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Cited by 62Plant-Microbe Interactions and ImmunityBacterial biofilms and quorum sensingLegume Nitrogen Fixing Symbiosis

Identification of Traits Shared by Rhizosphere-Competent Strains of Fluorescent Pseudomonads

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Ghirardi, Sandrine, Dessaint, Fabrice, Mazurier, Sylvie, Corberand, Thérèse, Raaijmakers, Jos M., Meyer, Jean-Marie, Dessaux, Yves, Lemanceau, Philippe·2012·Microbial Ecology
DOI 10.1007/s00248-012-0065-3
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Abstract

Rhizosphere competence of fluorescent pseudomonads is a prerequisite for the expression of their beneficial effects on plant growth and health. To date, knowledge on bacterial traits involved in rhizosphere competence is fragmented and derived mostly from studies with model strains. Here, a population approach was taken by investigating a representative collection of 23 Pseudomonas species and strains from different origins for their ability to colonize the rhizosphere of tomato plants grown in natural soil. Rhizosphere competence of these strains was related to phenotypic traits including: (1) their carbon and energetic metabolism represented by the ability to use a wide range of organic compounds, as electron donors, and iron and nitrogen oxides, as electron acceptors, and (2) their ability to produce antibiotic compounds and N-acylhomoserine lactones (N-AHSL). All these data including origin of the strains (soil/rhizosphere), taxonomic identification, phenotypic cluster based on catabolic profiles, nitrogen dissimilating ability, siderovars, susceptibility to iron starvation, antibiotic and N-AHSL production, and rhizosphere competence were submitted to multiple correspondence analyses. Colonization assays revealed a significant diversity in rhizosphere competence with survival rates ranging from approximately 0.1 % to 61 %. Multiple correspondence analyses indicated that rhizosphere competence was associated with siderophore-mediated iron acquisition, substrate utilization, and denitrification. However, the catabolic profile of one rhizosphere-competent strain differed from the others and its competence was associated with its ability to produce antibiotics phenazines and N-AHSL. Taken together, these data suggest that competitive strains have developed two types of strategies to survive in the rhizosphere.

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Research works printed but not linked: 78

  1. 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 · Paper page
  2. Benzécri JP, Benzécri F, Birou A, Blumenthal S, de Boeck A, Bordet J-P, Cancelier G, Cazes P, da Costa Nicolau F, Danech-Pajou M, Delprat R, Demonet M, Escoffier B, Forcade A, Friant F, Grelet Y, Kalogéroupolos D, Lebart L, Lebaux M-O, Leroy P, Marcotorchino J-F, Moussa T, Mutombo F, Nora C, Prost A, Rezvani A, Robert J, Rosenzveig C, Roux M, Solety P, Stépan S, Tabard N, Thauront G, de Virille M, Vuillaume Y (1973) L'analyse des données. Tome 2: L'analyse des correspondances. Dunod, Paris
  3. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13 · DOI
  4. Bergsma-Vlami M, Prins ME, Raaijmakers JM (2005) Influence of plant species on population dynamics, genotypic diversity and antibiotic production in the rhizosphere by indigenous Pseudomonas spp. FEMS Microbiol Ecol 52:59–69 · DOI
  5. Berta G, Sampo S, Gamalero E, Massa N, Lemanceau P (2005) Suppression of Rhizoctonia root-rot of tomato by Glomus mossae BEG12 and Pseudomonas fluorescens A6RI is associated with their effect on the pathogen growth and on the root morphogenesis. Eur J Plant Pathol 111:279–288 · DOI
  6. Bossis E, Lemanceau P, Latour X, Gardan L (2000) Taxonomy of Pseudomonas fluorescens and Pseudomonas putida: current status and need for revision. Agronomie 20:51–63 · DOI
  7. Bull CT, Weller DM, Thomashow LS (1991) Relationship between root colonization and suppresssion of Gaeumannomyces graminis var. tritici by Pseudomonas fluorescens strain 2–79. Phytopathology 81:954–959 · DOI
  8. Clays-Josserand A, Lemanceau P, Philippot L, Lensi R (1995) Influence of two plant species (flax and tomato) on the distribution of nitrogen dissimilative abilities within fluorescent Pseudomonas spp. Appl Environ Microbiol 61:1745–1749 · DOI
  9. de Souza JT, Weller DM, Raaijmakers JM (2003) Frequency, diversity, and activity of 2,4-diacetylphloroglucinol-producing fluorescent Pseudomonas spp. in dutch take-all decline soils. Phytopathology 93:54–63 · DOI
  10. De Weger LA, Van Der Vlught CIM, Wijfjes AHM, Bakker PAHM, Lugtenberg BJJ (1987) Flagella of a plant-growth-stimulating Pseudomonas fluorescens strain are required for colonization of potato roots. J Bacteriol 169:2769–2773 · DOI
  11. Delorme S, Philippot L, Edel-Hermann V, Deulvot C, Mougel C, Lemanceau P (2003) Compared genetic diversity of the narG, nosZ and 16S rRNA genes in fluorescent pseudomonads. Appl Environ Microbiol 69:1004–1012 · DOI
  12. Dietrich LEP, Teal TK, Price-Whealan A, Newman DK (2008) Redox-active antibiotics control gene expression and community behavior of divergent bacteria. Science 321:1203–1206 · DOI
  13. Elasri M, Delorme S, Lemanceau P, Stewart G, Laue B, Glickmann E, Oger PM, Dessaux Y (2001) Acyl-homoserine lactone production is more common amongst plant-associated than soil-borne Pseudomonas spp. Appl Environ Microbiol 67:1198–1209 · DOI
  14. Ellis RJ, Timms-Wilson TM, Bailey MJ (2000) Identification of conserved traits in fluorescent pseudomonads with antifungal activity. Environ Microbiol 2:274–284 · DOI
  15. Eparvier A, Lemanceau P, Alabouvette C (1991) Population dynamics of non-pathogenic Fusarium and fluorescent Pseudomonas strains in rockwool, a substratum for soilless culture. FEMS Microbiol Ecol 86:177–184 · DOI
  16. Fravel DR (2005) Commercialization and implementation of biocontrol. Ann Rev Phytopathol 43:337–359 · DOI
  17. Frey P, 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 · DOI
  18. Frey-Klett P, Churin JL, Pierrat JC, 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 31:1555–1562 · DOI
  19. Fuchs R, Schäfer M, Geoffroy V, Meyer JM (2001) Siderotyping–a powerful tool for the characterization of pyoverdines. Curr Topics Med Chem 1:31–57 · DOI
  20. Gamalero E, Martinotti MG, Trotta A, Lemanceau P, Berta G (2002) Morphogenetic modifications induced by Pseudomonas fluorescens A6RI and Glomus mosseae BEG12 in the root system of tomato differ according to the plant growth conditions. New Phytol 155:293–300 · DOI
  21. 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 42:243–270 · DOI · Paper page
  22. Glandorf DCM, Brand I, Bakker PAHM, Schippers B (1992) Stability of rifampicin resistance as a marker for root colonization studies of Pseudomonas putida in the field. Plant Soil 147:135–142 · DOI
  23. Glandorf DCM, Peters LG, Van der Sluis I, Bakker PAHM, Schippers B (1993) Crop specificity of rhizosphere pseudomonads and the involvement of root agglutinins. Soil Biol Biochem 25:981–989 · DOI
  24. Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117 · DOI
  25. Greenacre MJ (1984) Theory and applications of correspondence analysis. Academic, London
  26. Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307–319 · DOI
  27. Hernandez ME, Kappler A, Newman DK (2004) Phenazines and other redox-active antibiotics promote microbial mineral reduction. Appl Environ Microbiol 70:921–928 · DOI
  28. Howie WJ, Cook RJ, Weller DM (1987) Effects of soil matric potential and cell motility on wheat root colonization by fluorescent pseudomonads suppressive to take-all. Phytopathology 77:286–292 · DOI
  29. Jaccard P (1908) Nouvelles recherches sur la distribution florale. Bull Soc Vaud Sci Nat 44:223–270
  30. Kamilova F, Kravchenko LV, Shaposhnikov AI, Azarova T, Makarova N, Lugtenberg BJJ (2006) Organic acids, sugars, and l-tryptophane in exudates of vegetables growing on stonewool and their effects on activities of rhizosphere bacteria. Mol Plant-Microbe Interact 19:250–256 · DOI
  31. King EO, Ward MK, Raney DE (1954) Two simple media for the demonstration of pyocyanin and fluorescein. J Lab Clin Med 44:301–307
  32. Koedam N, Wittouck E, Gabbala A, Gillis A, Höfte M, Cornellis P (1994) Detection and differentiation of microbial siderophores by isoelectric focusing and chrome azurol S. overlay. BioMetals 7:287–291 · DOI
  33. Latour X, Delorme S, Mirleau P, Lemanceau P (2003) Identification of traits implicated in the rhizosphere competence of fluorescent pseudomonads: description of a strategy based on population and model strain studies. Agronomie 23:397–405 · DOI
  34. Latour X, Corberand T, Laguerre G, Allard F, Lemanceau P (1996) The composition of fluorescent pseudomonad population associated with roots is influenced by plant and soil type. Appl Environ Microbiol 62:2449–2556 · DOI
  35. Lemanceau P (1992) Beneficial-effects of rhizobacteria on plants—example of fluorescent Pseudomonas spp. Agronomie 12:413–437 · DOI
  36. Lemanceau P, Alabouvette C (1991) Biological control of Fusarium diseases by fluorescent Pseudomonas and non-pathogenic Fusarium. Crop Prot 10:279–286 · DOI
  37. Lemanceau P, Alabouvette C (1993) Suppression of Fusarium wilts by fluorescent pseudomonads: mechanisms and applications. Biocontrol Sci Tech 3:219–234 · DOI
  38. Lemanceau P, Alabouvette C, Couteaudier Y (1988) Recherches sur la résistance des sols aux maladies. XIV. Modification du niveau de réceptivité d'un sol résistant et d’un sol sensible aux fusarioses vasculaires en réponse à des apports de fer et de glucose. Agronomie 8:155–162 · DOI
  39. Lemanceau P, Maurhofer M, Défago G (2006) Contribution of studies on suppressive soils to the identification of bacterial control agents and to the knowledge of their modes of actions. In: Gnanamanickam SS (ed) Plant-associated bacteria. Springer, Dordrecht, pp 231–267 · DOI
  40. Lemanceau P, Samson R, Alabouvette C (1988) Recherches sur la résistance des sols aux maladies. XV. Comparaison des populations de Pseudomonas fluorescents dans un sol résistant et un sol sensible aux fusarioses vasculaires. Agronomie 8:243–249 · DOI
  41. Lemanceau P, Corberand T, Gardan L, Latour X, Laguerre G, Boeufgras J-M, Alabouvette C (1995) Effect of two plant species flax (Linum usitatissinum L.) and tomato (Lycopersicon esculentum Mill.) on the diversity of soilborne populations of fluorescent pseudomonads. Appl Environ Microbiol 61:1004–1012 · DOI
  42. Lugtenberg BJJ, Dekkers LC, Bloemberg GV (2001) Molecular determinations of rhizosphere colonization by Pseudomonas. Annu Rev Phytopathol 39:461–490 · DOI
  43. Mark GL, 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 USA 102:17454–17459 · DOI
  44. Matilla MA, Espinosa-Urgel M, Rodríguez-Herva JJ, Ramos JL, Ramos-González MI (2007) Genomic analysis reveals the major driving forces of bacterial life in the rhizosphere. Genome Biol 8:R179 · DOI
  45. Mavingui P, Laguerre G, Berge O, Heulin T (1992) Genetic and phenotypic diversity of Bacillus polymyxa in soil and in the wheat rhizosphere. Appl Environ Microbiol 58:1894–1903 · DOI
  46. Mavrodi DV, Blankenfeldt W, Thomashow LS (2006) Phenazine compounds in fluorescent Pseudomonas spp. biosynthesis and regulation. Annu Rev Phytopathol 44:417–445 · DOI
  47. Mazurier S, Lemunier M, Siblot S, Mougel C, Lemanceau P (2004) Distribution and diversity of type III secretion system-like genes in saprophytic and phytopathogenic fluorescent pseudomonads. FEMS Micobiol Ecol 49:455–467 · DOI
  48. Mazurier S, Corberand T, Lemanceau P, Raaijmakers JM (2009) Phenazine antibiotics produced by fluorescent pseudomonads contribute to natural soil suppressiveness to Fusarium wilt. ISME J 3:977–991 · DOI
  49. Mazzola M, Funnell DL, Raaijmakers JM (2004) Wheat cultivar-specific selection of 2,4-diacetylphloroglucinol-producing fluorescent Pseudomonas species from resident soil populations. Microbial Ecol 48:338–348 · DOI
  50. Mazzola M, Cook RJ, Thomashow LS, Weller DM, Pierson LS (1991) Contribution of phenazine antibiotic biosynthesis to the ecological competence of fluorescent pseudomonads in soil habitats. Appl Environ Microbiol 58:2616–2624 · DOI
  51. Meyer J-M (2000) Pyoverdines: pigments, siderophores and potential taxonomic markers of fluorescent Pseudomonas species. Arch Microbiol 174:135–142 · DOI
  52. Meyer J-M, Abdallah MA (1978) The fluorescent pigment of Pseudomonas fluorescens: biosynthesis, purification and physico-chemical properties. J Gen Microbiol 107:319–328 · DOI
  53. Meyer J-M, Stintzi A, Coulanges V, Shivaji S, Voss JA, Taraz K, Budzikiewicz H (1998) Siderotyping of fluorescent pseudomonads: characterization of pyoverdines of Pseudomonas fluorescens and Pseudomonas putida strains from Antartica. Microbiol 144:3119–3126 · DOI
  54. Meyer J-M, Geoffroy VA, Baida N, Gardan L, Izard D, Lemanceau P, Achouak W, Palleroni NJ (2002) Siderophore typing, a powerful tool for the taxonomy of fluorescent and non-fluorescent Pseudomonas. Appl Environ Microbiol 68:2745–2753 · DOI
  55. Meyer J-M, Geoffroy VA, Baysse C, Cornelis P, Barelmann I, Taraz K, Budzikiewicz H (2002) Siderophore-mediated iron uptake in fluorescent Pseudomonas: characterization of the pyoverdine-receptor binding site of three cross-reacting pyoverdines. Arch Biochem Biophys 397:179–183 · DOI
  56. Mirleau P, Philippot L, Corberand T, Lemanceau P (2001) Involvement of nitrate reductase and pyoverdine in competitiveness of Pseudomonas fluorescens strain C7R12 in soil. Appl Environ Microbiol 67:2627–2635 · DOI
  57. Mirleau P, Delorme S, Philippot L, Meyer J-M, Mazurier S, Lemanceau P (2000) Fitness in soil and rhizosphere of Pseudomonas fluorescens strain C7R12 compared with a C7R12 mutant affected in pyoverdine synthesis and uptake. FEMS Microbiol Ecol 34:35–44 · DOI
  58. Olivain C, Alabouvette C, Steinberg C (2004) Production of a mixed inoculum of Fusarium oxysporum Fo47 and Pseudomonas fluorescens C7 to control Fusarium diseases. Biocontrol Sci Tech 14:227–238 · DOI
  59. Picard C, Frascaroli E, Bosco M (2004) Frequency and biodiversity of 2,4-diacetylphloroglucinol-producing rhizobacteria are differentially affected by the genotype of two maize inbred lines and their hybrid. FEMS Microbiol Ecol 49:207–215 · DOI
  60. Price-Whelan A, Dietrich LE, Newman DK (2006) Rethinking ‘secondary’ metabolism: physiological roles for phenazine antibiotics. Nat Chem Biol 2:71–78 · DOI
  61. Raaijmakers JM, Weller DM (1998) Natural plant protection by 2,4-diacetylphloroglucinol-producing Pseudomonas spp. in take-all decline soils. Mol Plant-Microbe Interact 11:144–152 · DOI
  62. Raaijmakers JM, Weller DM (2001) Exploiting genotypic diversity of 2,4-diacetylphloroglucinol-producing Pseudomonas spp.: characterization of superior root-colonizing P. fluorescens strain Q8r1-96. Appl Environ Microbiol 67:2545–2554 · DOI
  63. Raaijmakers JM, Leeman M, Van Oorschot MMP, Van der Sluis L, Schippers B, Bakker PAHM (1995) Dose–response relationships in biological control of Fusarium wilt of radish by Pseudomonas spp. Phytopathology 85:1075–1081 · DOI
  64. Rainey PB (1999) Adaptation of Pseudomonas fluorescens to the plant rhizosphere. Environ Microbiol 1:243–257 · DOI
  65. Ramos-González MI, Campos MJ, Ramos JL (2005) Analysis of Pseudomonas putida KT2440 gene expression in the maize rhizosphere: in vitro expression technology capture and identification of root-activated promoters. J Bacteriol 187:4033–4041 · DOI
  66. Rezzonico F, Zala M, Keel C, Duffy B, Moënne-Loccoz Y, Défago G (2007) Is the ability of biocontrol fluorescent pseudomonads to produce the antifungal metabolite 2,4-diacetylphloroglucinol really synonymous with higher plant protection? New Phytol 173:861–872 · DOI
  67. Robin A, Mazurier S, Meyer J-M, Vansuyt G, Mougel C, Lemanceau P (2007) Diversity of root-associated fluorescent pseudomonads as affected by ferritin overexpression in tobacco. Environ Microbiol 9:1724–1737 · DOI
  68. Sanchez L, Weidmann S, Arnould C, Bernard AR, Gianinazzi S, Gianinazzi-Pearson V (2005) Pseudomonas fluorescens and Glomus mosseae trigger DMI3-dependent activation of genes related to a signal transduction pathway in roots of Medicago truncatula. Plant Physiol 139:1–13 · DOI
  69. Scher FM, Kloepper JW, Singleton C, Zaleski I, Laliberte M (1988) Colonization of soybean roots by Pseudomonas and Serratia species: relationship to bacteria motility, chemotaxis and generation time. Phytopathology 78:1055–1059 · DOI
  70. Schippers B, Scheffer RJ, Lugtenberg BJJ, Weeisbeek PJ (1995) Biocoating of seeds with plant growth-promoting rhizobacteria to improve plant establishment. Outlook Agr 24:179–185 · DOI
  71. Simons M, Permentier HP, de Weger LA, Wijffelman CA, Lugtenberg BJJ (1997) Amino acid synthesis is necessary for tomato root colonization by Pseudomonas fluorescens strain WCS365. Mol Plant-Microbe Interact 10:102–106 · DOI
  72. Simons M, van der Bij AJ, Brand I, de Weger LA, Wijffelman CA, Lugtenberg BJJ (1996) Gnotobiotic system for studying rhizosphere colonization by plant growth-promoting Pseudomonas bacteria. Mol Plant-Microbe Interact 9:600–607 · DOI
  73. Sneath PHA, Sokal RR (1973) Numerical taxonomy. The principles and practice of numerical classification. Freeman & Co., San Francisco
  74. Steinberg C, Gamard P, Faurie G, Lensi R (1989) Survival and potential denitrifying activity of Azospirillum lipoferum and Bradyrhizobium japonicum inoculated into sterilized soil. Biol Fertil Soils 7:101–107 · DOI
  75. Wang Y, Newman DK (2008) Redox reactions of phenazine antibiotics with ferric (hydr)oxides and molecular oxygen. Environ Sci Technol 42:2380–2386 · DOI
  76. Weller DM (1988) Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annu Rev Phytopathol 26:379–407 · DOI
  77. Weller DM, Raaijmakers JM, Gardener BBM, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40:309–348 · DOI
  78. Wood DW, Gong F, Daykin MM, Williams, Pierson LS 3rd (1997) N-acyl-homoserine lactone-mediated regulation of phenazine gene expression by Pseudomonas aureofaciens 30-84 in the wheat rhizosphere. J Bacteriol 179:7663–7670 · DOI

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Authors
Ghirardi, S., Dessaint, F., Mazurier, S., Corberand, T., Raaijmakers, J. M., Meyer, J.-M., Dessaux, Y., & Lemanceau, P.
Affiliations
  • Agroécologie (FR)
  • Wageningen University & Research (NL)
  • Centre National de la Recherche Scientifique (FR)
Corresponding author
Lemanceau, Philippe
ORCID
Venue
Microbial Ecology
Publisher
Springer Science and Business Media LLC
Published
2012-05-11
Volume
64
Issue
3
Pages
725-737
ISSN
  • 0095-3628 (ISSN-L)
  • 1432-184X
DOI
10.1007/s00248-012-0065-3
OpenAlex
W2006646311
Cited by
62
References
0
Citations by year
2026: 4 · 2024: 1 · 2023: 3 · 2022: 4 · 2021: 6 · 2020: 6 · 2019: 4 · 2018: 9 · 2017: 8 · 2016: 4 · 2015: 7 · 2014: 5 · 2013: 1
FWCI
4.75
Type
journal article
Language
en
Open access
Licence
www.springer.com/tdm (tdm)
Locations
  • Microbial Ecology (publishedVersion)
  • PubMed (publishedVersion)
  • Socio-Environmental Systems Modeling (acceptedVersion)
  • HAL (submittedVersion)
  • Data Archiving and Networked Services (DANS) (submittedVersion)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Legume Nitrogen Fixing Symbiosis
Keywords
rhizosphere competence, fluorescent pseudomonads, Pseudomonas, rhizosphere colonization, tomato, siderophores, iron acquisition, denitrification, phenazine, N-acyl homoserine lactones, antibiotic production, soil bacteria, plant growth-promoting bacteria
MeSH terms
Anti-Bacterial Agents, Phenazines, Phenotype, Pseudomonas, Pseudomonas fluorescens, Soil Microbiology, 4-Butyrolactone, Plant Roots, Solanum lycopersicum, Rhizosphere

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