJ, Thomashow LS, Weller DM, Fujimoto D, Mazzola M, Bangera G, Kim D (1995) Molecular mechanisms of defense by rhizobacteria against root disease. Proc Natl Acad Sci U S A 92:4197–4201. doi:10.1073/pnas.92.10.4197 PubMedCrossRefGoogle Scholar
  27. Costa R, Gotz M, Mrotzek N, Lottmann J, Berg G, Smalla K (2006a) Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbiol Ecol 56:236–249. doi:10.1111/j.1574-6941.2005.00026.x PubMedCrossRefGoogle Scholar
  28. Costa R, Salles JF, Berg G, Smalla K (2006b) Cultivation-independent analysis of Pseudomonas species in soil and in the rhizosphere of field-grown Verticillium dahliae host plants. Environ Microbiol 8:2136–2149. doi:10.1111/j.1462-2920.2006.01096.x PubMedCrossRefGoogle Scholar
  29. Costa R, Gomes NCM, Krogerrecklenfort E, Opelt K, Berg G, Smalla K (2007) Pseudomonas community structure and antagonistic potential in the rhizosphere: insights gained by combining phylogenetic and functional gene-based analyses. Environ Microbiol 9:2260–2273. doi:10.1111/j.1462-2920.2007.01340.x PubMedCrossRefGoogle Scholar
  30. Crowley DE, Rengel Z (1999) Biology and chemistry of rhizosphere influencing nutrient availability. In: Rengel Z (ed) Mineral nutrition of crops: Fundamental mechanisms and implications. The Haworth Press, New York, pp 1–40Google Scholar
  31. Czárán TL, Hoekstra RF, Pagie L (2002) Chemical warfare between microbes promotes biodiversity. Proc Natl Acad Sci U S A 99:786–790. doi:10.1073/pnas.012399899 PubMedCrossRefGoogle Scholar
  32. Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 13:35–47CrossRefGoogle Scholar
  33. d'Angelo-Picard C, Faure D, Penot I, Dessaux Y (2005) Diversity of N-acyl homoserine lactone-producing and -degrading bacteria in soil and tobacco rhizosphere. Environ Microbiol l7:1796–1808PubMedCrossRefGoogle Scholar
  34. Daniels BA, Trappe JM (1980) Factors affecting spore germination of the vesicular-arbusuclar mycorrhizal fungus Glomus epigaeus. Mycologia 72:457–471CrossRefGoogle Scholar
  35. Debette J, Blondeau R (1980) Présence de Pseudomonas maltophilia dans la rhizosphère de quelque plantes cultivée. Can J Microbiol 26:460–463PubMedCrossRefGoogle Scholar
  36. Degrassi G, Devescovi G, Solis R, Steindler L, Venturi V (2007) Oryza sativa rice plants contain molecules that activate different quorum-sensing N-acyl homoserine lactone biosensors and are sensitive to the specific AiiA lactonase. FEMS Microbiol Lett 269:213–220PubMedCrossRefGoogle Scholar
  37. Delalande L, Faure D, Raffoux A, Uroz S, D'Angelo-Picard C, Elasri M, Carlier A, Berruyer R, Petit A, Williams P, Dessaux Y (2005) N-hexanoyl-l-homoserine lactone, a mediator of bacterial quorum-sensing regulation, exhibits plant-dependent stability and may be inactivated by germinating Lotus corniculatus seedlings. FEMS Microbiol Ecol 52:13–20PubMedCrossRefGoogle Scholar
  38. de Weert S, Vermeiren H, Mulders IHM, Kuiper I, Hendrickx N, Bloemberg GV, Vanderleyden J, De Mot R, Lugtenberg BJJ (2002) Flagella-driven chemotaxis towards exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens Mol Plant Microbe Interact 15:1173–1180PubMedCrossRefGoogle Scholar
  39. Dinkelaker B, Hengeler C, Marschner H (1995) Distribution and function of proteoid roots and other root clusters. Bot Acta 108:183–200Google Scholar
  40. Dohrmann AB, Tebbe CC (2005) Effect of elevated tropospheric ozone on the structure of bacterial communities inhabiting the rhizosphere of herbaceous plants native to Germany. Appl Environ Microbiol 71:7750–7758PubMedCrossRefGoogle Scholar
  41. Dong Z, Wu L, Kettlewell B, Caldwell CD, Layzell DB (2003) Hydrogen fertilization of soils - is this a benefit of legumes in rotation? Plant Cell Environ 261:875–1879CrossRefGoogle Scholar
  42. Duineveld BM, Rosado AS, van Elsas JD, van Veen JA (1998) Analysis of the dynamics of bacterial communities in the rhizosphere of the Chrysanthemum via denaturing gradient gel electrophoresis and substrate utilization patterns. Appl Environ Microbiol 64:4950–4957PubMedGoogle Scholar
  43. Düring K, Porsch P, Fladung M, Lörz H (1993) Transgenic potato plants resistant to the phytopathogenic bacterium Erwinia carotovora Plant J 3:587–598CrossRefGoogle Scholar
  44. Farrar J, Hawes M, Jones D, Lindow S (2003) How roots control the flux of carbon to the rhizosphere. Ecology 84:827–837CrossRefGoogle Scholar
  45. Filion M, St-Arnaud M, Jabaji-Hare SH (2003) Direct quantification of fungal DNA from soil substrate using real-time PCR. J Microbiol Meth 53:67–76CrossRefGoogle Scholar
  46. Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36PubMedCrossRefGoogle Scholar
  47. Fuqua C, Parsek MR, Greenberg EP (2001) Regulation of gene expression by cell-to-cell communication: Acyl-homoserine lactone quorum sensing. Annu Rev Genet 35:439–468PubMedCrossRefGoogle Scholar
  48. Gamalero E, Martinotti MG, Trotta A, Lemanceau P, Berta G (2002) Morphogenetic modifications induced by Pseudomonas fluorescens A6RI and Glomus mosseae BEG12in the root system of tomato differ according to the plant growth conditions. New Phytol 155:293–300CrossRefGoogle Scholar
  49. Gantner S, Schmid M, Duerr C, Schuhegger R, Steidle A, Hutzler P, Langebartels C, Eberl L, Hartmann A, Dazzo FB (2006) In situ quantitation of the spatial scale of calling distances and population density-independent N-acylhomoserine lactone-mediated communication by rhizobacteria colonized on plant roots. FEMS Microbiol Ecol 56:188–194PubMedCrossRefGoogle Scholar
  50. Garbaye J (1994) Helper bacteria: A new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210CrossRefGoogle Scholar
  51. Garbeva P, van Veen JA, van Elsas JD (2004) Microbial diversity in soil: Selection of Microbial Populations by Plant and Soil Type and Implications for Disease Suppressiveness. Annu Rev Phytopathol 42:243–270PubMedCrossRefGoogle Scholar
  52. Germida JJ, Siciliano SD (2001)Taxonomic diversity of bacteria associated with the roots of modern, recent and ancient wheat cultivars. Biol Fert Soils 33:410–415CrossRefGoogle Scholar
  53. Germida JJ, Siciliano SD, Renato de Freitas J, Seib AM (1998) Diversity of root-associated bacteria associated with field-grown canola (Brassica napus L.) and wheat (Triticum aestivum L.). FEMS Microbiol Ecol 26:43–50CrossRefGoogle Scholar
  54. Girvan MS, Bullimore J, Pretty JN, Osborn AM, Ball AS (2003) Soil type is the primary determinant of the composition of the total and active bacterial communities in arable soils. Appl Environ Microbiol 69:1800–1809PubMedCrossRefGoogle Scholar
  55. Gollotte A, van Tuinen D, Atkinson D (2004) Diversity of arbuscular mycorrhizal fungi colonising roots of the grass species Agrostis capillaris and Lolium perenne in a field experiment. Mycorrhiza 14:111–117PubMedCrossRefGoogle Scholar
  56. Götz C, Fekete A, Gebefuegi I, Forczek S, Fuksová K, Li X, Englmann M, Gryndler M, Hartmann A, Matucha M, Schmitt-Kopplin P, Schröder P (2007) Uptake, degradation and chiral discrimination of N-acyl-D/L -homoserine lactones by barley (Hordeum vulgare) and yam bean (Pachyrhizus erosus) plants. Anal Bioanal Chem 389:1447–1457PubMedCrossRefGoogle Scholar
  57. Götz M, Nirenberg H, Krause S, Wolters H, Draeger S, Buchner A, Lottmann J, Berg G, Smalla K (2006) Fungal endophytes in potato roots studied by traditional isolation and cultivation-independent DNA-based methods. FEMS Microbiol Ecol 58:404–413PubMedCrossRefGoogle Scholar
  58. Grayston SJ, Wang S, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378CrossRefGoogle Scholar
  59. Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307–319PubMedCrossRefGoogle Scholar
  60. Harley JL, Smith SE (1983) Mycorrhizal Symbioses. Academic Press Inc., London, New York, pp 483Google Scholar
  61. Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153:335–344CrossRefGoogle Scholar
  62. Hartmann A (1988) Ecophysiological aspects of growth and nitrogen fixation in Azospirillum spp. Plant Soil 110:225–238CrossRefGoogle Scholar
  63. Hartmann A, Rothballer M, Schmid M (2008) Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant Soil 312:7–14Google Scholar
  64. Hempel S, Renker C, Buscot F (2007) Differences in the species composition of arbuscular mycorrhizal fungi in spore, root and soil communities in a grassland ecosystem. Environ Microbiol 9:1930–1938PubMedCrossRefGoogle Scholar
  65. Hense BA, Kuttler C, Müller J, Rothballer M, Hartmann A, Kreft J-U (2007) Does efficiency sensing unify diffusion and quorum sensing? Nat Rev Microbiol 5:230–239PubMedCrossRefGoogle Scholar
  66. Hentzer M, Riedel K, Rasmussen TB, Heydorn A, Andersen JB, Parsek MR, Rice SA, Eberl L, Molin S, Hoiby N, Kjelleberg S, Givskov M (2002) Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiol 148:87–102Google Scholar
  67. Heuer H, Kroppenstedt RM, Lottmann J, Berg G, Smalla K (2002) Effects of T4 lysozyme release from transgenic potato roots on bacterial rhizosphere communities are negligible relative to natural factors. Appl Environ Microbiol 68:1325–1335PubMedCrossRefGoogle Scholar
  68. Hinsinger P, Plassard C, Tang C, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: A review. Plant Soil 248:43–59CrossRefGoogle Scholar
  69. Hornschuh M, Grotha R, Kutschera U (2002) Epiphytic bacteria associated with the bryophyte Funaria hygrometrica: Effect of Methylobacterium strains on protonema development. Plant Biol 4:682–682CrossRefGoogle Scholar
  70. Husband R, Herre EA, Young JPW (2002) Temporal variation in the arbuscular mycorrhizal communities colonising seedlings in a tropical forest. FEMS Microbiol Ecol 42:131–136CrossRefPubMedGoogle Scholar
  71. Ikemoto S, Suzuki K, Kaneko T, Komagata K (1980) Characterization of strains of Pseudomonas maltophilia which do not require methionine. Int J Syst Bacteriol 30:437–447CrossRefGoogle Scholar
  72. Jaeger CHIII, Lindow SE, Miller W, Clark E, Firestone MK (1999) Mapping of sugar and amino acid availability in soil around roots with bacterial sensors of sucrose and tryptophan. Appl Environ Microbiol 65:2685–2690PubMedGoogle Scholar
  73. Jansa J, Mozafar A, Anken T, Ruh R, Sanders I, Frossard E (2002) Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza 12:225–234PubMedCrossRefGoogle Scholar
  74. Johnson D, Leake JR, Ostle N, Ineson P, Read DJ (2002) In situ 13CO2 pulse-labelling of upland grassland demonstrates a rapid pathway of carbon flux from arbuscular mycorrhizal mycelia to the soil. New Phytol 153:327–334CrossRefGoogle Scholar
  75. Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163:459–480CrossRefGoogle Scholar
  76. Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat Rev Microbiol 5:619–633PubMedCrossRefGoogle Scholar
  77. Kowalchuk GA, Bruinsma M, van Veen JA (2003) Assessing responses of soil microorganisms to GM plants. Trends Ecol Evol 18:403–410CrossRefGoogle Scholar
  78. Kremer RJ, Begonia MFT, Stanley L, Lanham ET (1990) Characterization of rhizobacteria associated with weed seedlings. Appl Environ Microbiol 56:1649–1655PubMedGoogle Scholar
  79. Kuzyakov Y, Bol R (2005) Three sources of CO2 efflux from soil partitioned by 13C natural abundance in an incubation study. Rapid Commun Mass Spectrom 19:1417–1423PubMedCrossRefGoogle Scholar
  80. Lehr NA, Schrey SD, Bauer R, Hampp R, Tarkka MT (2007) Suppression of plant defence response by a mycorrhiza helper bacterium. New Phytol 174:892–903PubMedCrossRefGoogle Scholar
  81. Leveau JH, Gerards S (2008) Discovery of a bacterial gene cluster for catabolism of the plant hormone indole 3-acetic acid. FEMS Microbiol Ecol 65:238–250PubMedCrossRefGoogle Scholar
  82. Lottmann J, Berg G (2001) Phenotypic and genotypic characterization of antagonistic bacteria associated with roots of transgenic and non-transgenic potato plants. Microbiol Res 156:75–82PubMedCrossRefGoogle Scholar
  83. Lottmann J, Heuer H, Smalla K, Berg G (1999) Influence of transgenic T4-lysozyme-producing potato plants on potentially beneficial plant-associated bacteria. FEMS Microbiol Ecol 29:365–377CrossRefGoogle Scholar
  84. Lottmann J, Heuer H, Vries J, Mahn A, During K, Wackernagel W, Smalla K, Berg G (2000) Establishment of introduced antagonistic bacteria in the rhizosphere of transgenic potatoes and their effect on the bacterial community. FEMS Microbiol Ecol 33:41–49PubMedCrossRefGoogle Scholar
  85. Lu Y, Conrad R (2005) In situ stable isotope probing of methanogenic Archaea in the rice rhizosphere. Science 309:1088–1090PubMedCrossRefGoogle Scholar
  86. Lu Y, Rosencrantz D, Liesack W, Conrad R (2006) Structure and activity of bacterial community inhabiting rice roots and the rhizosphere. Environ Microbiol 8(8):1351–1360PubMedCrossRefGoogle Scholar
  87. Lugtenberg BJJ, Dekkers LC (1999) What makes Pseudomonas bacteria rhizosphere competent? Environ Microbiol 1:9–13PubMedCrossRefGoogle Scholar
  88. Mansfeld-Giese K, Larsen J, Bodker L (2002) Bacterial populations associated with mycelium of the arbuscular mycorrhizal fungus Glomus intraradices. FEMS Microbiol Ecol 41:133–140CrossRefPubMedGoogle Scholar
  89. Mansouri H, Petit A, Oger P, Dessaux Y (2002) Engineered rhizosphere: the trophic bias generated by opine-producing plants is independent of the opine type, the soil origin, and the plant species. Appl Environ Microbiol 68:2562–2566PubMedCrossRefGoogle Scholar
  90. MarkG L, Dow JM, Kiely PD, Higgins H, Haynes J, Baysse C, Abbas A, Foley T, Franks A, Morrissey J, O, Gara F (2005) Transcriptome profiling of bacterial responses to root exudates identifies genes involved in microbe-plant interactions. Proc Natl Acad Sci U S A 102:17454–17459PubMedCrossRefGoogle Scholar
  91. Marschner H (1991) Root-induced changes in the availability of micronutrients in the rhizosphere. In: Waise lY, Eshel A, Kakafi U (eds) Plant Roots: The Hidden Half, Marcel Dekker, New York, U S A, p. 503Google Scholar
  92. Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102Google Scholar
  93. Marschner H, Römheld V (1994) Strategies of plants for acquisition of iron. Plant Soil 165:261–274CrossRefGoogle Scholar
  94. Marschner P, Crowley DE (1998) Phytosiderophores decrease iron stress and pyoverdine production of Pseudomonas fluorescens PF-5 (PVD-INAZ). Soil Biol Biochem 30:1275–1280CrossRefGoogle Scholar
  95. Marschner P, Baumann K (2003) Changes in bacterial community structure induced by mycorrhizal colonisation in split-root maize. Plant Soil 251:279–289CrossRefGoogle Scholar
  96. Marschner P, Yang CH, Lieberei R, Crowley DE (2001) Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol Biochem 33:1437–1445CrossRefGoogle Scholar
  97. Mathimaran N, Ruh R, Vullioud P, Frossard E, Jansa J (2005)Glomus intraradices dominates arbuscular mycorrhizal communities in a heavy textured agricultural soil. Mycorrhiza 16:61–66PubMedCrossRefGoogle Scholar
  98. Matilla M, Espinosa-Urgel M, Rodriguez-Herva J, Ramos J, Ramos-Gonzalez M (2007) Genomic analysis reveals the major driving forces of bacterial life in the rhizosphere. Genome Biol 8:R179PubMedCrossRefGoogle Scholar
  99. Mayo K, Davies RE, Motta J (1986) Stimulation of germination of spores of Glomus versiforme by spore associated bacteria. Mycologia 78:426–431CrossRefGoogle Scholar
  100. Miller HJ, Henken G, van Veen JA (1989) Variation and composition of bacterial populations in the rhizospheres of maize, wheat and grass cultivars. Can J Microbiol 35:656–660CrossRefGoogle Scholar
  101. Miller LD, Yost CK, Hynes MF, Alexandre G (2007) The major chemotaxis gene cluster of Rhizobium leguminosarum bv. viciae is essential for competitive nodulation. Mol Microbiol 63:348–362PubMedCrossRefGoogle Scholar
  102. Moenne-Loccoz Y, McHugh B, Stephens PM, McConnell FI, Glennon JD, Dowling DN, O'Gara F (1996) Rhizosphere competence of fluorescent Pseudomonas spB24 genetically modified to utilise additional ferric siderophores. FEMS Microbiol Ecol 19:215–225Google Scholar
  103. 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 (FISH) and confocal laser scanning microscopy (CLSM). Mycorrhiza 9:272–278CrossRefGoogle Scholar
  104. Moore JC, McCann K, de Ruiter PC (2007) Soil rhizosphere food webs, their stability, and implications for soil processes in ecosystems. In: Cardon ZG, Whitbeck JL (eds) The rhizosphere: An ecological perspective. Academic Press Inc., London, New York, pp 101–125Google Scholar
  105. Mosse B (1959) The regular germination of resting spores and some observations on the growth requirements of an Endogone sp. causing vesicular-arbuscular mycorrhiza. Trans Br Mycol Soc 42:273–286CrossRefGoogle Scholar
  106. Mougel C, Offre P, Ranjard L, Corberand T, Gamalero E, Robin C, Lemanceau P (2006) Dynamic of the genetic structure of bacterial and fungal communities at different developmental stages of Medicago truncatula Gaertn. cv. Jemalong line J5. New Phytol 170:165–175PubMedCrossRefGoogle Scholar
  107. Neumann G, Martinoia E (2002) Cluster roots - an underground adaptation for survival in extreme environments. Trends Plant Sci 7:162–167PubMedCrossRefGoogle Scholar
  108. Nunan N, Daniell TJ, Singh BK, Papert A, McNicol JW, Prosser JI (2005) Links between Plant and Rhizoplane Bacterial Communities in Grassland Soils, Characterized Using Molecular Techniques. Appl Environ Microbiol 71:6784–6792PubMedCrossRefGoogle Scholar
  109. O'Connell KP, Goodman RM, Handelsman J (1996) Engineering the rhizosphere: expressing a bias. Trends Biotechnol 14:83–88CrossRefGoogle Scholar
  110. Oehl F, Sieverding E, Ineichen K, Mader P, Boller T, Wiemken A (2003) Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of central europe. Appl Environ Microbiol 69:2816–2824PubMedCrossRefGoogle Scholar
  111. Oehl F, Sieverding E, Ineichen K, RisE-A, Boller T, Wiemken A (2005) Community structure of arbuscular mycorrhizal fungi at different soil depths in extensively and intensively managed agroecosystems. New Phytol 165:273–283PubMedCrossRefGoogle Scholar
  112. Oger P, Petit A, Dessaux Y (1997) Genetically engineered plants producing opines alter their biological environment. Nat Biotechnol 15:369–372PubMedCrossRefGoogle Scholar
  113. Oger PM, Mansouri H, Nesme X, Dessaux Y (2004) Engineering root exudation of Lotus toward the production of two novel carbon compounds leads to the selection of distinct microbial populations in the rhizosphere. Microb Ecol 47:96–103PubMedCrossRefGoogle Scholar
  114. Oliver KL, Hamelin RC, Hintz WE (2008) Effects of transgenic hybrid aspen over-expressing P 1 olyphenol oxidase on rhizosphere diversity. Appl Environ Microbiol. doi:10.1128/AEM.02836-02807
  115. Olsson PA, Thingstrup I, Jakobsen I, Baath F (1999) Estimation of the biomass of arbuscular mycorrhizal fungi in a linseed field. Soil Biol Biochem 31:1879–1887CrossRefGoogle Scholar
  116. Paterson E, Gebbing T, Abel C, Sim A, Telfer G (2007) Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytol 173:600–610PubMedCrossRefGoogle Scholar
  117. Pearson JN, Abbott LK, Jasper DA (1993) Mediation of competition between two colonizing VA mycorrhizal fungi by host plants. New Phytol 123:93–98CrossRefGoogle Scholar
  118. Pivato B, Mazurier S, Lemanceau P, Siblot S, Berta G, Mougel C, van Tuinen D (2007) Medicago species affect the community composition of arbuscular mycorrhizal fungi associated with roots. New Phytol 176:197–210PubMedCrossRefGoogle Scholar
  119. Prosser JI, Rangel-Castro JI, Killham K (2006) Studying plant-microbe interactions using stable isotope technologies. Curr Opin Biotechnol 17:98–102PubMedCrossRefGoogle Scholar
  120. Raaijmakers JM, Paulitz CT, Steinberg C, Alabouvette C, Moenne-Loccoz Y (2008) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil. doi:10.1007/s11104-11008-19568-11106
  121. Radajewski S, Ineson P, Parekh NR, Murrell JC (2000) Stable-isotope probing as a tool in microbial ecology. Nature 403:646–649PubMedCrossRefGoogle Scholar
  122. Rambelli A (1973) The Rhizosphere of mycorrhizae. In: Mg L, Koslowski TT (eds) Ectomycorrhizae. Academic Press, New York, pp 299–343Google Scholar
  123. Rangel-Castro JI, Killham K, Ostle N, Nicol GW, Anderson IC, Scrimgeour CM, Ineson P, Meharg A, Prosser JI (2005) Stable isotope probing analysis of the influence of liming on root exudate utilization by soil microorganisms. Environ Microbiol 7:828–838PubMedCrossRefGoogle Scholar
  124. Rasche F, Hodl V, Poll C, Kandeler E, Gerzabek MH, van Elsas JD, Sessitsch A (2006) Rhizosphere bacteria affected by transgenic potatoes with antibacterial activities compared with the effects of soil, wild-type potatoes, vegetation stage and pathogen exposure. FEMS Microbiol Ecol 56:219–235PubMedCrossRefGoogle Scholar
  125. Rasmussen TB, Bjarnsholt T, Skindersoe ME, Hentzer M, Kristoffersen P, Kote M, Nielsen J, Eberl L, Givskov M (2005) Screening for quorum-sensing inhibitors (QSI) by use of a novel genetic system, the QSI selector. J Bacteriol 187:1799–1814PubMedCrossRefGoogle Scholar
  126. Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci U S A 91:11841–11843PubMedCrossRefGoogle Scholar
  127. Rengel Z (1999) Physiological mechanisms underlying differential nutrient efficiency of crop genotypes. In: Rengel Z (ed) Mineral nutrition of crops: Mechanisms and implications, The Haworth Press, New York, U S A, pp 227–265Google Scholar
  128. Rengel Z, Marschner P (2005) Nutrient availability and management in the rhizosphere: exploiting genotypic differences. New Phytol 168:305–312PubMedCrossRefGoogle Scholar
  129. Rettenmaier H, Lingens F (1985) Purification and some properties of two isofunctional juglone hydroxylases from Pseudomonas putida J1. Biol Chem Hoppe Seyler 366(7):637–646PubMedGoogle Scholar
  130. Richter DD, OhN-H, Fimmen R, Jackson J (2007) The rhizosphere and soil formation. In: Cardon ZG, Whitbeck JL (eds) The rhizosphere: An ecological perspective. Elsevier Academic Press, Burlington, U S A, pp 179–200Google Scholar
  131. Riedlinger J, Schrey SD, Tarkka MT, Hampp R, Kapur M, Fiedler H-P (2006) Auxofuran, a novel metabolite that stimulates the growth of fly agaric, is produced by the mycorrhiza helper bacterium Streptomyces strain AcH 505. Appl Environ Microbiol 72:3550–3557PubMedCrossRefGoogle Scholar
  132. Rillig MC, Lutgen ER, Ramsey PW, Klironomos JN, Gannon JE (2005) Microbiota accompagning different arbuscular mycorrhizal fungal isolates influence soil aggregation. Pedobiologia 49:251–259CrossRefGoogle Scholar
  133. Rillig MC, Mummey DL, Ramsey PW, Klironomos JN, Gannon JE (2006) Phylogeny of arbuscular mycorrhizal fungi predicts community composition of symbiosis-associated bacteria. FEMS Microbiol Ecol 57:389–395PubMedCrossRefGoogle Scholar
  134. Rodriguez-Navarro DN, Dardanelli MS, Ruiz-Sainz JE (2007) Attachment of bacteria to the roots of higher plants. FEMS Microbiol Lett 272:127–136PubMedCrossRefGoogle Scholar
  135. Roose T, Fowler AC (2004) A mathematical model for water and nutrient uptake by plant root systems. J Theor Biol 228:173–184PubMedCrossRefGoogle Scholar
  136. Rosenblueth M, Martinez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact 19:827–837PubMedCrossRefGoogle Scholar
  137. Rothballer M, Schmid M, Fekete A, Hartmann A (2005) Comparative in situ analysis of ipdC-gfpmut3 promoter fusions of Azospirillum brasilense strains Sp7 and Sp245. Environ Microbio l7:1839–1846PubMedCrossRefGoogle Scholar
  138. Ryu C-M, Farag MA, Hu C-H, Reddy MS, Kloepper JW, Pare PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026PubMedCrossRefGoogle Scholar
  139. Savka MA, Dessaux Y, Oger P, Rossbach S (2002) Engineering bacterial competitiveness and persistence in the phytosphere. Mol Plant Microbe Interact 15:866–874PubMedCrossRefGoogle Scholar
  140. Scheublin TR, Ridgway KP, Young JPW, van der Heijden MGA (2004) Nonlegumes, legumes, and root nodules harbor different arbuscular mycorrhizal fungal communities. Appl Environ Microbiol 70:6240–6246PubMedCrossRefGoogle Scholar
  141. Schloter M, Lebuhn M, Heulin T, Hartmann A (2000) Ecology and evolution of bacterial microdiversity. FEMS Microbiol Rev 24:647–660PubMedCrossRefGoogle Scholar
  142. Schuhegger R, Ihring A, Gantner S, Bahnweg G, Knappe C, Vogg G, Hutzler P, Schmid M, van Breusegem F, Eberl L, Hartmann A, Langebartels C (2006) Induction of systemic resistance in tomato by N-acylhomoserine lactone-producing rhizosphere bacteria. Plant Cell and Environment 29:909–918CrossRefGoogle Scholar
  143. Schulz B, Boyle C, Sieber N (2006) Microbial root endophytes. Springer VerlagBerlin, Heidelberg, New YorkCrossRefGoogle Scholar
  144. Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: Phylogeny and evolution. Mycol Res 105:1413–1421CrossRefGoogle Scholar
  145. Schwarzott D, Walker C, Schuler A (2001)Glomus, the largest genus of the arbuscular mycorrhizal fungi (Glomales), is non monophyletic. Mol Phylogenet Evol 21:190–197PubMedCrossRefGoogle Scholar
  146. Selesi D, Schmid M, Hartmann A (2005) Diversity of green-like and red-like ribulose−1,5-bisphosphate carboxylase/oxygenase large-subunit genes (cbbL) in differently managed agricultural soils. Appl Environ Microbiol 71:175–184PubMedCrossRefGoogle Scholar
  147. Selim S, Negrel J, Govaerts C, Gianinazzi S, van Tuinen D 92005) Isolation and partial characterization of antagonistic peptides produced by Paenibacillus spstrain B2 isolated from the Sorghum mycorrhizosphere. Appl Environ Microbiol 71:6501–6507PubMedCrossRefGoogle Scholar
  148. Shaw LJ, Morris P, Hooker JE (2006) Perception and modification of plant flavonoid signals by rhizosphere microorganisms. Environ Microbiol 8:1867–1880PubMedCrossRefGoogle Scholar
  149. Simpson FB, Burris RH (1984) A nitrogen pressure of 50 atmospheres does not prevent evolution of hydrogen by nitrogenase. Science 224:1095–1097PubMedCrossRefGoogle Scholar
  150. Singh BK, Nunan N, Ridgway KP, McNicol J, Young JPW, Daniell TJ, Prosser JI, Millard P (2008) Relationship between assemblages of mycorrhizal fungi and bacteria on grass roots. Environ Microbiol 10:534–541PubMedCrossRefGoogle Scholar
  151. Skene KR (2000) Pattern formation in cluster roots: Some developmental and evolutionary considerations. Ann Bot 85:901–908CrossRefGoogle Scholar
  152. Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (2001)Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: Plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751PubMedCrossRefGoogle Scholar
  153. Smith SE, Read DJ (1997) Mycorrhizal Symbiosis. Academic Press, LondonGoogle Scholar
  154. Somers E, Vanderleyden J, Srinivasan M (2004)Rhizosphere bacterial signalling: A love parade beneath our feet. Crit Rev Microbiol 304:205–240PubMedCrossRefGoogle Scholar
  155. Soto MJ, Sanjuan J, Olivares J (2006) Rhizobia and plant-pathogenic bacteria: common infection weapons. Microbiol 152:3167–3174CrossRefGoogle Scholar
  156. Stein S, Selesi D, Schilling R, Pattis I, Schmid M, Hartmann A (2005) Microbial activity and bacterial composition of H2-treated soils with net CO2 fixation. Soil Biol Biochem 37:1938–1945CrossRefGoogle Scholar
  157. Teplitski M, Robinson JB, Bauer WD (2000) Plants secrete substances that mimic bacterial N-Acyl Homoserine Lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol Plant Microbe Interact 13:637–648PubMedCrossRefGoogle Scholar
  158. Thordal-Christensen H (2003) Fresh insights into processes of nonhost resistance. Curr Opin Plant Biol 6:351–357PubMedCrossRefGoogle Scholar
  159. Tjamos EC, Rowe RC, Heale JB, Fravel DR (2000) Advances in Verticillium research and disease managementAPS Press. The American Phytopathological Society, Minnesota, USA, 357Google Scholar
  160. Toljander JF, Lindahl BD, Paul LR, Elfstrand M, Finlay RD (2007) Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. FEMS Microbiol Ecol 61:295–304PubMedCrossRefGoogle Scholar
  161. Treonis AM, Ostle NJ, Stott AW, Primrose R, Grayston SJ, Ineson P (2004) Identification of groups of metabolically-active rhizosphere microorganisms by stable isotope probing of PLFAs. Soil Biol Biochem 36:533–537CrossRefGoogle Scholar
  162. Tucker SL, Talbot NJ (2001) Surface attachment and pre-penetration stage development by plant pathogenic fungi. Annu Rev Phytopathol 39:385–417PubMedCrossRefGoogle Scholar
  163. Turnau K, Ryszka P, Gianinazzi-Pearson V, van Tuinen D (2001)Identification of arbuscular mycorrhizal fungi in soils and roots of plants colonizing zinc wastes in southern Poland. Mycorrhiza 10:169–174CrossRefGoogle Scholar
  164. Uren NC (1981) Chemical reduction of an insoluble higher oxide of manganese by plant roots. J Plant Nutr Soil Sci 4:65–71Google Scholar
  165. Uren NC (2007) Types, amounts and possible functions of compounds released into the rhizosphere by soil-grown plants. In: Pinto RZ, Varanini PN (eds) The Rhizosphere: Biochemistry and organic substances at the soil-plant interface. CRC Press, Boca Raton, Florida, USA, pp 1–21Google Scholar
  166. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72CrossRefGoogle Scholar
  167. van Elsas JD, Turner S, Bailey MJ (2003) Horizontal gene transfer in the phytosphere. New Phytol 157:525–537CrossRefGoogle Scholar
  168. van Tuinen D, Jacquot E, Zhao B, Gollotte A, Gianinazzi-Pearson V (1998) Characterization of root colonization profiles by a microcosm community of arbuscular mycorrhizal fungi using 25S rDNA-targeted nested PCR. Mol Ecol 7:879–887PubMedCrossRefGoogle Scholar
  169. van Veen JA, Morgan JAW, Whipps JM (2007) Methodological approaches to the study of carbon flow and the associated microbial population dynamics in the rhizospherePintoRZ, VaraniniPNThe Rhizosphere: Biochemistry and organic substances at the soil-plant interface. CRC Press , Boca Raton, Florida, USA, 371–399Google Scholar
  170. Vandenkoornhuyse P, Ridgway KP, Watson IJ, Fitter AH, Young JPW (2003) Co-existing grass species have distinctive arbuscular mycorrhizal communities. Mol Ecol 12:3085–3095PubMedCrossRefGoogle Scholar
  171. von Rad U, Klein I, Dobrev PI, Kottova J, Zazimalova E, Fekete A, Hartmann A, Schmitt-Kopplin P, Durner J (2008) Response of Arabidopsis thaliana to N-hexanoyl-DL-homoserinelactone, a bacterial quorum sensing molecule produced in the rhizosphere. Planta. doi:10.1007/s00425-008-0811-4
  172. von Wiren N, Marschner H, Römheld V (1995) Uptake kinetics of iron-phytosiderophores in two maize genotypes differing in iron efficiency. Physiol Plant 93:611–616CrossRefGoogle Scholar
  173. von Wiren N, Mori S, Marschner H, Römheld V (1994) Iron inefficiency in maize mutant ys1 (Zea mays Lcv Yellow-Stripe) is caused by a defect in uptake of iron phytosiderophores. Plant Physiol 106:71–77Google Scholar
  174. Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299PubMedCrossRefGoogle Scholar
  175. Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511PubMedGoogle Scholar
  176. Wolfe B, Mummey D, Rillig M, Klironomos J (2007) Small-scale spatial heterogeneity of arbuscular mycorrhizal fungal abundance and community composition in a wetland plant community. Mycorrhiza 17:175–183PubMedCrossRefGoogle Scholar
  177. Yan F, Zhu Y, Muller C, Zorb C, Schubert S (2002) Adaptation of H+-pumping and plasma membrane H+ ATPase activity in proteoid roots of white Lupin under phosphate deficiency. Plant Physiol 129:50–63PubMedCrossRefGoogle Scholar
  178. Yao J, Allen C (2006) Chemotaxis is required for virulence and competitive fitness of the bacterial wilt pathogen Ralstonia solanacearum. J Bacteriol 188:3697–3708PubMedCrossRefGoogle Scholar
  179. Zabetakis I (1997) Enhancement of flavour biosynthesis from strawberry (Fragaria ananassa) callus cultures by Methylobacterium species. Plant Cell Tissue Organ Cult 50:179–183CrossRefGoogle Scholar
  180. Zeidler D, Zahringer U, Gerber I, Dubery I, Hartung T, BorsW, Hutzler P, Durner J (2004) From The Cover: Innate immunity in Arabidopsis thaliana: Lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. Proc Natl Acad Sci U S A 101:15811–15816PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Anton Hartmann
    • 1
  • Michael Schmid
    • 1
  • Diederik van Tuinen
    • 2
  • Gabriele Berg
    • 3
  1. 1.Department Microbe-Plant InteractionsHelmholtz Zentrum München, German Research Center for Environmental Health (GmbH)NeuherbergGermany
  2. 2.UMR INRA Université de Bourgogne, Plante-Microbe-Environnement CMSE-INRADijon CedexFrance
  3. 3.Institute for Environmental BiotechnologyGraz University of TechnologyGrazAustria

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