title: Role of the cyclic lipopeptide massetolide A in biological control of Phytophthora infestans and in colonization of tomato plants by Pseudomonas fluorescens.
abstract: Pseudomonas strains have shown promising results in biological control of late blight caused by Phytophthora infestans. However, the mechanism(s) and metabolites involved are in many cases poorly understood. Here, the role of the cyclic lipopeptide massetolide A of Pseudomonas fluorescens SS101 in biocontrol of tomato late blight was examined. Pseudomonas fluorescens SS101 was effective in preventing infection of tomato (Lycopersicon esculentum) leaves by P. infestans and significantly reduced the expansion of existing late blight lesions. Massetolide A was an important component of the activity of P. fluorescens SS101, since the massA-mutant was significantly less effective in biocontrol, and purified massetolide A provided significant control of P. infestans, both locally and systemically via induced resistance. Assays with nahG transgenic plants indicated that the systemic resistance response induced by SS101 or massetolide A was independent of salicylic acid signalling. Strain SS101 colonized the roots of tomato seedlings significantly better than its massA-mutant, indicating that massetolide A was an important trait in plant colonization. This study shows that the cyclic lipopeptide surfactant massetolide A is a metabolite with versatile functions in the ecology of P. fluorescens SS101 and in interactions with tomato plants and the late blight pathogen P. infestans.
authors: Laboratory of Phytopathology, Wageningen University, Wageningen, the Netherlands.|Department of Plant Protection, Hue University of Agriculture and Forestry, Hue, Vietnam.
authors: Ha
authors: H
authors: Tran
authors: Laboratory of Phytopathology, Wageningen University, Wageningen, the Netherlands.
authors: Andrea
authors: A
authors: Ficke
authors: Laboratory of Phytopathology, Wageningen University, Wageningen, the Netherlands.
authors: Theodore
authors: T
authors: Asiimwe
authors: Laboratory of Phytopathology, Ghent University, Ghent, Belgium.
authors: Monica
authors: M
authors: Höfte
authors: Laboratory of Phytopathology, Wageningen University, Wageningen, the Netherlands.
authors: Jos M
authors: JM
authors: Raaijmakers
mesh_terms: D001426:Bacterial Proteins / Q000494:pharmacology*; D018551:Solanum lycopersicum / Q000235:genetics / Q000382:microbiology*; D006899:Mixed Function Oxygenases / Q000235:genetics / Q000378:metabolism; D010456:Peptides, Cyclic / Q000494:pharmacology*; D010838:Phytophthora / Q000187:drug effects*; D010935:Plant Diseases / Q000382:microbiology; D018515:Plant Leaves / Q000382:microbiology; D030821:Plants, Genetically Modified; D011551:Pseudomonas fluorescens / Q000502:physiology*
chemical_list: D001426:Bacterial Proteins; D010456:Peptides, Cyclic; D006899:Mixed Function Oxygenases; C022619:salicylate 1-monooxygenase
references: Andersen JB, Koch B, Nielsen TH, Sørensen D, Hansen M, Nybroe O, Christophersen C, Sørensen J, Molin S, Givskov M. 2003. Surface motility in Pseudomonas sp DSS73 is required for efficient biological containment of the root-pathogenic microfungi Rhizoctonia solani and Pythium ultimum. Microbiology-Sgm 149: 37-46.
references: Asaka O, Shoda M. 1996. Biocontrol of Rhizoctonia solani damping-off of tomato with Bacillus subtilis RB14. Applied and Environmental Microbiology 62: 4081-4085.
references: Bais HP, Fall R, Vivanco JM. 2004. Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiology 134: 307-319.
references: Daayf F, Adam L, Fernando WGD. 2003. Comparative screening of bacteria for biological control of potato late blight (strain US-8), using in-vitro, detached-leaves, and whole-plant testing systems. Canadian Journal of Plant Pathology-Revue Canadienne de Phytopathologie 25: 276-284.
references: De Boer M, Van Os GJ, Bijman V, Raaijmakers JM. 2006. Biological control of soil-borne diseases in flowerbulb cultivation in the Netherlands. Multitrophic Interactions in Soil IOBC/ Wprs Bulletin 29: 83-87.
references: De Bruijn I, De Kock MJD, Yang M, De Waard P, Van Beek TA, Raaijmakers JM. 2007. Genome-based discovery, structure prediction and functional analysis of cyclic lipopeptide antibiotics in Pseudomonas species. Molecular Microbiology 63: 417-428.
references: De Meyer G, Höfte M. 1997. Salicylic acid produced by the rhizobacterium Pseudomonas aeruginosa 7NSK2 induces resistance to leaf infection by Botrytis cinerea on bean. Phytopathology 87: 588-593.
references: De Souza JT, De Boer M, De Waard P, Van Beek TA, Raaijmakers JM. 2003. Biochemical, genetic, and zoosporicidal properties of cyclic lipopeptide surfactants produced by Pseudomonas fluorescens. Applied and Environmental Microbiology 69: 7161-7172.
references: De Vleesschauwer D, Cornelis P, Höfte M. 2006. Redox-active pyocyanin secreted by Pseudomonas aeruginosa 7NSK2 triggers systemic resistance to Magnaporthe grisea but enhances Rhizoctonia solani susceptibility in rice. Molecular Plant-Microbe Interactions 19: 1406-1419.
references: Doke N, Ramirez AV, Tomiyama K. 1987. Systemic induction of resistance in potato plants against Phytophthora infestans by local treatment with hyphal wall components of the fungus. Journal of Phytopathology-Phytopathologische Zeitschrift 119: 232-239.
references: Donaldson SP, Deacon JW. 1993. Effects of amino-acids and sugars on zoospore taxis, encystment and cyst germination in Pythium aphanidermatum (Edson) Fitzp., P. catenulatum Matthews and P. dissotocum Drechs. New Phytologist 123: 289-295.
references: Erwin DC, Robeiro OK. 1996. Phytophthora diseases world wide. St Paul, MI, USA: APS press.
references: Fogliano V, Gallo M, Vinale F, Ritieni A, Randazzo G, Greco M, Lops R, Graniti A. 1999. Immunological detection of syrirngopeptins produced by Pseudomonas syringae pv. lachrymans. Physiological and Molecular Plant Pathology 55: 255-261.
references: Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J. 1993. Requirement of salicylic-acid for the induction of systemic acquired-resistance. Science 261: 754-756.
references: Gomez-Gomez L, Boller T. 2002. Flagellin perception: a paradigm for innate immunity. Trends in Plant Science 7: 251-256.
references: Han SH, Anderson AJ, Yang KY, Cho BH, Kim KY, Lee MC, Kim YH, Kim YC. 2006. Multiple determinants influence root colonization and induction of induced systemic resistance by Pseudomonas chlororaphis O6. Molecular Plant Pathology 7: 463-472.
references: Howe GA, Lightner J, Browse J, Ryan CA. 1996. An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell 8: 2067-2077.
references: Kamoun S. 2003. Molecular genetics of pathogenic Oomycetes. Eukaryotic Cell 2: 191-199.
references: Kloepper JW, Ryu CM, Zhang SA. 2004. Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94: 1259-1266.
references: Kováts K, Binder A, Hohl HR. 1991. Cytology of induced systemic resistance of tomato to Phytophthora infestans. Planta 183: 491-496.
references: Lanahan MB, Yen HC, Giovannoni JJ, Klee HJ. 1994. The never ripe mutation blocks ethylene perception in tomato. Plant Cell 6: 521-530.
references: Latijnhouwers M, Ligterink W, Vleeshouwers V, Van West P, Govers F. 2004. A G-alpha subunit controls zoospore motility and virulence in the potato late blight pathogen Phytophthora infestans. Molecular Microbiology 51: 925-936.
references: Lavicoli A, Boutet E, Buchala A, Metraux JP. 2003. Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Molecular Plant-Microbe Interactions 16: 851-858.
references: Leclère V, Bechet M, Adam A, Guez JS, Wathelet B, Ongena M, Thonart P, Gancel F, Chollet-Imbert M, Jacques P. 2005. Mycosubtilin overproduction by Bacillus subtilis BBG100 enhances the organism's antagonistic and biocontrol activities. Applied and Environmental Microbiology 71: 4577-4584.
references: Leeman M, DenOuden EM, VanPelt JA, Dirkx FPM, Steijl H, Bakker P, Schippers B. 1996. Iron availability affects induction of systemic resistance to Fusarium wilt of radish by Pseudomonas fluorescens. Phytopathology 86: 149-155.
references: Leeman M, Vanpelt JA, Denouden FM, Heinsbroek M, Bakker P, Schippers B. 1995. Induction of systemic resistance by Pseudomonas fluorescens in radish cultivars differing in susceptibility to Fusarium wilt, using a novel bioassay. European Journal of Plant Pathology 101: 655-664.
references: Lindow SE, Brandl MT. 2003. Microbiology of the phyllosphere. Applied and Environmental Microbiology 69: 1875-1883.
references: Van Loon LC, Bakker P, Pieterse CMJ. 1998. Systemic resistance induced by rhizosphere bacteria. Annual Review of Phytopathology 36: 453-483.
references: Lourenço Júnior V, Maffia LA, Romeiro RdS, Mizubuti ESG. 2006. Biocontrol of tomato late blight with the combination of epiphytic antagonists and rhizobacteria. Biological Control 38: 331-340.
references: Meziane H, Van der Sluis I, Van Loon LC, Höfte M, Bakker P. 2005. Determinants of Pseudomonas putida WCS358 involved in inducing systemic resistance in plants. Molecular Plant Pathology 6: 177-185.
references: Molina L, Constantinescu F, Michel L, Reimmann C, Duffy B, Defago G. 2003. Degradation of pathogen quorum-sensing molecules by soil bacteria: a preventive and curative biological control mechanism. FEMS Microbiology Ecology 45: 71-81.
references: Nielsen TH, Nybroe O, Koch B, Hansen M, Sørensen J. 2005. Genes involved in cyclic lipopeptide production are important for seed and straw colonization by Pseudomonas sp. strain DSS73. Applied and Environmental Microbiology 71: 4112-4116.
references: Nielsen TH, Sørensen J. 2003. Production of cyclic lipopeptides by Pseudomonas fluorescens strains in bulk soil and in the sugar beet rhizosphere. Applied and Environmental Microbiology 69: 861-868.
references: Nybroe O, Sørensen J. 2004. Production of cyclic lipopeptides by fluorescent Pseudomonads. Biosynthesis of marcromolecules and molecular metablolism: Ramos. Vol. 3, New York, NY, USA: Kluwer Academic/Plenum Publishers, 147-172.
references: Ongena M, Jacques P, Toure Y, Destain J, Jabrane A, Thonart P. 2005a. Involvement of fengycin-type lipopeptides in the multifaceted biocontrol potential of Bacillus subtilis. Applied Microbiology and Biotechnology 69: 29-38.
references: Ongena M, Jourdan E, Schafer M, Kech C, Budzikiewicz H, Luxen A, Thonart P. 2005b. Isolation of an n-alkylated benzylamine derivative from Pseudomonas putida BTP1 as elicitor of induced systemic resistance in bean. Molecular Plant-Microbe Interactions 18: 562-569.
references: Pieterse CMJ, Van Wees SCM, Van Pelt JA, Knoester M, Laan R, Gerrits N, Weisbeek PJ, Van Loon LC. 1998. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10: 1571-1580.
references: Raaijmakers JM, De Bruijn I, De Kock MJD. 2006. Cyclic lipopeptide production by plant-associated Pseudomonas spp. Diversity, activity, biosynthesis, and regulation. Molecular Plant-Microbe Interactions 19: 699-710.
references: Raaijmakers JM, Vandersluis I, Vandenhout M, Bakker P, Schippers B. 1995. Dispersal of wild-type and genetically-modified Pseudomonas spp. from treated seeds or soil to aerial parts of radish plants. Soil Biology and Biochemistry 27: 1473-1478.
references: Roongsawang N, Hase K, Haruki M, Imanaka T, Morikawa M, Kanaya S. 2003. Cloning and characterization of the gene cluster encoding arthrofactin synthetase from Pseudomonas sp MIS38. Chemistry and Biology 10: 869-880.
references: Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Pare PW. 2004. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiology 134: 1017-1026.
references: Sanchez V, Bustamante E, Shattock R. 1998. Selection of antagonists for biological control of Phytophthora infestans in tomato. Manejo Integrado de Plagas 48: 25-34.
references: 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-acyl-L-homoserine lactone-producing rhizosphere bacteria. Plant, Cell & Environment 29: 909-918.
references: Stachelhaus T, Mootz HD, Marahiel MA. 1999. The specificity-conferring code of adenylation domains in nonribosomal peptide synthetases. Chemistry & Biology 6: 493-505.
references: Stromberg A, Brishammar S. 1991. Induction of systemic resistance in potato (Solanum tuberosum L.) plants to late blight by local treatment with Phytophthora infestans (Mont) Debary, Phytophthora cryptogea Pethyb and Laff, or dipotassium phosphate. Potato Research 34: 219-225.
references: Ton J, Davison S, Van Wees SCM, Van Loon LC, Pieterse CMJ. 2001. The arabidopsis ISR1 locus controlling rhizobacteria-mediated induced systemic resistance is involved in ethylene signaling. Plant Physiology 125: 652-661.
references: Van West P, Morris BM, Reid B, Appiah AA, Osborne MC, Campbell TA, Shepherd SJ, Gow NAR. 2002. Oomycete plant pathogens use electric fields to target roots. Molecular Plant-Microbe Interactions 15: 790-798.
references: Yan ZN, Reddy MS, Ryu CM, McInroy JA, Wilson M, Kloepper JW. 2002. Induced systemic protection against tomato late blight elicited by plant growth-promoting rhizobacteria. Phytopathology 92: 1329-1333.
references: Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JDG, Felix G, Boller T. 2004. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428: 764-767.