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Involvement of fengycin-type lipopeptides in the multifaceted biocontrol potential of Bacillus subtilis

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Abstract

In this work, the potential of Bacillus subtilis strain M4 at protecting plants against fungal diseases was demonstrated in different pathosystems. We provide evidence for the role of secreted lipopeptides, and more particularly of fengycins, in the protective effect afforded by the strain against damping-off of bean seedlings caused by Pythium ultimum and against gray mold of apple in post-harvest disease. This role was demonstrated by the strong biocontrol activity of lipopeptide-enriched extracts and through the detection of inhibitory quantities of fengycins in infected tissues. Beside such a direct antagonism of the pathogen, we show that root pre-inoculation with M4 enabled the host plant to react more efficiently to subsequent pathogen infection on leaves. Fengycins could also be involved in this systemic resistance-eliciting effect of strain M4, as these molecules may induce the synthesis of plant phenolics involved in or derived from the defense-related phenylpropanoid metabolism. Much remains to be discovered about the mechanisms by which Bacillus spp suppress disease. Through this study on strain M4, we reinforce the interest in B. subtilis as a pathogen antagonist and plant defense-inducing agent. The secretion of cyclic fengycin-type lipopeptides may be tightly related to the expression of these two biocontrol traits.

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References

  • Akpa E, Jacques P, Wathelet B, Paquot M, Fuchs R, Budzikiewicz H, Thonart P (2001) Influence of culture conditions on lipopeptide production by Bacillus subtilis. Appl Biochem Biotechnol 91:551–561

    Article  PubMed  Google Scholar 

  • Asaka O, Shoda M (1996) Biocontrol of Rhizoctonia solani damping-off of tomato with Bacillus subtilis RB14. Appl Environ Microbiol 62:4081–4085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 Physiol 134:307–319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benhamou N, Kloepper JW, Quadt-Hallman A, Tuzun S (1996) Induction of defense-related ultrastructural modifications in pea root tissues inoculated with endophytic bacteria. Plant Physiol 112:919–929

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bostock RM, Schaeffer DA (1986) Comparison of elicitor activities of arachidonic acid, fatty acids and glucans from Phytophthora infestans in hypersensitivity expression in potato tuber. Physiol Mol Plant Pathol 29:349–360

    CAS  Google Scholar 

  • Choi D, Bostock RM, Avdiushko S, Hildebrand DF (1994) Lipid-derived signals that discriminate wound- and pathogen-reponsive isoprenoid pathways in plants: methyl jasmonate and the fungal elicitor arachidonic acid induce different 3-hydroxy-3-methylglutaryl-coenzyme A reductase genes and antimicrobial isoprenoids in Solanum tuberosum L. Proc Natl Acad Sci USA 91:2329–2333

    CAS  PubMed  PubMed Central  Google Scholar 

  • De Boer M, Born P, Kindt F, Keurentjes JJB, Sluis I van der, Loon LC van, Bakker PAHM (2003) Control of Fusarium wilt of radish by combining Pseudomonas putida strains that have different disease-suppressive mechanisms. Phytopathology 93:626–632

    PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MSS, Wang LJ (2002) The phenylpropanoid pathway and plant defence—a genomics perspective. Mol Plant Pathol 3:371–390

    CAS  PubMed  Google Scholar 

  • Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209

    CAS  PubMed  Google Scholar 

  • Emmert EAB, Handelsman J (1999) Biocontrol of plant disease: a (Gram-) positive perspective. FEMS Microbiol Lett 171:1–9

    CAS  PubMed  Google Scholar 

  • Guetsky R, Shtienberg D, Elad Y, Fischer E, Dinoor A (2002) Improving biological control by combining biocontrol agents each with several mechanisms of disease suppression. Phytopathology 92:976–985

    PubMed  Google Scholar 

  • Hammerschmidt R (1999) Induced disease resistance: how do induced plants stop pathogens? Physiol Mol Plant Pathol 55:77–84

    CAS  Google Scholar 

  • Harborne JB (1999) The comparative biochemistry of phytoalexin induction in plants. Biochem Syst Ecol 27:335–367

    CAS  Google Scholar 

  • Hbid C (1996) Contribution à l’étude de la relation entre la structure des lipopeptides de Bacillus subtilis et leurs activités hémolytique et antifongique. PhD thesis, University of Liège, Liège

  • Henfling JWDM, Kùc J (1979) A semi-micro method for the quantitation of sesquiterpenoid stress metabolites in potato tuber tissue. Phytopathology 69:609–612

    CAS  Google Scholar 

  • Hofemeister J, Conrad B, Adler B, Hofemeister B, Feesche J, Kucheryava N, Steinborn G, Franke P, Grammel N, Zwintscher A, Leenders F, Hitzeroth G, Vater J (2004) Genetic analysis of the biosynthesis of non-ribosomal peptide- and polyketide-like antibiotics, iron uptake and biofilm formation by Bacillus subtilis A1/3. Mol Genet Genomics 272:363–378

    CAS  PubMed  Google Scholar 

  • Jacques P, Hbid C, Destain J, Razafindralambo H, Paquot M, De Pauw E, Thonart P (1999) Optimization of biosurfactant lipopeptide production from Bacillus subtilis S499 by Plackett–Burman design. Appl Biochem Biotechnol 77:223–233

    Google Scholar 

  • Janisiewicz WJ, Korsten L (2002) Biological control of post-harvest diseases of fruits. Annu Rev Phytopathol 40:411–441

    CAS  PubMed  Google Scholar 

  • Kloepper JW, Tuzun S, Kùc JA (1992) Proposed definitions related to induced disease resistance. Biocontrol Sci Technol 2:349–351

    Google Scholar 

  • Kloepper JW, Ryu CM, Zhang SA (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266

    CAS  PubMed  Google Scholar 

  • Leeman M, Pelt JA van, Ouden FM den, 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

    CAS  Google Scholar 

  • Leenders F, Stein TH, Kablitz B, Franke P, Vater J (1999) Rapid typing of Bacillus subtilis strains by their secondary metabolites using matrix-assisted laser desorption/ionization mass spectrometry of intact cells. Rapid Commun Mass Spectrom 13:943–949

    CAS  Google Scholar 

  • Loeffler W, Tschen JSM, Vanittanakom N, Kugler M, Knorpp E, Hsieh TF, Wu TG (1986) Antifungal effects of bacilysin and fengymycin from Bacillus subtilis F-29-3. A comparison with activities of other Bacillus antibiotics. J Phytopathol 115:204–213

    CAS  Google Scholar 

  • Maget-Dana R, Thimon L, Peypoux F, Ptack M (1992) Surfactin/Iturin A interactions may explain the synergistic effect of surfactin on the biological properties of iturin A. Biochimie 74:1047–1051

    CAS  PubMed  Google Scholar 

  • Maher EA, Bate NJ, Ni W, Elkind Y, Dixon RA, Lamb CJ (1994) Increased disease susceptibility of transgenic tobacco plants with suppressed levels of preformed phenylpropanold products. Proc Natl Acad Sci USA 91:7802–7806

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Ongena M, Duby F, Jourdan E, Beaudry T, Jadin V, Dommes J, Thonart P (2004) Bacillus subtilis M4 decreases plant susceptibility towards fungal pathogens by increasing host resistance associated with differential gene expression. Appl Microbiol Biotechnol DOI https://doi.org/10.1007/s00253-004-1741-0

    Google Scholar 

  • Persello-Cartieaux F, Nussaume L, Robaglia C (2003) Tales from the underground: molecular plant–rhizobacteria interactions. Plant Cell Environ 26:189–199

    CAS  Google Scholar 

  • Peypoux F, Guimand M, Michel G, Delcambe L, Das BC, Lederec E (1978) Structure of iturin A, a peptidolipid antibiotic from Bacillus subtilis. Biochemistry 17:3992–3996

    CAS  PubMed  Google Scholar 

  • Peypoux F, Bonmatin JM, Wallach J (1999) Recent trends in the biochemistry of surfactin. Appl Microbiol Biotechnol 51:553–563

    CAS  PubMed  Google Scholar 

  • Phae CG, Shoda M, Kubota H (1990) Suppressive effect of Bacillus subtilis and its products on phytopathogenic microorganisms. J Ferment Bioeng 69:1–7

    CAS  Google Scholar 

  • Raaijmakers JM, Leeman M, Oorschot MMP van, Sluis I van der, Schippers B, Bakker PAHM (1995) Dose–response relationships in biological control of Fusarium wilt of radish by Pseudomonas spp. Phytopathology 85:1075–1081

    Google Scholar 

  • Raupach GS, Kloepper JW (1998) Mixtures of plant growth-promoting rhizobacteria enhance biological control of multiple cucumber pathogens. Phytopathology 88:1158–1164

    CAS  PubMed  Google Scholar 

  • Raupach GS, Kloepper JW (2000) Biocontrol of cucumber diseases in the field by plant growth-promoting rhizobacteria with and without methyl bromide fumigation. Plant Dis 84:1073–1075

    CAS  PubMed  Google Scholar 

  • Razafindralambo H, Paquot M, Hbid C, Jacques P, Destain J, Thonart P (1993) Purification of antifungal lipopeptides by reserved-phase high performance liquid chromatography. J Chromatogr A 639:81–85

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Ryu CM, Hu CH, Reddy MS, Kloepper JW (2003) Different signaling pathways of induced resistance by rhizobacteria in Arabidopsis thaliana against two pathovars of Pseudomonas syringae. New Phytol 160:413–420

    CAS  PubMed  Google Scholar 

  • Schneider J, Taraz K, Budzikiewicz H, Deleu M, Thonart P, Jacques P (1999) The structure of two fengycins from Bacillus subtilis S499. Z Naturforsch 54:859–866

    CAS  Google Scholar 

  • Shoda M (2000) Bacterial control of plant diseases. J Biosci Bioeng 89:515–521

    CAS  PubMed  Google Scholar 

  • Vanittanakom N, Loeffler W, Koch U, Jung G (1986) Fengycin—a novel antifungal lipopeptide antibiotic produced by Bacillus subtilis F-29-3. J Antibiot 39:888–901

    CAS  Google Scholar 

  • Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483

    PubMed  Google Scholar 

  • Walsh UF, Morrissey JP, O’Gara F (2001) Pseudomonas for biocontrol of phytopathogens: from functional genomics to commercial exploitation. Curr Opin Biotechnol 12:289–295

    CAS  PubMed  Google Scholar 

  • Warrior P, Konduru K, Vasudevan P (2002) Formulation of biological control agents for pest and disease management. In: Gnanamanickam SS (ed) Biological control of crop diseases. Dekker, New York, pp 421–442

    Google Scholar 

  • Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Zahir ZA, Arshad M, Frankenberger WT (2004) Plant growth promoting rhizobacteria: applications and perspectives in agriculture. Adv Agron 81:97–168

    CAS  Google Scholar 

  • Zehnder GW, Yao CB, Murphy JF, Sikora ER, Kloepper JW (2000) Induction of resistance in tomato against cucumber mosaic cucumovirus by plant growth-promoting rhizobacteria. BioControl 45:127–137

    Google Scholar 

  • Zhang S, Reddy MS, Kloepper JW (2004) Tobacco growth enhancement and blue mold disease protection by rhizobacteria: relationship between plant growth promotion and systemic disease protection by PGPR strain 90-166. Plant Soil 262:277–288

    CAS  Google Scholar 

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Acknowledgements

This work was partly financed by the AGROSTAR s.a. company and by a grant from the Walloon Region of Belgium (program AV BIOVAL 3847). It also received support from the National Funds for Scientific Research (FNRS, Belgium; Program FRFC 2.4.570.00).

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Correspondence to Marc Ongena.

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Ongena, M., Jacques, P., Touré, Y. et al. Involvement of fengycin-type lipopeptides in the multifaceted biocontrol potential of Bacillus subtilis . Appl Microbiol Biotechnol 69, 29–38 (2005). https://doi.org/10.1007/s00253-005-1940-3

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