Biocontrol potential of Pseudomonas fluorescens strains producing 2,4-diacetylphloroglucinol and hydrogen cyanide against tomato Fusarium wilt

Document Type : Complete paper

Authors

1 Assistant Professor, Department of Plant Protection, College of Agriculture and Natural Resources, Persian Gulf University, Bushehr, Iran

2 Assistant Professor, Department of Plant Breeding, College of Agriculture and Natural Resources, Persian Gulf University, Bushehr, Iran

Abstract

Pseudomonas fluorescens strains producing 2,4-diacetylphloroglucinol (DAPG) contribute to the biological control of many fungal plant diseases. Tomato Fusarium wilt is one of the most important diseases of this plant that causes considerable damage to the crop. In the current study, 35 strains of P. fluorescens were screened for the presence of phlD and hcnAB genes and it was revealed that nine strains harbored the target genes. Antagonistic ability of phlD+- and hcnAB+strains was tested against pathogen under in vitro conditions using dual culture method and five strains including PGU, PGU1, PGU2, PGU3 and CHA0 were selected for further studies. Strains were checked for production of antimicrobial metabolites and plant growth promoting traits and then, their potential to control Fusarium wilt and promoting tomato growth was investigated under greenhouse conditions. Laboratory results showed that bacterial strains were capable of producing antimicrobial compounds like DAPG, pyoluteorin and monoacetylphloroglucinol, hydrogen cyanide, indole-3-acetic acid, protease and solubilization of mineral phosphate. Strains were also able to control the disease and stimulate tomato plants growth significantly under greenhouse conditions and PGU strain performed better in comparison to other strains. This study suggests that the production of antimicrobial metabolites and/or metabolites stimulating plant growth plays a key role in effective disease control and increasing plant growth parameters under greenhouse conditions.

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References

Abo-Elyousr KAM, Mohamed HM (2009). Biological control of Fusarium wilt in tomato by plant Growth-promoting yeast and Rhizobacteria. Plant Pathology Journal 25(2):199-204.
Alström A, Burns RG (1989) Cyanide production by rhizobacteria as a possible mechanism of plant growth inhibition. Biology and Fertility of Soils 7: 232-238.
Amini K (2009). Physiological race of Fusarium oxysporum f. sp. Lycopersici in Kurdistan Provice of Iran and reaction of some tomato cultivars to race 1 of pathogen. Plant Pathology 8: 68-73.
Beckman CH (1987) The nature of wilt diseases of plants. APS Press, St Paul, MN.
Blumer C, Haas D (2000) Mechanism, regulation, and ecological role of bacterial cyanide biosynthesis. Archives of Microbiology 173: 170-177.
Buysens S, Heungens K, Poppe J, Höfte M (1996) Involvement of pyochelin and pyoverdin in suppression of Pythium-induced damping-off of tomato by Pseudomonas aeruginosa 7NSK2. Applied and Environmental Microbiology 62: 865-871.
Bottiglieri M, Keel C (2006) Characterization of PhlG, a hydrolase that specifically degrades the antifungal compound 2,4-diacetylphloroglucionol in biocontrol agent Pseudomonas fluorescens CHA0. Applied and Environmental Microbiology 72: 418-427.
Castric PA (1977) Glycine metabolism by Pseudomonas aeruginosa: hydrogen cyanide biosynthesis. Journal of Bacteriology 130: 826-831.
Chen YP, Rekha PD, Arun AB, Shen FT, Lai WA, Young CC (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Applied Soil Ecology 34: 33-41.
De La Fuente L, Thomashow L, Weller D, Bajsa N, Quagliotto L, Chernin L, Arias A (2004) Pseudomonas fluorescens UP61 isolated from birds foot trefoil rhizosphere produces multiple antibiotics and exerts a broad spectrum of biocontrol activity. European Journal of Plant Pathology 110: 671-681.
De Meyer G, Capieau K, Audenaert K, Buchala A, Métraux J, Höfte M (1999). Nanogram amount of salicylic acid produced by the rhizobacterium Pseudomonas aeruginosa 7NSK2 activate the systemic acquired resistance pathway in bean. Molecular Plant-Microbe Interaction 12: 450-458.
De Souza JT, Arnould C, Deulvot C, Lemanceau P, Gianinazzi-Pearson V, Raaijmakers JM (2003) Effect of 2,4-diacetylphloroglucinol on Pythium: cellular responses and variation in sensitivity among propagules and species. Phytopathology 93: 966-975.
De Werra P,Péchy-Tarr M,Keel C,Maurhofer M (2009) Role of gluconic acid production in the regulation of biocontrol traits of Pseudomonas fluorescens CHA0. Applied and Environmental Microbiology75(12): 4162-74.
Duffy B, Keel C, Defago G (2004) Potential role of pathogen signaling in multitrophic plant-microbe interactions involved in disease protection. Applied and Environmental Microbiology 70(3): 1836-1842. 
Fakhouri W, Buchenauer H (2002) Characteristics of fluorescent pseudomonad isolates towards controlling of tomato wilt caused by Fusarium oxysporum f. sp. lycopersici. Journal of Plant diseases and Protection 110 (2): 143-156.
Flaishman MA, Eyal Z, Zilberstein A, Voisard C, Haas D (1996) Suppression of Septoria tritici blotch and leaf rust of wheat by recombinant cyanide-producing strains of Pseudomonas putida. Molecular Plant-Microbe Interaction 9: 642-645.
Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nature Reviews Microbiology 3: 307-319.
Haas D, Keel C (2003) Regulation of antibiotic production in root-colonizing Pseudomonas spp. and relevance for biological control of plant disease. Annual Review of Phytopathology 41: 117-153.
Hagedorn C, Gould WD, Bardinelli TR (1998) Rhizobacteria of cotton and their repression of seedling disease pathogens. Applied and Environmental Microbiology 55: 2793-2797.
Han J, Sun L, Dong X, Cai Z, Sun X, Yang H, Wang Y, Song W (2005) Characterization of a novel plant growth-promoting bacteria strain Delftia tsuruhatensis HR4 both as a diazotroph and a potential biocontrol agent against various plant pathogens. Systematic and Applied Microbiology 28(1): 66-76.
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. Molecular Plant-Microbe Interaction 16: 851-858.
Jamali F (2009) Influence of some biotic factors on the expression of hydrogen cyanide- and 2,4-diacetylphloroglucinol biosynthesis genes in Pseudomonas fluorescens on bean rhizosphere, Ph. D. thesis in Plant pathology, College of Agriculture, Tehran University. (in Persian)
Jamali F, Bayat F (2015) Phenotypic and genotypic study of Pseudomonas fluorescens strain PGU0 and assessment of its biocontrol against Rhizoctonia solani, the causal agent of bean damping- off. Biological Control of Pests and Plant Diseases 4 (1): 37-46.
Keel C, Défago G (1997) Interactions between beneficial soil bacteria and root pathogens: Mechanisms and ecological impact. In: Gange AC, Brown VK (eds.), Multitrophic Interactions in terrestrial Systems, the 36th symposium of the British Ecological Society, Royal Holloway College, university of London, Blackwell Science, Oxford. pp. 27-46.
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. Molecular Plant-Microbe Interaction 5(1): 4-13.
Keel C, Weller DM, Natsch A, Défago G, Cook RJ, Thomashow LS (1996) Conservation of the 2,4-diacetylphloroglucinol biosynthesis locus among fluorescent Pseudomonas strains from diverse geographic locations. Applied and Environmental Microbiology 62: 552-563.
Kloepper JW, Gutierrez-Estrada A, Mclnroy JA (2007) Photoperiod regulates elicitation of growth promotion but not induced resistance by plant growth-promoting rhizobacteria. Microbiology 53(2): 159-167.
Landa BB, Mavrodi OV, Raaijmakers JM, McSpadden Gardener BB, Thomashow LS, Weller DM (2002) Differential ability of genotypes of 2,4-diacetylphloroglucinolproducing Pseudomonas fluorescens strains to colonize the roots of pea plants. Applied and Environmental Microbiology 68: 3226-3237.
Larkin RP, Fravel, DR (1998) Efficacy of various fungal and bacterial biocontrol organisms for control of Fusarium wilt of tomato. Plant Disease 82: 1022–1028.
Laville J, Blumer C, Von Schroetter C, Gaia V, Défago G, Keel C, Haas D (1998) Characterization of the hcnABC gene cluster encoding hydrogen cyanide synthase and anaerobic regulation by ANR in the strictly aerobic biocontrol agent Pseudomonas fluorescens CHA0. Journal of Bacteriology 180(12): 3187-3196.
Lucy M, Reed E, Glick BR (2004). Application of free living plant growth-promoting rhizobacteria. Antonie van Leeuwenhoek 86: 1-25.
Lugtenberg BJJ, Dekkers LC (1999) What makes Pseudomonas bacteria rhizosphere competent? Environmental Microbiology 1: 9-13.
Maurhofer M, Keel C, Haas D, Défago G (1994) Pyoluteorin production by Pseudomonas fluorescens strain CHA0 is involved in the suppression of Pythium damping-off of cress, but not cucumber. European Journal of Plant Pathology100: 221-232.
Maurhofer M, Keel C, Haas D, Défago G (1995) Influence of plant species on disease suppression by Pseudomonas fluorescens CHA0 with enhanced antibiotic production. Plant Pathology 44: 40-50.
Maurhofer M, Keel C, Schnider U, Voisard C, Défago G (1992) Influence of enhanced antibiotic production in Pseudomonas fluorescens strain CHA0 on its disease suppressive capacity. Phytopathology 82: 190-195.
Maurhofer M, Reimmann C, Schmidli-Sacherer P, Heeb S, Haas D, Défago G (1998) Salicylic acid biosynthetic genes expressed in Pseudomonas fluorescens strain P3 improve the induction of systemic resistance in tobacco against tobacco necrosis virus. Phytopathology 88: 678-684.
Mc Spadden Gardener BB, Mavrodi DV, Thomashow LS, Weller DM (2001) A rapid polymerase chain reaction-based assay characterizing rhizosphere populations of 2,4-diacetylphloroglucinol-producing bacteria. Phytopathology 91: 44-54.
Morrissey JP, Abbas A, Mark L, Cullinane M, O’Gara F (2004) Biosynthesis of antifungal metabolites by biocontrol strains of Pseudomonas. In: Ramos JL (ed.), Pseudomonas: Biosynthesis of macromolecules and molecular metabolism, Vol. 3. New York, USA: Kluwer Academic/Plenum Publishers, pp. 635-670.
Moynihan JA, Morrissey JP, Coppoolse ER, Stiekema WJ, O'Gara F, Boyd EF (2009) Evolutionary history of the phl gene cluster in the plant-associated bacterium Pseudomonas fluorescens. Applied and Environmental Microbiology 75(7): 2122-2131.
Patten CL, Glick BR (2002) The role of bacterial indole acetic acid in the development of the host plant root system. Applied and Environmental Microbiology 68: 3795-3801.
Picard C, Di Cello F, Ventura M, Fani R, Guckert A (2000) Frequency and biodiversity of 2,4-diacetylphloroglucinol-producing bacteria isolated from the maize rhizosphere at different stages of plant growth. Applied and Environmental Microbiology 66: 948-955.
Raaijmakers JM, Weller DM, Thomashow LS (1997) Frequency of antibiotic-producing Pseudomonas spp. in natural environments. Applied and Environmental Microbiology 63: 881-887.
Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant and Soil 321: 305-339.
Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability. Plant Physiology156: 989-996.
Rodriguez-Molina M, Medina L, lorres-vila L, cuartero J (2003) Vascular colonization pattern in susceptible and resistant tomato cultivars inoculated with Fusarium oxysporum f. sp. lycopersici race 0 and 1. Plant pathology 52:199-203.
Rodriguez H, Fraga R, Gonzalez, T, Bashan Y (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant and Soil 287: 15-21.
Sharifi-Tehrani A, Zala M, Natsch A, Moënne-Loccoz Y, Défago G (1998) Biocontrol of soil-borne fungal plant diseases by 2,4-diacetylphloroglucinol-producing fluorescent pseudomonads with different restriction profiles of amplified 16S rDNA. European Journal of Plant Pathology 104: 631-643.
Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiology Reviews 31(4): 425-448.
Sperber JI (1958) The incidence of apatite-solubilizing organisms in the rhizosphere and soil. Australian Journal of Agricultural Research 9: 778-781.
Svercel M, Duffy B, Défago G (2007) PCR amplification of hydrogen cyanide biosynthetic locus hcnAB in Pseudomonas spp. Journal of Microbiological Methods 70: 209-213.
Thomashow LS, Weller DM (1996) Current concepts in the use of introduced bacteria for biological control: mechanisms and antifungal metabolites, In: Stacey G, Keen NT (eds.), Plant-Microbe Interactions, Vol. 1. Chapman and Hall, New York. pp. 187-235.
Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annual Review of Phytopathology 36: 453-483.
Vessey KJ (2003) Plant growth-Promoting rhizobacteria as biofertilizers. Plant and Soil 255: 571-586.
Viani A, Alizadeh A, Babadoust M, Peighami E (2008) Investigation of Fusarium diseases of tomatoes in East Azarbaijan. Journal of Agricultural Sciences and Natural Resources 14(5):192-206. (in Persian)
Wang C, Ramette A, Pungasamarnwong P, Zala M, Natsch A, Moënne-Loccoz Y, Défago G (2001) Cosmopolitan distribution of phlD-containing dicotyledonous crop-associated biocontrol pseudomonads of worldwide origin. FEMS Microbiology Ecology 37: 105-116.
Weller DM (2007) Pseudomonas biocontrol agents of soilborne pathogens: looking back over 30 years. Phytopathology 97: 250-256.
Weller DM, Landa BB, Mavrodi OV, Schroeder LL, De La Fuente L, Blouin Bankhead S, Allende Molar R, Bonsall RF, Mavrodi DV, Thomashow LS (2006) Role of 2,4-diacetylphloroglucinol-producing fluorescent Pseudomonas spp. in the defense of plant roots. Plant Biology 9(1): 4-20.
Weller DM, Raaijmakers JM, McSpadden Gardener BB, Thomashow LS (2002) Microbial populations responsible for specific suppressiveness to plant pathogens. Annual Review of Phytopathology 40: 309-348.
Zhou T-T, Li C-Y, Chen D, Wu K, Shen Q-R, Shen B (2014) phlF- mutant of Pseudomonas fluorescens J2 improved 2,4-DAPG biosynthesis and biocontrol efficacy against tomato bacterial wilt. Biological Control 78: 1-8.
BIOLOGICAL CONTROL OF PESTS AND PLANT DISEASES
Volume 5, Issue 2 - Serial Number 2
Autumn & Winter
December 2016
Pages 235-246

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