[en] Multiple strains of Bacillus subtilis were demonstrated to stimulate plant defense responses, and cyclic lipopeptides may be involved in the elicitation of this induced systemic resistance phenomenon. Here, we further investigated molecular events underlying the interaction between wuch lipopeptides and plant cells. Addition of surfactin but not fengycin or iturin in the micromolar range to tobacco cell suspensions induced defense-related early events such as extracellular medium alkalinization coupled with ion fluxes and reactive oxygen species production. Surfactin also stimulated the defense enzymes phenylalanine ammonia lyase and lipoxygenase and modified the pattern of phenolics produced by the elicited cells. The occurence of these surfactin-elicited early events is closely related to Ca2+ influx and dynamic changes in protein phosphorylation but is not associed with any marked phytotoxicity or adverse effect on the integrity and growth potential of the treated tobacco cells.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Jourdan, Emmanuel ; Université de Liège - ULiège > Centre Wallon de biologie industrielle
Henry, Guillaume; Université de Liège - ULiège > CWBI
Duby, F.; Université de Liège - ULiège > Sciences de la Vie > Biologie Moléculaire et Biotechnologie Végétales
Dommes, Jacques ; Université de Liège - ULiège > Département des sciences de la vie > Biologie moléculaire et biotechnologie végétales
Apel, K., and Hirt, H. 2004. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55:373-399.
Audenaert, K., Pattery, T., Cornelis, P., and Höfte, M. 2002. Induction of systemic resistance to Botrytis cinema in tomato by Pseudomonas aeruginosa 7NSK2:Role of salicylic acid, pyochelin, and pyocyanin. Mol. Plant-Microbe Interact. 15:1147-1156.
Bais, H. P., Fall, R., and Vivanco, J. M. 2004. Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol. 134:307-319.
Baker, C. J., and Mock, N. M. 1994. An improved method for monitoring cell-death in cell-suspension and leaf disc assays using Evans blue. Plant Cell Tissue Organ. Cult. 39:7-12.
Bakker, P., Pieterse, C. M. J., and Van Loon, L. C. 2007. Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97:239-243.
Baysal, T., and Demirdoven, A. 2007. Lipoxygenase in fruits and vegetables: Areview. Enzyme Microb. Technol. 40:491-496.
Blée, E. 2002. Impact of phyto-oxylipins in plant defense. Trends Plant Sci. 7:315-321.
Boiler, T. 1995. Chemoperception of microbial signals in plant cells. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46:189-214.
Bonmatin, J. M., Laprevote, O., and Peypoux, F. 2003. Diversity among microbial cyclic lipopeptides: Iturins and surfactins. Activity-structure relationships to design new bioactive agents. Comb. Chem. High Throughput Screen 6:541-556.
Bourque, S., Ponchet, M., Binet, M. N., Ricci, P., Pugin, A., and Lebrun- Garcia, A. 1998. Comparison of binding properties and early biological effects of elicitins in tobacco cells. Plant Physiol. 118:1317-1326.
Carrillo, C., Teruel, J. A., Aranda, F. J., and Ortiz, A. 2003. Molecular mechanism of membrane permeabilization by the peptide antibiotic surfactin. Biochim. Biophys. Acta 1611:91-97.
Chandra, S., Heinstein, P. E, and Low, P. S. 1996. Activation of phospholipase A by plant defence elicitors. Plant Physiol. 110:979-986.
Chisholm, S. T., Coaker, G., Day, B., and Staskawicz, B. J. 2006. Hostmicrobe interactions: Shaping the evolution of the plant immune response. Cell 124:803-814.
Coventry, H. S., and Dubery, I. A. 2001. Lipopolysaccharides from Burkholderia cepacia contribute to an enhanced defensive capacity and the induction of pathogenesis-related proteins in Nicotianae tabacum. Physiol. Mol. Plant Pathol. 58:149-158.
Deleu, M., Bouffioux, O., Razafindralambo, H., Paquot, M., Hbid, C., Thonart, P., Jacques, P., and Brasseur, R. 2003. Interaction of surfactin with membranes: A computational approach. Langmuir 19:3377-3385.
De Meyer, G., Audenaert, K., and Hofte, M. 1999. Pseudomonas aeruginosa 7NSK2-induced systemic resistance in tobacco depends on in planta salicylic acid accumulation but is not associated with PRla expression. Eur. J. Plant. Pathol. 105:513-517.
Desender, S., Klarzynski, O., Potin, P., Barzic, M. R., Andrivon, D., and Val, F. 2006. Lipopolysaccharides of Pectobacterium atrosepticum and Pseudomonas corrugata induce different defense response patterns in tobacco, tomato, and potato. Plant Biol. 8:636-645.
Desender, S., Andrivon, D., and Val, F. 2007. Activation of defense reactions in Solanaceae: Where is the specificity? Cell. Microbiol. 9:21-30.
De Vleesschauwer, D., Cornelis, P., and Hofte, 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.
Dixon, R. A., Achnine, L., Kota, P., Liu, C. J., Reddy, M. S. S., and Wang, L. J. 2002. The phenylpropanoid pathway and plant defense-a genomics perspective. Mol. Plant Pathol. 3:371-390.
Dong, H., Delaney, T. P., Bauer, D. W, and Beer, S. V 1999. Harpin induces disease resistance in Arabidopsis through the systemic acquired resistance pathway mediated by salicylic acid and the NIM1 gene. Plant J. 20:207-215.
Dorey, S., Kopp, M., Geoffrey, P., Fritig, B., and Kauffmann, S. 1999. Hydrogen peroxide from the oxidative burst is neither necessary nor sufficient for hypersensitive cell death induction, phenylalanine ammonia lyase stimulation, salicylic acid accumulation, or scopoletin consumption in cultured tobacco cells treated with elicitin. Plant Physiol. 121:163-171.
Dufour, S., Deleu, M., Nott, K., Wathelet, B., Thonart, P., and Paquot, M. 2005. Hemolytic activity of new linear surfactin analogs in relation to their physico-chemical properties. Biochim. Biophys. Acta 1726:87-95.
Duijff, B. J., Gianinazzi-Pearson, V, and Lemanceau, P. 1997. Involvement of the outer membrane lipopolysaccharides in the endophytic colonization of tomato roots by biocontrol Pseudomonas fluorescens strain WCS417r. New Phytol. 135:325-334.
Durrant, W. E., and Dong, X. 2004. Systemic acquired resistance. Annu. Rev. Phytopathol. 42:185-209.
Eeman, M., Berquand, A., Dufrene, Y. E, Paquot, M., Dufour, S., and Deleu, M. 2006. Penetration of surfactin into phospholipid monolayers: Nanoscale interfacial organization. Langmuir 22:11337-11345.
Fedoroff, N. 2006. Redox regulatory mechanisms in cellular stress responses. Ann. Bot. 98:289-300.
Felix, G., Duran, J. D., Volko, S., and Boiler, T. 1999. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18:265-276.
Feussner, I., and Wasternack, C. 2002. The lipoxygenase pathway. Annu. Rev. Plant Biol. 53:275-297.
Fobert, P. R., and Despres, C. 2005. Redox control of systemic acquired resistance. Curr. Opin. Plant. Biol. 8:378-382.
Garcia-Brugger, A., Lamotte, O., Vandelle, E., Bourque, S., Lecourieux, D., Poinssot, B., Wendehenne, D., and Pugin, A. 2006. Early signaling events induced by elicitors of plant defenses. Mol. Plant-Microbe Interact. 19:711-724.
Gómez-Gómez, L. 2004. Plant perception systems for pathogen recognition and defense. Mol. Immunol. 41:1055-1062.
Greenberg, J. T., and Yao, N. 2004. The role and regulation of programmed cell death in plant-pathogen interactions. Cell. Microbiol. 6:201-211.
Haas, D., and Défago, G. 2005. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat. Rev. Microbiol. 3:307-319.
He, P, Shan, L, and Sheen, J. 2007. Elicitation and suppression of microbe-associated molecular pattern-triggered immunity in plant-microbe interactions. Cell Microbiol. 9:1385-1396.
Heath, M. C. 2000. Hypersensitive response-related death. Plant Mol. Biol. 44:321-334.
Heerklotz, H., and Seelig, J. 2007. Leakage and lysis of lipid membranes induced by the lipopeptide surfactin. Eur. Biophys. J. Biophys. Lett. 36:305-314.
Hofemeister, J., Conrad, B., Adler, B., Hofemeister, B., Feesche, J., Kucheryava, N., Steinborn, G., Franke, P., Grammel, N., Zwintscher, A., Leenders, E, Hitzeroth, G., and Vater, J. 2004. Genetic analysis of the biosynthesis of non-ribosomal peptide- and polyketide-like antibiotics, iron uptake and biofilm formation by Bacillus subtilis Al/3. Mol. Genet. Genomics 272:363-378.
Iavicoli, A., Boutet, E., Buchala, A., and Métraux, J. P. 2003. Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Mol. Plant-Microbe Interact. 16:851-858.
Jones, J. D., and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329.
Kawano, T, Pinontoan, R., Uozumi, N., Miyake, C., Asada, K., Kolattukudy, P. E., and 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.
Kim, S. Y, Kim, J. Y, Kim, S. H., Bae, H. J., Yi, H., Yoon, S. H., Koo, B. S., Kwon, M., Cho, J. Y, Lee, C. E., and Hong, S. 2007. Surfactin from Bacillus subtilis displays anti-proliferative effect via apoptosis induction, cell cycle arrest and survival signaling suppression. FEBS (Fed. Eur. Biochem Soc.) Lett. 581:865-871.
Kloepper, J. W., Ryu, C. M., and Zhang, S. A. 2004. Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259-1266.
Koehl, J., Obwald, W, Kohn, H., Elstner E, E, and Heiser, I. 2003. Different responses of two tobacco cultivars and their cell suspense on cultures to quercinin, a novel elicitin from Phytophthora quercina. Plant Physiol. Biochem. 41:261-269.
Kombrink, E., and Schmelzer, E. 2001. The hypersensitive response and its role in local and systemic disease resistance. Eur. J. Plant. Pathol. 107:69-78.
La Camera, S., Gouzerh, G., Dhondt, S., Hoffmann, L., Fritig, B., Legrand, M., and Heitz, T. 2004. Metabolic reprogramming in plant innate immunity: The contributions of phenylpropanoid and oxylipin pathways. Immunol. Rev. 198:267-284.
Leclère, V., Béchet, M., Adam, A., Guez, J. S., Wathelet, B., Ongena, M., Thonart, P., Gancel, R, Chollet-Imbert, M., and Jacques, P. 2005. Mycosubtilin overproduction by Bacillus subtilis BBG100 enhances the organism's antagonistic and biocontrol activities. Appl. Environ. Microbiol. 71:4577-4584.
Lecourieux, D., Raneva, R., and Pugin, A. 2006. Calcium in plant defensesignaling pathways. New Phytol. 171:249-269.
Lee, S., Suh, S., Kim, S., Crain, R. C., Kwak, J. M., Nam, H. G., and Lee, Y. 1997. Systemic elevation of phosphatidic acid and lysophospholipid levels in wounded plants. Plant J. 12:547-556.
Leeman, M., den Ouden, F. M., Van Pelt, J. A., Dirkx, F. P. M., Steijl, H., Bakker, P. H. A. M., and Schippers, B. 1996. Iron availability affects induction of systemic resistance to Fusarium wilt of radish by Pseudomonas fluorescens: Phytopathology 86:149-155.
Maher, E. A., Bate, N. J., Ni, W., Elkind, Y., Dixon, R. A., and Lamb, C. J. 1994. Increased disease susceptibility of transgenic tobacco plants with suppressed levels of preformed phenylpropanoid products. Proc. Natl. Acad. Sci. U.S.A. 91:7802-7806.
Matsui, K. 2006. Green leaf volatiles: Hydroperoxide lyase pathway of oxylipin metabolism. Curr. Opin. Plant. Biol. 9:274-280.
Meziane, H., Van der Sluis, I., Van Loon, L. C., Höfte, M., and Bakker, P. A. H. M. 2005. Determinants of Pseudomonas putida WCS358 involved in inducing systemic resistance in plants. Mol. Plant Pathol. 6:177-185.
Montesano, M., Brader, G., and Palva, E. T. 2003. Pathogen derived elicitors: Searching for receptors in plants. Mol. Plant Pathol. 4:73-79.
Navarez-Vasquez, J., Florin-Christensen, J., and Ryan, C. A. 1999. Positional specificity of a phospholipase a activity induced by wounding, systemin and oligosaccharide elicitors in tomato leaves. Plant Cell 11:2249-2260.
Ongena, M., and Thonart, P. 2006. Resistance induced in plants by nonpathogenic microorganisms: Elicitation and defense responses. Pages 447-463 in: Floriculture, Ornamental and Plant Biotechnology: Advances and Topical Issues, 1st ed. A. Jaime and T. Da Silva, eds. Global Science Books, London.
Ongena, M., Duby, E, Rossignol, E, Fauconnier, M. L., Dommes, J., and Thonart, P. 2004. Stimulation of the lipoxygenase pathway is associated with systemic resistance induced in bean by a nonpathogenic Pseudomonas strain. Mol. Plant-Microbe Interact. 17:1009-1018.
Ongena, M., Jacques, P., Touré, Y, Destain, J., Jabrane, A., and Thonart, P. 2005a. Involvement of fengycin-type lipopeptides in the multifaceted biocontrol potential of Bacillus subtilis. Appl. Microbiol. Biotechnol. 69:29-38.
Ongena, M., Duby, E, Jourdan, E., Beaudry, T., Jadin, V, Dommes, J., and Thonart, P. 2005b. Bacillus subtilis M4 decreases plant susceptibility towards fungal pathogens by increasing host resistance associated with differential gene expression. Appl. Microbiol. Biotechnol. 67:692-698.
Ongena, M., Jourdan, E., Schafer, M., Kech, C., Budzikiewicz, H., Luxen, A., and Thonart, P. 2005c. 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.
Ongena, M., Adam, A., Jourdan, E., Paquot, M., Brans, A., Joris, B., Arpigny, J. L., and Thonart, P. 2007. Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ. Microbiol. 9:1084-1090.
Peypoux, E, Bonmatin, J. M., and Wallach, J. 1999. Recent trends in the biochemistry of surfactin. Appl. Microbiol. Biotechnol. 51:553-563.
Pieterse, C. M. J., Van Pelt, J. A., Van Wees, S. C. M., Ton, J., Leon- Kloosterziel, K. M., Keurentjes, J. J. B., Verhagen, B. W. M., Knoester, M., Van der Sluis, I., Bakker, P. A. H. M., and Van Loon, L. C. 2001. Rhizobacteria-mediated induced systemic resistance: Triggering, signaling and expression. Eur. J. Plant. Pathol. 107:51-61.
Pineros, M. A., and Kochian, L. V 2003. Differences in whole-cell and single-channel ion currents across the plasma membrane of mesophyll cells from two closely related Thlaspi species. Plant Physiol. 131:583- 594.
Prost, I., Dhondt, S., Rothe, G., Vicente, J., Rodriguez, M. J., Kift, N., Carbonne, E, Griffiths, G., Esquerre-Tugaye, M. T, Rosahl, S., Castresana, C., Hamberg, M., and Fournier, J. 2005. Evaluation of the antimicrobial activities of plant oxylipins supports their involvement in defense against pathogens. Plant Physiol. 139:1902-1913.
Pugin, A, Frachisse, J. M., Tavernier, E., Bligny, R., Gout, E., Douce, R., and Guern, J. 1997. Early events induced by the elicitor cryptogein in tobacco cells: Involvement of a plasma membrane NADPH oxidase and activation of glycolysis and the pentose phosphate pathway. Plant Cell 9:2077-2091.
Raaijmakers, J. M., de Bruijn, I., and de Kock, M. J. D. 2006. Cyclic lipopeptide production by plant-associated Pseudomonas spp.: Diversity, activity, biosynthesis, and regulation. Mol. Plant-Microbe Interact. 19:699-710.
Ran, L. X., Li, Z. N., Wu, G. J., Van Loon, L. C., and Bakker, P. A. H. M. 2005. Induction of systemic resistance against bacterial wilt in Eucalyptus urophylla by fluorescent Pseudomonas spp. Eur. J. Plant. Pathol. 113:59-70.
Reitz, M., Oger, P., Meyer, A., Niehaus, K., Farrand, S. K., Hallmann, J., and Sikora, R. A. 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.
Roos, W., Dordschbal, B., Steighardt, J., Hieke, M., Weiss, D., and Saalbach, G. 1999. A redox-dependent, G-protein-coupled phospholipase A of the plasma membrane is involved in the elicitation of alkaloid biosynthesis in Eschscholtzia californica. Biochim. Biophys. Acta 1448:390-402.
Ryu, C. M., Farag, M. A., Hu, C. H., Reddy, M. S., Kloepper, J. W., and Pare, P. W 2004. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol. 134:1017-1026.
Schneider, J., Taraz, K., Budzikiewicz, H., Deleu, M., Thonart, P., and Jacques, P. 1999. The structure of two fengycins from Bacillus subtilis S499. Z. Naturforsch. C: Biosci. 54:859-866.
Schuhegger, R., Ihring, A., Gantner, S., Bahnweg, G., Knappe, C., Vogg, G., Hutzler, P., Schmid, M., Van Breusegem, E, Eberl, L., Hartmann, A., and Langebartels, C. 2006. Induction of systemic resistance in tomato by N-acyl-L-homoserine lactone-producing rhizosphere bacteria. Plant Cell Environ. 29:909-918.
Shah, J. 2005. Lipids, Upases, and lipid-modifying enzymes in plant disease resistance. Annu. Rev. Phytopathol. 43:229-260.
Sharan, M., Taguchi, G., Gonda, K., Jouke, T., Shimosaka, M., Hayashida, N., and Okazaki, M. 1998. Effects of methyl jasmonate and elicitor on the activation of phenylalanine ammonia-lyase and the accumulation of scopoletin and scopolin in tobacco cell cultures. Plant Sci. 132:13-19.
Sheppard, J. D., Jumarie, C., Cooper, D. G., and Laprade, R. 1991. Ionic channels induced by surfactin in planar lipid bilayer membranes. Biochim. Biophys. Acta 1064:13-23.
Siddiqui, I. A., and Shaukat, S. S. 2003. Suppression of root-knot disease by Pseudomonas fluorescens CHA0 in tomato: Importance of bacterial secondary metabolite, 2,4-diacetylpholoroglucinol. Soil Biol. Biochem. 35:1615-1623.
Sticher, L., Mauch-Mani, B., and Métraux, J. P. 1997. Systemic acquired resistance. Annu. Rev. Phytopathol. 35:235-270.
Strobel, N. E., Ji, C., Gopalan, S., Kuc, J. A., and He, S. Y 1996. Induction of systemic acquired resistance in cucumber by Pseudomonas syringae pv. syringae 61 HrpZ(Pss) protein. Plant J. 9:431-439.
Tran, H., Ficke, A., Asiimwe, T., Hofte, M., and Raaijmakers, J. M. 2007. Role of the cyclic lipopeptide massetolide A in biological control of Phytophthora infestans and in colonization of tomato plants by Pseudomonas fluorescens. New Phytol. 175:731-742.
Vanittanakom, N., Loeffler, W, Koch, U., and Jung, G. 1986. Fengycin-A novel antifungal lipopeptide antibiotic produced by Bacillus subtilis F-29-3. J. Antibiot. 39:888-901.
Van Loon, L. C. 2007. Plant responses to plant growth-promoting rhizobacteria. Eur. J. Plant. Pathol. 119:243-254.
Van Loon, L. C., and Bakker, P. A. H. M. 2005. Induced systemic resistance as a mechanism of disease suppression by rhizobacteria. In: PGPR: Biocontrol and Biofertilization. Z. A. Siddiqui, ed. Springer Science, Dordrecht, The Netherlands.
Van Loon, L. C., Bakker, P. A. H. M., and Pieterse, C. M. J. 1998. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36:453-483.
Van Loon, L. C., Rep, M., and Pieterse, C. M. J. 2006. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44:135-162.
Van Wees, S. C. M., Van der Ent, S., and Pieterse, C. M. J. 2008. Plant immune responses triggered by beneficial microbes. Curr. Opin. Plant Biol. 11:443-448.
Youssef, N. H., Duncan, K. E., and Mclnerney, M. J. 2005. Importance of 3-hydroxy fatty acid composition of lipopeptides for biosurfactant activity. Appl. Environ. Microbiol. 71:7690-7695.
Zahir, Z. A., Arshad, M., and Frankenberger, W T. 2004. Plant growth promoting rhizobacteria: Applications and perspectives in agriculture. Adv. Agron. 81:97-168.
Zhao, J., Davis, L. C., and Verpoorte, R. 2005. Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol. Adv. 23:283-333.