Amino Acids, Iron, and Growth Rate as Key Factors Influencing Production of the Pseudomonas Putida Btp1 Benzylamine Derivative Involved in Systemic Resistance Induction in Different Plants
[en] The biological control bacterium Pseudomonas putida BTP1 exerts its protective effect mostly by inducing an enhanced state of resistance in the host plant against pathogen attack [induced systemic resistance (ISR)]. We previously reported that a specific compound derived from benzylamine may be involved in the elicitation of the ISR phenomenon by this Pseudomonas strain. In this article, we provide further information about the N,N-dimethyl-N-tetradecyl-N-benzylammonium structure of this determinant for ISR and show that the benzylamine moiety may be important for perception of the molecule by root cells of different plant species. We also investigated some regulatory aspects of elicitor production with the global aim to better understand how in situ expression of these ISR elicitors can be modulated by physiological and environmental factors. The biosynthesis is clearly related to secondary metabolism, and chemostat experiments showed that the molecule is more efficiently produced at low cell growth rate. Interestingly, the presence of free amino acids in the environment is necessary for optimal production, and a specific positive effect of phenylalanine was evidenced in pulsed continuous cultures. The influence of other abiotic factors, such as mineral content, oxygen concentration, or pH, on elicitor production is also reported and discussed with respect to the specific conditions that the producing strain undergoes in the rhizosphere environment.
Ongena, MARC ; Université de Liège - ULiège > Gembloux Agro-Bio Tech > Gembloux Agro-Bio Tech
Jourdan, Emmanuel ; Université de Liège - ULiège > Centre Wallon de biologie industrielle
Adam, Akram
Schafer, M.
Budzikiewicz, H.
Thonart, Philippe ; Université de Liège - ULiège > Gembloux Agro-Bio Tech > Gembloux Agro-Bio Tech - Biochimie et microbiologie industrielles
Language :
English
Title :
Amino Acids, Iron, and Growth Rate as Key Factors Influencing Production of the Pseudomonas Putida Btp1 Benzylamine Derivative Involved in Systemic Resistance Induction in Different Plants
Ahn IP, Kim S, Lee YH (2005) Vitamin B1 functions as an activator of plant disease resistance. Plant Physiol 138: 1505-1515
Audenaert K, Pattery T, Cornélis P, Höfte M (2002) Induction of systemic resistance to Botrytis cinerea in tomato by Pseudomonas aeruginosa 7NSK2: role of salicylic acid, pyochelin and pyocyanin. Mol Plant-Microbe Interact 15:1147-1156
Bakker PAHM, Pieterse CMJ, van Loon LC (2007) Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97:239-243
Bent, E (2006) Induced systemic resistance mediated by plant growth-promoting rhizobacteria (PGPR) and fungi (PGPF). In: Tuzun, S, Bent E (Eds.) Multigenic and Induced Systemic Resistance in Plants, Springer, New York, pp 225-258
Bloemberg GV, Lugtenberg BJJ (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol 4:343-350
Budzikiewicz H (2004) Siderophores of the Pseudomonadaceae sensu stricto (fluorescent and non-fluorescent Pseudomonas spp.). Fortschr Chem Org Naturst 87:81-237
Budzikiewicz H, Schäfer M (2005) Massenspektrometrie, 5th edn. Wiley-VCH, Weinheim, p 129
Chin-A-Woeng TFC, de Priester W, van der Bij AJ, Lugtenberg BJJ (1997) Description of the colonization of a gnotobiotic tomato rhizosphere by Pseudomonas fluorescens biocontrol strain WCS365, using scanning electron microscopy. Mol Plant-Microbe Interact 10:79-86
De Meyer G, Capieau K, Audenaert K, Buchala A, Métraux JP, Höfte M (1999) Nanogram amounts of salicylic acid produced by the rhizobacterium Pseudomonas aeruginosa 7NSK2 activate the systemic acquired resistance pathway in bean. Mol Plant-Microbe Interact 12:450-458
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
De Souza JT, Mazzola M, Raaijmakers JM (2003) Conservation of the response regulator gene gacA in Pseudomonas species. Environ Microbiol 5:1328-1340
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. Mol Plant Microbe Interact. 19:1406-1419
Dekkers LC, Mulders IHM, Phoelich CC, Chin-A-Woeng TFC, Wijfjes AHM, Lugtenberg BJJ (2000) The sss colonization gene of the tomato-Fusarium oxysporum f. sp radicis-lycopersici biocontrol strain Pseudomonas fluorescens WCS365 can improve root colonization of other wild-type Pseudomonas spp. bacteria. Mol Plant-Microbe Interact 13:1177-1183
Di Mattia E, Grego S, Cacciari I (2002) Eco-physiological characterization of soil bacterial populations in different states of growth. Microb Ecol 43:34-43
Dos Santos VAPM, Heim S, Moore ERB, Stratz M, Timmis KN (2004) Insights into the genomic basis of niche specificity of Pseudomonas putida KT2440. Environ Microbiol 6:1264-1286
Duffy BK, Défago G (1999) Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. Appl Environ Microbiol 65:2429-2438
Duijff BJ, Gianinazzi-Pearson V, Lemanceau P (1997) Involvement of the outer-membrane lipopolysaccharides in the endophytic colonization of tomato roots by biocontrol Pseudomonas fluorescens WCS417r. New Phytol 135:325-334
Durrant WE, Dong X (2004) Systemic acquired resistance. Ann Rev Phytopathol 42:185-209
Espinosa-Urgel M, Kolter R, Ramos JL (2002) Root colonization by Pseudomonas putida: love at first sight. Microbiology 148:1-3
Fravel DR (2005) Commercialization and implementation of biocontrol. Ann Rev Phytopathol 43:337-359
Ghiglione JF, Gourbiere F, Potier P, Philippot L, Lensi, R (2000) Role of respiratory nitrate reductase in ability of Pseudomonas fluorescens YT101 to colonize the rhizosphere of maize. Appl Environ Microbiol 66:4012-4016
Glazebrook J, Chen WJ, Estes B, Chang HS, Nawrath C, Métraux JP, Zhu T, Katagiri F (2003) Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant J 34:217-228
Gomez-Gomez L, Boller T (2002) Flagellin perception: a paradigm for innate immunity. Trends Plant Sci 7:251-256
Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 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. Ann Rev Phytopathol 41:117-153
Hojberg O, Schnider U, Winteler HV, Sorensen J, Haas D (1999) Oxygen-sensing reporter strain of Pseudomonas fluorescens for monitoring the distribution of low-oxygen habitats in soil. Appl Environ Microbiol 65:4085-4093
Iavicoli A, Boutet E, Buchala A, Métraux JP (2003) Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Mol Plant-Microbe Interact 16:851-858
Jiménez JI, Minambres B, Garcia JL, Diaz E (2002) Genomic analysis of the aromatic catabolic pathways from Pseudomonas putida KT2440. Environ Microbiol 4:824-841
Kawano T, Pinontoan R, Uozumi N, Miyake C, Asada K, Kolattukudy PE, Muto S (2000) Aromatic monoamine-induced immediate oxidative burst leading to an increase in cytosolic Ca2+ concentration in tobacco suspension culture. Plant Cell Physiol 41:1251-1258
Keel C, Voisard C, Berling CH, Kahr G, Défago G (1989) Iron sufficiency, a prerequisite for the suppression of tobacco black root rot by Pseudomonas fluorescens strain CHA0 under gnotobiotic conditions. Phytopathology 79:584-589
Kloepper JW, Ryu CM, Zhang SA (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259-1266
Kloepper JW, Tuzun S, Kùc JA (1992) Proposed definitions related to induced disease resistance. Biocontrol Sci Technol 2:349-351
Kozdroj J, van Elsas JD (2000) Response of the bacterial community to root exudates in soil polluted with heavy metals assessed by molecular and cultural approaches. Soil Biol Biochem 32:1405-1417
Leeman M, den Ouden FM, van Pelt JA, Dirkx FPM, Steijl H, Bakker PAHM, Schippers B (1996) Iron availability affects induction of systemic resistance to Fusarium wilt of radish by Pseudomonas fluorescens. Phytopathology 86:149-155
Leeman M, van Pelt JA, den Ouden FM, Heinsbrock M, Bakker PAHM, Schippers B (1995) Induction of systemic resistance against Fusarium wilt of radish by lipopolysaccharides of Pseudomonas fluorescens. Phytopathology 85:1021-1027
Lugtenberg BJJ, Chin-A-Woeng TFC, Bloemberg GV (2002) Microbe-plant interactions: principles and mechanisms. Antonie Van Leeuwenhoek 81:373-383
Maurhofer M, Hase C, Meuwly P, Métraux JP, Défago G (1994) 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 84:139-146
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
Meziane H, van der Sluis I, van Loon LC, Höfte M, Bakker PAHM (2005) Determinants of Pseudomonas putida WCS358 involved in inducing systemic resistance in plants. Mol Plant Pathol 6:177-185
Nystrom T (2004) Stationary-phase physiology. Annu Rev Microbiol 58:161-181
Ongena M, Daayf F, Jacques P, Thonart P, Benhamou N, Paulitz TC, Bélanger RR (2000) Systemic induction of phytoalexins in cucumber in response to treatments with fluorescent pseudomonads. Plant Pathol 49:523-530
Ongena M, Daayf F, Jacques P, Thonart P, Benhamou N, Paulitz TC, Cornélis P, Koedam N, Bélanger RR (1999) Protection of cucumber against Pythium root rot by fluorescent pseudomonads: predominant role of induced resistance over siderophores and antibiosis. Plant Pathol 48:66-76
Ongena M, Giger A, Jacques P, Dommes J, Thonart P (2002) Study of bacterial determinants involved in the induction of systemic resistance in bean by Pseudomonas putida BTP1. Eur J Plant Pathol 108:187-196
Ongena M, Jacques P, Delfosse P, Thonart P (2001) Unusual traits of the pyoverdin-mediated iron acquisition system in Pseudomonas putida strain BTP1. Biometals 15:1-13
Ongena M, Jourdan E, Schäfer M, Kech C, Budzikiewicz H, Luxen A, Thonart P (2005) Isolation of an N-alkylated benzylamine derivative from Pseudomonas putida BTP1 as elicitor of induced systemic resistance in bean. Mol Plant-Microbe Interact 18:562-569
Osburn RM, Schroth MN, Hancock JG, Hendson M (1989) Dynamics of sugar beet seed colonization by Pythium ultimum and Pseudomonas species: effects on seed rot and damping-off. Phytopathology 79:709-716
Pieterse CMJ, van Pelt JA, Verhagen BWM, Ton J, van Wees SCM, Leon-Kloosterziel KM, van Loon LC (2003) Induced systemic resistance by plant growth-promoting rhizobacteria. Symbiosis 35:39-54
Press CM, Loper JE, Kloepper JW (2001) Role of iron in rhizobacteria-mediated induced systemic resistance of cucumber. Phytopathology 91:593-598
Press CM, Wilson M, Tuzun S, Kloepper JW (1997) Salicylic acid produced by Serratia marcescens 90-166 is not the primary determinant of induced systemic resistance in cucumber or tobacco. Mol Plant-Microbe Interact 10:761-768
Raaijmakers JM, Leeman M, van Oorschot MMP, van der Sluis I, Schippers B, Bakker PAHM (1995) Dose-response relationships in biological control of Fusarium wilt of radish by Pseudomonas spp. Phytopathology 85:1075-1081
Rainey PB (1999) Adaptation of Pseudomonas fluorescens to the plant rhizosphere. Environ Microbiol 1:243-257
Reitz M, Oger P, Meyer A, Niehaus K, Farrand SK, Hallmann J, Sikora RA (2002) Importance of the O-antigen, core-region and lipid A of rhizobial lipopolysaccharides for the induction of systemic resistance in potato to Globodera pallida. Nematology 4:73-79
Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Pare PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017-1026
Salvatore RN, Nagle AS, Jung KW (2002) Cesium effect: High chemoselectivity in direct N-alkylation of amines. J Org Chem 67:674-683
Serino L, Reimmann C, Visca P, Beyeler M, Della Chiesa V, Haas D (1997) Biosynthesis of pyochelin and dihydroaeruginosic acid requires the iron-regulated pchDCBA operon in Pseudomonas aeruginosa. J Bacteriol 179:248-257
Silla Santos MH (1996) Biogenic amines: their importance in foods. Int J Food Microbiol 29:213-231
Simeoni LA, Lindsay WL, Baker R (1987) Critical iron level associated with biological control of Fusarium wilt. Phytopathology 77:1057-1061
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
Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Ann Rev Phytopathol 36:453-483
Van Peer R, Schippers B (1992) Lipopolysaccharides of plant-growth promoting Pseudomonas sp. strain WCS417r induce resistance in carnation to Fusarium wilt. Neth J Plant Pathol 98:129-139
Van Rij ET, Wesselink M, Chin-A-Woeng TFC, Bloemberg GV, Lugtenberg BJJ (2004) Influence of environmental conditions on the production of phenazine-1-carboxamide by Pseudomonas chlororaphis PCL1391. Mol Plant-Microbe Interact 17:557-566
Venturi V, Ottevanger C, Bracke M, Weisbeek P (1995) Iron regulation of siderophore biosynthesis and transport in Pseudomonas putida WCS358-involvement of a transcriptional activator and of the fur protein. Mol Microbiol 15:1081-1093