1887

Abstract

Pseudomonads producing the antimicrobial metabolite 2,4-diacetylphloroglucinol (Phl) can control soil-borne phytopathogens, but their impact on other plant-beneficial bacteria remains poorly documented. Here, the effects of synthetic Phl and Phl F113 on phytostimulators were investigated. Most strains were moderately sensitive to Phl. , Phl induced accumulation of carotenoids and poly-β-hydroxybutyrate-like granules, cytoplasmic membrane damage and growth inhibition in Cd. Experiments with F113 and a Phl mutant indicated that Phl production ability contributed to growth inhibition of Cd and Sp245. Under gnotobiotic conditions, each of the three strains, F113 and Cd and Sp245, stimulated wheat growth. Co-inoculation of Sp245 and resulted in the same level of phytostimulation as in single inoculations, whereas it abolished phytostimulation when Cd was used. Phl production ability resulted in lower cell numbers per root system (based on colony counts) and restricted microscale root colonization of neighbouring cells (based on confocal microscopy), regardless of the strain used. Therefore, this work establishes that Phl pseudomonads have the potential to interfere with phytostimulators on roots and with their plant growth promotion capacity.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.043943-0
2011-06-01
2020-07-06
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/6/1694.html?itemId=/content/journal/micro/10.1099/mic.0.043943-0&mimeType=html&fmt=ahah

References

  1. Aßmus B., Schloter M., Kirchhof G., Hutzler P., Hartmann A.. ( 1997;). Improved in situ tracking of rhizosphere bacteria using dual staining with fluorescence-labeled antibodies and rRNA targeted oligonucleotides. Microb Ecol33:32–40 [CrossRef][PubMed]
    [Google Scholar]
  2. Bakker P. A. H. M., Pieterse C. M. J., van Loon L. C.. ( 2007;). Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology97:239–243 [CrossRef][PubMed]
    [Google Scholar]
  3. Bally R., Elmerich C.. ( 2007;). Biocontrol of plant diseases by associative and endophytic nitrogen-fixing bacteria. Associative and Endophytic Nitrogen-fixing Bacteria and Cyanobacterial Associations171–190 Elmerich C., Newton W. E.. Dordrecht, The Netherlands: Kluwer Academic Publishers; [CrossRef]
    [Google Scholar]
  4. Barea J. M., Pozo M. J., Azcón R., Azcón-Aguilar C.. ( 2005;). Microbial co-operation in the rhizosphere. J Exp Bot56:1761–1778 [CrossRef][PubMed]
    [Google Scholar]
  5. Bashan Y., Levanony H., Whitmoyer R. E.. ( 1991;). Root surface colonization of non-cereal crop plants by pleomorphic Azospirillum brasilense Cd. J Gen Microbiol137:187–196[CrossRef]
    [Google Scholar]
  6. Blaha D., Prigent-Combaret C., Mirza M. S., Moënne-Loccoz Y.. ( 2006;). Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminase-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiol Ecol56:455–470 [CrossRef][PubMed]
    [Google Scholar]
  7. Bloemberg G. V., Wijfjes A. H., Lamers G. E., Stuurman N., Lugtenberg B. J.. ( 2000;). Simultaneous imaging of Pseudomonas fluorescens WCS365 populations expressing three different autofluorescent proteins in the rhizosphere: new perspectives for studying microbial communities. Mol Plant Microbe Interact13:1170–1176 [CrossRef][PubMed]
    [Google Scholar]
  8. Brazelton J. N., Pfeufer E. E., Sweat T. A., Gardener B. B., Coenen C.. ( 2008;). 2,4-diacetylphloroglucinol alters plant root development. Mol Plant Microbe Interact21:1349–1358 [CrossRef][PubMed]
    [Google Scholar]
  9. Chilton M. D., Currier T. C., Farrand S. K., Bendich A. J., Gordon M. P., Nester E. W.. ( 1974;). Agrobacterium tumefaciens DNA and PS8 bacteriophage DNA not detected in crown gall tumors. Proc Natl Acad Sci U S A71:3672–3676 [CrossRef][PubMed]
    [Google Scholar]
  10. Combes-Meynet E., Pothier J. F., Moënne-Loccoz Y., Prigent-Combaret C.. ( 2011;). The Pseudomonas secondary metabolite 2,4-diacetylphloroglucinol is a signal inducing rhizoplane expression of Azospirillum genes involved in plant-growth promotion. Mol Plant Microbe Interact24:271–284 [CrossRef][PubMed]
    [Google Scholar]
  11. Costacurta A., Vanderleyden J.. ( 1995;). Synthesis of phytohormones by plant-associated bacteria. Crit Rev Microbiol21:1–18 [CrossRef][PubMed]
    [Google Scholar]
  12. Couillerot O., Prigent-Combaret C., Caballero-Mellado J., Moënne-Loccoz Y.. ( 2009;). Pseudomonas fluorescens and closely-related fluorescent pseudomonads as biocontrol agents of soil-borne phytopathogens. Lett Appl Microbiol48:505–512 [CrossRef][PubMed]
    [Google Scholar]
  13. Creus C. M., Graziano M., Casanovas E. M., Pereyra M. A., Simontacchi M., Puntarulo S., Barassi C. A., Lamattina L.. ( 2005;). Nitric oxide is involved in the Azospirillum brasilense-induced lateral root formation in tomato. Planta221:297–303 [CrossRef][PubMed]
    [Google Scholar]
  14. Cronin D., Moënne-Loccoz Y., Fenton A., Dunne C., Dowling D. N., O’Gara F.. ( 1997;a). Ecological interaction of a biocontrol Pseudomonas fluorescens strain producing 2,4-diacetylphloroglucinol with the soft rot potato pathogen Erwinia carotovora subsp. atroseptica . FEMS Microbiol Ecol23:95–106 [CrossRef]
    [Google Scholar]
  15. Cronin D., Moënne-Loccoz Y., Fenton A., Dunne C., Dowling D. N., O’Gara F.. ( 1997;b). Role of 2,4-diacetylphloroglucinol in the interactions of the biocontrol pseudomonad strain F113 with the potato cyst nematode Globodera rostochiensis . Appl Environ Microbiol63:1357–1361[PubMed]
    [Google Scholar]
  16. de Souza J. T., Arnould C., Deulvot C., Lemanceau P., Gianinazzi-Pearson V., Raaijmakers J. M.. ( 2003;). Effect of 2,4-diacetylphloroglucinol on Pythium: cellular responses and variation in sensitivity among propagules and species. Phytopathology93:966–975 [CrossRef][PubMed]
    [Google Scholar]
  17. Dobbelaere S., Croonenborghs A., Thys A., Vande Broek A., Vanderleyden J.. ( 1999;). Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil212:153–164 [CrossRef]
    [Google Scholar]
  18. Dobbelaere S., Croonenborghs A., Thys A., Ptacek D., Vanderleyden J., Dutto P., Labandera-Gonzalez C., Caballero-Mellado J., Aguirre J. F. et al. ( 2001;). Responses of agronomically important crops to inoculation with Azospirillum . Aust J Plant Physiol28:871–879
    [Google Scholar]
  19. Dobbelaere S., Vanderleyden J., Okon Y.. ( 2003;). Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci22:107–149 [CrossRef]
    [Google Scholar]
  20. Duffy B. K., Défago G.. ( 1999;). Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. Appl Environ Microbiol65:2429–2438[PubMed]
    [Google Scholar]
  21. Elbeltagy A., Nishioka K., Sato T., Suzuki H., Ye B., Hamada T., Isawa T., Mitsui H., Minamisawa K.. ( 2001;). Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. isolated from wild rice species. Appl Environ Microbiol67:5285–5293 [CrossRef][PubMed]
    [Google Scholar]
  22. Eskew D. L., Focht D. D., Ting I. P.. ( 1977;). Nitrogen fixation, denitrification, and pleomorphic growth in a highly pigmented Spirillum lipoferum . Appl Environ Microbiol34:582–585[PubMed]
    [Google Scholar]
  23. Fenton A. M., Stephens P. M., Crowley J., O’Callaghan M., O’Gara F.. ( 1992;). Exploitation of gene(s) involved in 2,4-diacetylphloroglucinol biosynthesis to confer a new biocontrol capability to a Pseudomonas strain. Appl Environ Microbiol58:3873–3878[PubMed]
    [Google Scholar]
  24. Fuentes-Ramirez L., Caballero-Mellado J.. ( 2006;). Bacterial biofertilizers. PGPR: Biocontrol and Biofertilization143–172 Siddiqui Z. A.. Heidelberg, Germany: Springer; [CrossRef]
    [Google Scholar]
  25. Girlanda M., Perotto S., Moënne-Loccoz Y., Bergero R., Lazzari A., Défago G., Bonfante P., Luppi A. M.. ( 2001;). Impact of biocontrol Pseudomonas fluorescens CHA0 and a genetically modified derivative on the diversity of culturable fungi in the cucumber rhizosphere. Appl Environ Microbiol67:1851–1864 [CrossRef][PubMed]
    [Google Scholar]
  26. Gleeson O., O’Gara F., Morrissey J. P.. ( 2010;). The Pseudomonas fluorescens secondary metabolite 2,4 diacetylphloroglucinol impairs mitochondrial function in Saccharomyces cerevisiae . Antonie van Leeuwenhoek97:261–273 [CrossRef][PubMed]
    [Google Scholar]
  27. Haas D., Défago G.. ( 2005;). Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol3:307–319 [CrossRef][PubMed]
    [Google Scholar]
  28. Haas D., Keel C.. ( 2003;). Regulation of antibiotic production in root-colonizing Pseudomonas spp. and relevance for biological control of plant disease. Annu Rev Phytopathol41:117–153 [CrossRef][PubMed]
    [Google Scholar]
  29. Hartmann A., Hurek T.. ( 1988;). Effect of carotenoid overproduction on oxygen tolerance of nitrogen fixation in Azospirillum brasilense Sp7. J Gen Microbiol134:2449–2455
    [Google Scholar]
  30. Hontzeas N., Zoidakis J., Glick B. R., Abu-Omar M. M.. ( 2004;). Expression and characterization of 1-aminocyclopropane-1-carboxylate deaminase from the rhizobacterium Pseudomonas putida UW4: a key enzyme in bacterial plant growth promotion. Biochim Biophys Acta1703:11–19[PubMed][CrossRef]
    [Google Scholar]
  31. Howell C. R., Stipanovic R. D.. ( 1979;). Control of Rhizoctonia solani on cotton seedlings with Pseudomonas fluorescens and with an antibiotic produced by the bacterium. Phytopathology69:480–482 [CrossRef]
    [Google Scholar]
  32. Iavicoli A., Boutet E., Buchala A., Métraux J.-P.. ( 2003;). Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Mol Plant Microbe Interact16:851–858 [CrossRef][PubMed]
    [Google Scholar]
  33. Johansen J. E., Binnerup S. J., Lejbølle K. B., Mascher F., Sørensen J., Keel C.. ( 2002;). Impact of biocontrol strain Pseudomonas fluorescens CHA0 on rhizosphere bacteria isolated from barley (Hordeum vulgare L.) with special reference to Cytophaga-like bacteria. J Appl Microbiol93:1065–1074 [CrossRef][PubMed]
    [Google Scholar]
  34. Kabir M., Faure D., Heulin T., Achouak W., Bally R.. ( 1996;). Azospirillum populations in soils infested by a parasitic weed (Striga) under Sorghum cultivation in Mali, West Africa. Eur J Soil Biol32:157–163
    [Google Scholar]
  35. Kadouri D., Burdman S., Jurkevitch E., Okon Y.. ( 2002;). Identification and isolation of genes involved in poly(β-hydroxybutyrate) biosynthesis in Azospirillum brasilense and characterization of a phbC mutant. Appl Environ Microbiol68:2943–2949 [CrossRef][PubMed]
    [Google Scholar]
  36. Kadouri D., Jurkevitch E., Okon Y.. ( 2003;). Involvement of the reserve material poly-β-hydroxybutyrate in Azospirillum brasilense stress endurance and root colonization. Appl Environ Microbiol69:3244–3250 [CrossRef][PubMed]
    [Google Scholar]
  37. Keel C., Schnider U., Maurhofer M., Voisard C., Laville J., Burger U., Wirthner P., Haas D., Défago G.. ( 1992;). Suppression of root diseases by Pseudomonas fluorescens CHA0: Importance of the bacterial secondary metabolite 2,4-diacetylphloroglucinol. Mol Plant Microbe Interact5:4–13 [CrossRef]
    [Google Scholar]
  38. King E. O., Ward M. K., Raney D. E.. ( 1954;). Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med44:301–307[PubMed]
    [Google Scholar]
  39. Kyselková M., Kopecký J., Frapolli M., Défago G., Ságová-Marecková M., Grundmann G. L., Moënne-Loccoz Y.. ( 2009;). Comparison of rhizobacterial community composition in soil suppressive or conducive to tobacco black root rot disease. ISME J3:1127–1138 [CrossRef][PubMed]
    [Google Scholar]
  40. Lemanceau P., Bakker P. A. H. M., De Kogel W. J., Alabouvette C., Schippers B.. ( 1992;). Effect of pseudobactin 358 production by Pseudomonas putida WCS358 on suppression of fusarium wilt of carnations by nonpathogenic Fusarium oxysporum Fo47. Appl Environ Microbiol58:2978–2982[PubMed]
    [Google Scholar]
  41. Maurhofer M., Baehler E., Notz R., Martinez V., Keel C.. ( 2004;). Cross talk between 2,4-diacetylphloroglucinol-producing biocontrol pseudomonads on wheat roots. Appl Environ Microbiol70:1990–1998 [CrossRef][PubMed]
    [Google Scholar]
  42. Michiels K., Vanderleyden J., Van Gool A.. ( 1989;). Azospirillum-plant root associations: a review. Biol Fertil Soils8:356–368 [CrossRef]
    [Google Scholar]
  43. Mirza M. S., Mehnaz S., Normand P., Prigent-Combaret C., Moënne-Loccoz Y., Bally R., Malik K. A.. ( 2006;). Molecular characterization and PCR detection of a nitrogen-fixing Pseudomonas strain promoting rice growth. Biol Fertil Soils43:163–170 [CrossRef]
    [Google Scholar]
  44. Moënne-Loccoz Y., Tichy H. V., O’Donnell A., Simon R., O’Gara F.. ( 2001;). Impact of 2,4-diacetylphloroglucinol-producing biocontrol strain Pseudomonas fluorescens F113 on intraspecific diversity of resident culturable fluorescent pseudomonads associated with the roots of field-grown sugar beet seedlings. Appl Environ Microbiol67:3418–3425 [CrossRef][PubMed]
    [Google Scholar]
  45. Natsch A., Keel C., Hebecker N., Laasik E., Défago G.. ( 1998;). Impact of Pseudomonas fluorescens strain CHA0 and a derivative with improved biocontrol activity on the culturable resident bacterial community on cucumber roots. FEMS Microbiol Ecol27:365–380 [CrossRef]
    [Google Scholar]
  46. Nelson L. M., Knowles R.. ( 1978;). Effect of oxygen and nitrate on nitrogen fixation and denitrification by Azospirillum brasilense grown in continuous culture. Can J Microbiol24:1395–1403 [CrossRef][PubMed]
    [Google Scholar]
  47. Nur I., Steinitz Y. L., Okon Y., Henis Y.. ( 1981;). Carotenoid composition and function in nitrogen-fixing bacteria of the genus Azospirillum . J Gen Microbiol122:27–32
    [Google Scholar]
  48. Penot I., Bergès N., Guinguené C., Fages J.. ( 1992;). Characterization of Azospirillum associated with maize (Zea mays) in France using biochemical tests and plasmid profiles. Can J Microbiol38:798–803 [CrossRef]
    [Google Scholar]
  49. Phillips D. A., Fox T. C., King M. D., Bhuvaneswari T. V., Teuber L. R.. ( 2004;). Microbial products trigger amino acid exudation from plant roots. Plant Physiol136:2887–2894 [CrossRef][PubMed]
    [Google Scholar]
  50. Picard C., Bosco M.. ( 2005;). Maize heterosis affects the structure and dynamics of indigenous rhizospheric auxins-producing Pseudomonas populations. FEMS Microbiol Ecol53:349–357 [CrossRef][PubMed]
    [Google Scholar]
  51. Pothier J. F., Wisniewski-Dyé F., Weiss-Gayet M., Moënne-Loccoz Y., Prigent-Combaret C.. ( 2007;). Promoter-trap identification of wheat seed extract-induced genes in the plant-growth-promoting rhizobacterium Azospirillum brasilense Sp245. Microbiology153:3608–3622 [CrossRef][PubMed]
    [Google Scholar]
  52. Raaijmakers J. M., Vlami M., de Souza J. T.. ( 2002;). Antibiotic production by bacterial biocontrol agents. Antonie van Leeuwenhoek81:537–547 [CrossRef][PubMed]
    [Google Scholar]
  53. Raaijmakers J. M., Paulitz T. C., Steinberg C., Alabouvette C., Moënne-Loccoz Y.. ( 2009;). The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil321:341–361 [CrossRef]
    [Google Scholar]
  54. Reid J. B., Renquist A. R.. ( 1997;). Enhanced root production as a feed-forward response to soil water deficit in field-grown tomatoes. Aust J Plant Physiol24:685–692 [CrossRef]
    [Google Scholar]
  55. 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 Phytol173:861–872 [CrossRef][PubMed]
    [Google Scholar]
  56. Richardson A. E., Barea J.-M., McNeill A. M., Prigent-Combaret C.. ( 2009;). Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil321:305–339 [CrossRef]
    [Google Scholar]
  57. Rinaudo G.. ( 1982;) Fixation hétérotrophe de l'azote dans la rhizosphère du riz.
  58. Sambrook J., Fritsch E. F., Maniatis T.. ( 1989;). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory;
    [Google Scholar]
  59. Sanguin H., Sarniguet A., Gazengel K., Moënne-Loccoz Y., Grundmann G. L.. ( 2009;). Rhizosphere bacterial communities associated with disease suppressiveness stages of take-all decline in wheat monoculture. New Phytol184:694–707 [CrossRef][PubMed]
    [Google Scholar]
  60. Scher F. M., Baker R.. ( 1982;). Effect of Pseudomonas putida and a synthetic iron chelator on induction of soil suppressiveness to Fusarium wilt pathogens. Phytopathology72:1567–1573 [CrossRef]
    [Google Scholar]
  61. Schloter M., Hartmann A.. ( 1998;). Endophytic and surface colonization of wheat roots (Triticum aestivum) by different Azospirillum brasilense strains studied with strain-specific monoclonal antibodies. Symbiosis25:159–179
    [Google Scholar]
  62. Schouten A., Van den Berg G., Edel-Hermann V., Steinberg C., Gautheron N., Alabouvette C., De Vos C. H., Lemanceau P., Raaijmakers J. M.. ( 2004;). Defense responses of Fusarium oxysporum to 2,4-diacetylphloroglucinol, a broad-spectrum antibiotic produced by Pseudomonas fluorescens . Mol Plant Microbe Interact17:1201–1211 [CrossRef][PubMed]
    [Google Scholar]
  63. Schouten A., Maksimova O., Cuesta-Arenas Y., van den Berg G., Raaijmakers J. M.. ( 2008;). Involvement of the ABC transporter BcAtrB and the laccase BcLCC2 in defence of Botrytis cinerea against the broad-spectrum antibiotic 2,4-diacetylphloroglucinol. Environ Microbiol10:1145–1157 [CrossRef][PubMed]
    [Google Scholar]
  64. Shanahan P., O’sullivan D. J., Simpson P., Glennon J. D., O’Gara F.. ( 1992;). Isolation of 2,4-diacetylphloroglucinol from a fluorescent pseudomonad and investigation of physiological parameters influencing its production. Appl Environ Microbiol58:353–358[PubMed]
    [Google Scholar]
  65. Tal S., Okon Y.. ( 1985;). Production of the reserve material poly-β-hydroxybutyrate and its function in Azospirillum brasilense Cd. Can J Microbiol31:608–613 [CrossRef]
    [Google Scholar]
  66. Tarrand J. J., Krieg N. R., Döbereiner J.. ( 1978;). A taxonomic study of the Spirillum lipoferum group, with descriptions of a new genus, Azospirillum gen. nov. and two species, Azospirillum lipoferum (Beijerinck) comb. nov. and Azospirillum brasilense sp. nov. Can J Microbiol24:967–980 [CrossRef][PubMed]
    [Google Scholar]
  67. Thirunavukkarasu N., Mishra M. N., Spaepen S., Vanderleyden J., Gross C. A., Tripathi A. K.. ( 2008;). An extra-cytoplasmic function sigma factor and anti-sigma factor control carotenoid biosynthesis in Azospirillum brasilense . Microbiology154:2096–2105 [CrossRef][PubMed]
    [Google Scholar]
  68. Vincent M. N., Harrison L. A., Brackin J. M., Kovacevich P. A., Mukerji P., Weller D. M., Pierson E. A.. ( 1991;). Genetic analysis of the antifungal activity of a soilborne Pseudomonas aureofaciens strain. Appl Environ Microbiol57:2928–2934[PubMed]
    [Google Scholar]
  69. Walsh U. F., Moënne-Loccoz Y., Tichy H.-V., Gardner A., Corkery D. M., Lorkhe S., O’Gara F.. ( 2003;). Residual impact of the biocontrol inoculant Pseudomonas fluorescens F113 on the resident population of rhizobia nodulating a red clover rotation crop. Microb Ecol45:145–155 [CrossRef][PubMed]
    [Google Scholar]
  70. Weller D. M., Raaijmakers J. M., Gardener B. B. M., Thomashow L. S.. ( 2002;). Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol40:309–348 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.043943-0
Loading
/content/journal/micro/10.1099/mic.0.043943-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error