Monitoring of the relation between 2,4-diacetylphloroglucinol-producing Pseudomonas and Thielaviopsis basicola populations by real-time PCR in tobacco black root-rot suppressive and conducive soils

Soil Biology and Biochemistry

Volumn 57, Issue , 2013, Pages 144-155

  Almario, Juliana ^a,b,c   Moënne Loccoz, Yvan ^a,b,c   Muller, Daniel ^a,b,c  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITÉ LYON 1   (France)

^c University of Lyon   (France)

Author keywords

2,4 Diacetylphloroglucinol; Biocontrol; Morens; PhlD; Pseudomonas; Rhizosphere; Suppressive soil; Thielaviopsis basicola

Indexed keywords

2 ,4-DIACETYLPHLOROGLUCINOL; MORENS; PHLD; PSEUDOMONAS; RHIZOSPHERE; THIELAVIOPSIS BASICOLA;

BACTERIA; BIOCONTROL; CELL CULTURE; FUNCTIONAL GROUPS; POLYMERASE CHAIN REACTION; TOBACCO;

SOILS;

FUNCTIONAL GROUP; PATHOGEN; POPULATION DYNAMICS; REAL TIME; RHIZOSPHERE; SOIL ANALYSIS; SOIL ECOSYSTEM; TOBACCO;

NICOTIANA TABACUM; PSEUDOMONAS; PSEUDOMONAS FLUORESCENS GROUP; THIELAVIOPSIS BASICOLA; VALERIANA EDULIS;

EID: 84869871635     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2012.09.003     Document Type: Article

References (80)

1. Anzai Y., Kim H., Park J.Y., Wakabayashi H., Oyaizu H. Phylogenetic affiliation of the pseudomonads based on 16S rRNA sequence. International Journal of Systematic and Evolutionary Microbiology 2000, 50:1563-1589.
2. Becker J., Eisenhauer N., Scheu S., Jousset A. Increasing antagonistic interactions cause bacterial communities to collapse at high diversity. Ecology Letters 2012, 15:468-474.
3. Bergsma-Vlami M., Prins M.E., Raaijmakers J.M. Influence of plant species on population dynamics, genotypic diversity and antibiotic production in the rhizosphere by indigenous Pseudomonas spp. FEMS Microbiology Ecology 2005, 52:59-69.
4. Box G.E.P., Cox D.R. An analysis of transformation. Journal of the Royal Statistical Society: Series B 1964, 26:211-252.
5. Brazelton J.N., Pfeufer E.E., Sweat T.A., McSpadden Gardener B.B., Coenen C. 2,4-Diacetylphloroglucinol alters plant root development. Molecular Plant-Microbe Interactions 2008, 21:1349-1358.
6. Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M.W., Shipley G.L., Vandesompele J., Wittwer C.T. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 2009, 55:611-622.
7. Carroll H., Moënne-Loccoz Y., Dowling D.N., O'Gara F. Mutational disruption of the biosynthesis genes coding for the antifungal metabolite 2,4-diacetylphloroglucinol does not influence the ecological fitness of Pseudomonas fluorescens F113 in the rhizosphere of sugarbeets. Applied and Environmental Microbiology 1995, 61:3002-3007.
8. Chapon A., Guillerm A.Y., Delalande L., Lebreton L., Sarniguet A. Dominant colonisation of wheat roots by Pseudomonas fluorescens Pf29A and selection of the indigenous microflora in the presence of the take-all fungus. European Journal of Plant Pathology 2002, 108:449-459.
9. Chen X.P., Zhu Y.G., Xia Y., Shen J.P., He J.Z. Ammonia-oxidizing archaea: important players in paddy rhizosphere soil?. Environmental Microbiology 2008, 10:1978-1987.
10. Combes-Meynet E., Pothier J.F., Moënne-Loccoz Y., Prigent-Combaret C. The Pseudomonas secondary metabolite 2,4-diacetylphloroglucinol is a signal inducing rhizoplane expression of Azospirillum genes involved in plant-growth promotion. Molecular Plant-Microbe Interactions 2011, 24:271-284.
11. Couillerot O., Prigent-Combaret C., Caballero-Mellado J., Moënne-Loccoz Y. Pseudomonas fluorescens and closely-related fluorescent pseudomonads as biocontrol agents of soil-borne phytopathogens. Letters in Applied Microbiology 2009, 48:505-512.
12. Couillerot O., Bouffaud M.L., Baudoin E., Muller D., Caballero-Mellado J., Moënne-Loccoz Y. Development of a real-time PCR method to quantify the PGPR strain Azospirillum lipoferum CRT1 on maize seedlings. Soil Biology & Biochemistry 2010, 42:2298-2305.
13. De La Fuente L., Mavrodi D.V., Landa B.B., Thomashow L.S., Weller D.M. phlD-based genetic diversity and detection of genotypes of 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens. FEMS Microbiology Ecology 2006, 56:64-78.
14. De Mendiburu F. Agricolae: Statistical Procedures for Agricultural Research, R Package Version 1.0-9 2007, http://tarwi.lamolina.edu.pe/%7Efmendiburu.
15. Duffy B., Schouten A., Raaijmakers J.M. Pathogen self-defense: mechanisms to counteract microbial antagonism. Annual Review of Phytopathology 2003, 41:501-538.
16. Fedi S., Tola E., Moënne-Loccoz Y., Dowling D.N., Smith L.M., O'Gara F. Evidence for signaling between the phytopathogenic fungus Pythium ultimum and Pseudomonas fluorescens F113: P. ultimum represses the expression of genes in P. fluorescens F113, resulting in altered ecological fitness. Applied and Environmental Microbiology 1997, 63:4261-4266.
17. Fenton A.M., Stephens P.M., Crowley J., O'Callaghan M., O'Gara F. Exploitation of gene(s) involved in 2,4-diacetylphloroglucinol biosynthesis to confer a new biocontrol capability to a Pseudomonas strain. Applied and Environmental Microbiology 1992, 58:3873-3878.
18. Fox J., Weisberg S. An R Companion to Applied Regression 2011, SAGE Publications Inc., Thousand Oaks (CA). second ed.
19. Frapolli M., Défago G., Moënne-Loccoz Y. Multilocus sequence analysis of biocontrol fluorescent Pseudomonas spp. producing the antifungal compound 2,4-diacetylphloroglucinol. Environmental Microbiology 2007, 9:1939-1955.
20. Frapolli M., Moënne-Loccoz Y., Meyer J., Défago G. A new DGGE protocol targeting 2,4-diacetylphloroglucinol biosynthetic gene phlD from phylogenetically contrasted biocontrol pseudomonads for assessment of disease-suppressive soils. FEMS Microbiology Ecology 2008, 64:468-481.
21. Frapolli M., Défago G., Moënne-Loccoz Y. Denaturing gradient gel electrophoretic analysis of dominant 2,4-diacetylphloroglucinol biosynthetic phlD alleles in fluorescent Pseudomonas from soils suppressive or conducive to black root rot of tobacco. Soil Biology & Biochemistry 2010, 42:649-656.
22. Gasser R., Défago G. Case of the certain soils which are suppressive to the black root-rot of tobacco caused by Thielaviopsis basicola. Botanica Helvetica 1981, 91:75-80.
23. Griffiths R.I., Whiteley A.S., O'Donnell A.G., Bailey M.J. Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Applied and Environmental Microbiology 2000, 66:5488-5491.
24. Haas D., Défago G. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nature Reviews Microbiology 2005, 3:307-319.
25. Haas D., Keel C. Regulation of antibiotic production in root-colonizing Pseudomonas spp. and relevance for biological control of plant disease. Annual Review of Phytopathology 2003, 41:117-153.
26. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 1999, 41:95-98.
27. Hogg A.C., Johnston R.H., Dyer A.T. Applying real-time quantitative PCR to Fusarium crown rot of wheat. Plant Disease 2007, 91:1021-1028.
28. Hood M.E., Shew H.D. Reassessment of the role of saprophytic activity in the ecology of Thielaviopsis basicola. Phytopathology 1997, 87:1214-1219.
29. Huang J., Kang Z. Detection of Thielaviopsis basicola in soil with real-time quantitative PCR assays. Microbiological Research 2010, 165:411-417.
30. Iavicoli A., Boutet E., Buchala A., Métraux J.P. Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Molecular Plant-Microbe Interactions 2003, 16:851-858.
31. Ippolito A., Schena L., Nigro F., Ligorio V.S., Yaseen T. Real-time detection of Phytophthora nicotianae and P. citrophthora in citrus roots and soil. European Journal of Plant Pathology 2004, 110:833-843.
32. Jamali F., Sharifi-Tehrani A., Lutz M., Maurhofer M. Influence of host plant genotype, presence of a pathogen, and coinoculation with Pseudomonas fluorescens strains on the rhizosphere expression of hydrogen cyanide- and 2,4-diacetylphloroglucinol biosynthetic genes in P. fluorescens biocontrol strain CHA0. Microbial Ecology 2009, 57:267-275.
33. Jensen D.E., Kelly R.C., Vonhippel P.H. DNA " melting" proteins. II. Effects of bacteriophage T4 gene 32-protein binding on the conformation and stability of nucleic acid structures. Journal of Biological Chemistry 1976, 251:7215-7228.
34. Johnson K.B., Dileone J.A. Effect of antibiosis on antagonist dose-plant disease response relationships for the biological control of crown gall of tomato and cherry. Phytopathology 1999, 89:974-980.
35. Keel C., Schnider U., Maurhofer M., Voisard C., Laville J., Burger U., Wirthner P., Haas D., Défago G. Suppression of root diseases by Pseudomonas fluorescens CHA0: importance of the bacterial secondary metabolite 2,4-diacetylphloroglucinol. Molecular Plant-Microbe Interactions 1992, 5:4-13.
36. Keel C., Weller D.M., Natsch A., Défago G., Cook R.J., Thomashow L.S. Conservation of the 2,4-diacetylphloroglucinol biosynthesis locus among fluorescent Pseudomonas strains from diverse geographic locations. Applied and Environmental Microbiology 1996, 62:552-563.
37. Kimura M. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 1980, 16:111-120.
38. King E.O., Ward M.K., Raney D.E. Two simple media for the demonstration of pyocyanin and fluorescein. Journal of Laboratory and Clinical Medicine 1954, 44:301-307.
39. Kloepper J.W., Beauchamp C.J. A review of issues related to measuring colonization of plant roots by bacteria. Canadian Journal of Microbiology 1992, 38:1219-1232.
40. Kyselková M., Moënne-Loccoz Y. Pseudomonas and other microbes in disease-suppressive soils. Organic Fertilisation, Soil Quality and Human Health - Sustainable Agriculture Reviews 2012, vol. 9:93-140. Springer, Dordrecht, Netherlands.
41. Kyselková M., Kopecký J., Frapolli M., Défago G., Ságová-Marečková M., Grundmann G.L., Moënne-Loccoz Y. Comparison of rhizobacterial community composition in soil suppressive or conducive to tobacco black root rot disease. The ISME Journal 2009, 3:1127-1138.
42. Landa B.B., Mavrodi O.V., Raaijmakers J.M., McSpadden Gardener B.B., Thomashow L.S., Weller D.M. Differential ability of genotypes of 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens strains to colonize the roots of pea plants. Applied and Environmental Microbiology 2002, 68:3226-3237.
43. Larkin R.P., Fravel D.R. Mechanisms of action and dose-response relationships governing biological control of Fusarium wilt of tomato by nonpathogenic Fusarium spp. Phytopathology 1999, 89:1152-1161.
44. Lebreton L., Gosme M., Lucas P., Guillerm-Erckelboudt A.Y., Sarniguet A. Linear relationship between Gaeumannomyces graminis var. tritici (Ggt) genotypic frequencies and disease severity on wheat roots in the field. Environmental Microbiology 2007, 9:492-499.
45. Le Roux X., Poly F., Currey P., Commeaux C., Hai B., Nicol G.W., Prosser J.I., Schloter M., Attard E., Klumpp K. Effects of aboveground grazing on coupling among nitrifier activity, abundance and community structure. The ISME Journal 2008, 2:221-232.
46. Lievens B., Brouwer M., Vanachter A.C.R.C., Cammue B.P.A., Thomma B.P.H.J. Real-time PCR for detection and quantification of fungal and oomycete tomato pathogens in plant and soil samples. Plant Science 2006, 171:155-165.
47. Marschner P., Crowley D.E. Physiological activity of a bioluminescent Pseudomonas fluorescens (strain 2-79) in the rhizosphere of mycorrhizal and non-mycorrhizal pepper (Capsicum annuum L.). Soil Biology & Biochemistry 1996, 28:869-876.
48. Mamedov T.G., Pienaar E., Whitney S.E., TerMaat J.R., Carvill G., Goliath R., Subramanian A., Viljoen H.J. A fundamental study of the PCR amplification of GC-rich DNA templates. Computational Biology and Chemistry 2008, 32:452-457.
49. Maurhofer M., Hase C., Meuwly P., Métraux J.P., Défago G. Induction of systemic resistance of tobacco to tobacco necrosis virus by the root-colonizing Pseudomonas fluorescens strain CHA0: influence of the gacA gene and of pyoverdine production. Phytopathology 1994, 84:139-146.
50. Mavrodi O.V., Mavrodi D.V., Thomashow L.S., Weller D.M. Quantification of 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens strains in the plant rhizosphere by real-time PCR. Applied and Environmental Microbiology 2007, 73:5531-5538.
51. McSpadden Gardener B.B., Weller D.M. Changes in populations of rhizosphere bacteria associated with take-all disease of wheat. Applied and Environmental Microbiology 2001, 67:4414-4425.
52. McSpadden Gardener B.B., Mavrodi D.V., Thomashow L.S., Weller D.M. A rapid polymerase chain reaction-based assay characterizing rhizosphere populations of 2,4-diacetylphloroglucinol-producing bacteria. Phytopathology 2001, 91:44-54.
53. Meyer J.B., Lutz M.P., Frapolli M., Péchy-Tarr M., Rochat L., Keel C., Défago G., Maurhofer M. Interplay between wheat cultivars, biocontrol pseudomonads, and soil. Applied and Environmental Microbiology 2010, 76:6196-6204.
54. Moynihan J.A., Morrissey J.P., Coppoolse E.R., Stiekema W.J., O'Gara F., Boyd E.F. Evolutionary history of the phl gene cluster in the plant-associated bacterium Pseudomonas fluorescens. Applied and Environmental Microbiology 2009, 75:2122-2131.
55. Notz R., Maurhofer M., Schnider-Keel U., Duffy B., Haas D., Défago G. Biotic factors affecting expression of the 2,4-diacetylphloroglucinol biosynthesis gene phlA in Pseudomonas fluorescens biocontrol strain CHA0 in the rhizosphere. Phytopathology 2001, 91:873-881.
56. Paulsen I.T., Press C.M., Ravel J., Kobayashi D.Y., Myers G.S., Mavrodi D.V., DeBoy R.T., Seshadri R., Ren Q., Madupu R., Dodson R.J., Durkin A.S., Brinkac L.M., Daugherty S.C., Sullivan S.A., Rosovitz M.J., Gwinn M.L., Zhou L., Schneider D.J., Cartinhour S.W., Nelson W.C., Weidman J., Watkins K., Tran K., Khouri H., Pierson E.A., Pierson L.S., Thomashow L.S., Loper J.E. Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5. Nature Biotechnology 2005, 23:873-878.
57. Phillips D.A., Fox T.C., King M.D., Bhuvaneswari T.V., Teuber L.R. Microbial products trigger amino acid exudation from plant roots. Plant Physiology 2004, 136:2887-2894.
58. Picard C., Bosco M. Heterozygosis drives maize hybrids to select elite 2,4-diacethylphloroglucinol-producing Pseudomonas strains among resident soil populations. FEMS Microbiology Ecology 2006, 58:193-204.
59. Raaijmakers J.M., Weller D.M. Natural plant protection by 2,4-diacetylphloroglucinol-producing Pseudomonas spp. in take-all decline soils. Molecular Plant-Microbe Interactions 1998, 11:144-152.
60. Raaijmakers J.M., Paulitz T.C., Steinberg C., Alabouvette C., Moënne-Loccoz Y. The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant and Soil 2009, 321:341-361.
61. Ramette A., Moënne-Loccoz Y., Défago G. Prevalence of fluorescent pseudomonads producing antifungal phloroglucinols and/or hydrogen cyanide in soils naturally suppressive or conducive to tobacco black root rot. FEMS Microbiology Ecology 2003, 44:35-43.
62. Ramette A., Moënne-Loccoz Y., Défago G. Genetic diversity and biocontrol potential of fluorescent pseudomonads producing phloroglucinols and hydrogen cyanide from Swiss soils naturally suppressive or conducive to Thielaviopsis basicola-mediated black root rot of tobacco. FEMS Microbiology Ecology 2006, 55:369-381.
63. Ramette A., Frapolli M., Fischer-Le Saux M., Gruffaz C., Meyer J.M., Défago G., Sutra L., Moënne-Loccoz Y. Pseudomonas protegens sp nov., widespread plant-protecting bacteria producing the biocontrol compounds 2,4-diacetylphloroglucinol and pyoluteorin. Systematic and Applied Microbiology 2011, 34:180-188.
64. Rezzonico F., Moënne-Loccoz Y., Défago G. Effect of stress on the ability of a phlA-based quantitative competitive PCR assay to monitor biocontrol strain Pseudomonas fluorescens CHA0. Applied and Environmental Microbiology 2003, 69:686-690.
65. Rotenberg D., Joshi R., Benitez M.S., Gutierrez Chapin L., Camp A., Zumpetta C., Osborne A., Dick W.A., McSpadden Gardener B.B. Farm management effects on rhizosphere colonization by native populations of 2,4-diacetylphloroglucinol-producing Pseudomonas spp. and their contributions to crop health. Phytopathology 2007, 97:756-766.
66. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 1987, 4:406-425.
67. Sørensen J., Jensen L.E., Nybroe O. Soil and rhizosphere as habitats for Pseudomonas inoculants: new knowledge on distribution, activity and physiological state derived from micro-scale and single-cell studies. Plant and Soil 2001, 232:97-108.
68. Stutz E.W., Défago G., Kern H. Naturally-occurring fluorescent Pseudomonas involved in suppression of black root-rot of tobacco. Phytopathology 1986, 76:181-185.
69. Stutz E.W., Kahr G., Défago G. Clays involved in suppression of tobacco black root-rot by a strain of Pseudomonas fluorescens. Soil Biology & Biochemistry 1989, 21:361-366.
70. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 2007, 24:1596-1599.
71. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 1997, 25:4876-4882.
72. Troxler J., Berling C.H., MoënneLoccoz Y., Keel C., Défago G. Interactions between the biocontrol agent Pseudomonas fluorescens CHA0 and Thielaviopsis basicola in tobacco roots observed by immunofluorescence microscopy. Plant Pathology 1997, 46:62-71.
73. Troxler J., Svercel M., Natsch A., Zala M., Keel C., Moënne-Loccoz Y., Défago G. Persistence of a biocontrol Pseudomonas inoculant as high populations of culturable and non-culturable cells in 200-cm-deep soil profiles. Soil Biology & Biochemistry 2012, 44:122-129.
74. Vincent M.N., Harrison L.A., Brackin J.M., Kovacevich P.A., Mukerji P., Weller D.M., Pierson E.A. Genetic analysis of the antifungal activity of a soilborne Pseudomonas aureofaciens strain. Applied and Environmental Microbiology 1991, 57:2928-2934.
75. von Felten A., Meyer J.B., Défago G., Maurhofer M. Novel T-RFLP method to investigate six main groups of 2,4-diacetylphloroglucinol-producing pseudomonads in environmental samples. Journal of Microbiological Methods 2011, 84:379-387.
76. Wang C.X., Ramette A., Punjasamarnwong P., Zala M., Natsch A., Moënne-Loccoz Y., Défago G. Cosmopolitan distribution of phlD-containing dicotyledonous crop-associated biocontrol pseudomonads of worldwide origin. FEMS Microbiology Ecology 2001, 37:105-116.
77. Ward E. Use of molecular methods for the detection of fungal spores. Plant Pathology: Techniques and Protocols 2009, 147-159. Humana Press, New York (NY). R. Burns (Ed.).
78. Weller D.M., Landa B.B., Mavrodi O.V., Schroeder K.L., De La Fuente L., Blouin Bankhead S., Allende Molar R., Bonsall R.F., Mavrodi D.V., Thomashow L.S. Role of 2,4-diacetylphloroglucinol-producing fluorescent Pseudomonas spp. in the defense of plant roots. Plant Biology 2007, 9:4-20.
79. Weller D.M., Mavrodi D.V., van Pelt J.A., Pieterse C.M.J., van Loon L.C., Bakker P.A.H.M. Induced systemic resistance in Arabidopsis thaliana against Pseudomonas syringae pv. tomato by 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens. Phytopathology 2012, 102:403-412.
80. Zhang T., Fang H.H.P. Applications of real-time polymerase chain reaction for quantification of microorganisms in environmental samples. Applied Microbiology and Biotechnology 2006, 70:281-289.