Skip to main content
Log in

Protection of Oilseed Rape (Brassica napus) Toward Fungal Pathogens by Strains of Plant-associated Bacillus amyloliquefaciens

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

In this report, four Bacillus strains were tested for effects on plant fitness and disease protection of oilseed rape (Brassica napus). The strains belonged to newly discovered plant-associated Bacillus amyloliquefaciens and a recently proposed species, Bacillus endophyticus. The fungal pathogens tested represented different infection strategies and included Alternaria brassicae, Botrytis cinerea, Leptosphaeria maculans, and Verticillium longisporum. The B. amyloliquefaciens strains showed no or a weak plant growth promoting activity, whereas the B. endophyticus strain had negative effects on the plant as revealed by phenological analysis. On the other hand, two of the B. amyloliquefaciens strains conferred protection of oilseed rape toward all pathogens tested. In vitro experiments studying the effects of Bacillus exudates on fungal growth showed clear growth inhibition in several but not all cases. The protective effects of Bacillus can therefore, at least in part, be explained by production of antibiotic substances, but other mechanisms must also be involved probably as a result of intricate plant–bacteria interaction. The protective effects observed for certain Bacillus strains make them highly interesting for further studies as biocontrol agents in Brassica cultivation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2

Similar content being viewed by others

References

  1. Asaka, O, Shoda, M (1996) Biocontrol of Rhizoctonia solani damping-off of tomato with Bacillus subtilis rb14. Appl Environ Microbiol 62: 4081–4085

    PubMed  CAS  Google Scholar 

  2. 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  PubMed  CAS  Google Scholar 

  3. 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

    PubMed  CAS  Google Scholar 

  4. Bohman, S, Staal, J, Thomma, BPHJ, Wang, M, Dixelius, C (2004) Characterisation of an ArabidopsisLeptosphaeria maculans pathosystem: resistance partially requires camalexin biosynthesis and is independent of salicylic acid, ethylene and jasmonic acid signalling. Plant J 37: 9–20

    Article  PubMed  CAS  Google Scholar 

  5. Bostock, RM (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu Rev Phytopathol 43: 545–580

    Article  PubMed  CAS  Google Scholar 

  6. Denison, RF, Kiers, ET (2004) Lifestyle alternatives for rhizobia: mutualism, parasitism, and forgoing symbiosis. FEMS Microbiol Lett 237: 187–193

    Article  PubMed  CAS  Google Scholar 

  7. Dunn, AK, Klimowicz, AK, Handelsman, J (2003) Use of a promoter trap to identify Bacillus cereus genes regulated by tomato seed exudate and a Rhizosphere resident, Pseudomonas aureofaciens. Appl Environ Microbiol 69: 1197–1205

    Article  PubMed  CAS  Google Scholar 

  8. Garbeva, P, van Veen, JA, van Elsas, JD (2004) Microbial diversity in soil: selection microbial populations by plant and soil type and implications for disease suppressiveness. Annu Rev Phytopathol 42: 243–270

    Article  PubMed  CAS  Google Scholar 

  9. Granér, G, Persson, P, Meijer, J, Alstrom, S (2003) A study on microbial diversity in different cultivars of Brassica napus in relation to its wilt pathogen, Verticillium longisporum. FEMS Microbiol Lett 224: 269–276

    Article  PubMed  Google Scholar 

  10. Handelsman, J, Stabb, EV (1996) Biocontrol of soilborne plant pathogens. Plant Cell 8: 1855–1869

    Article  PubMed  CAS  Google Scholar 

  11. Howlett, BJ, Idnurm, A, Pedras, MSC (2001) Leptosphaeria maculans, the causal agent of blackleg disease of Brassicas. Fungal Genet Biol 33: 1–14

    Article  PubMed  CAS  Google Scholar 

  12. Iavicoli, A, Boutet, E, Buchala, A, Metraux, 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

    Article  PubMed  CAS  Google Scholar 

  13. Idriss, EE, Makarewicz, O, Farouk, A, Rosner, K, Greiner, R, Bochow, H, Richter, T, Borriss, R (2002) Extracellular phytase activity of Bacillus amyloliquefaciens FZB45 contributes to its plant-growth-promoting effect. Microbiol 148: 2097–2109

    CAS  Google Scholar 

  14. Leifert, C, Li, H, Chidburee, S, Hampson, S, Workman, S, Sigee, D, Epton, HAS, Harbour, A (1995) Antibiotic production and biocontrol activity by Bacillus subtilis CL27 and Bacillus pumilus CL45. J Appl Bacteriol 78: 97–108

    PubMed  CAS  Google Scholar 

  15. Lindow, SE, Brandl, MT (2003) Microbiology of the Phyllosphere. Appl Environ Microbiol 69: 1875–1883

    Article  PubMed  CAS  Google Scholar 

  16. Lucy, M, Reed, E, Glick, BR (2004) Applications of free living plant growth-promoting rhizobacteria. Antonie Van Leeuwenhoek 86: 1–25

    Article  PubMed  CAS  Google Scholar 

  17. Marcroft, SJ, Sprague, SJ, Salisbury, PA, Howlett, BJ (2004) Potential for using host resistance to reduce production of pseudothecia and ascospores of Leptosphaeria maculans, the blackleg pathogen of Brassica napus. Plant Pathol 53: 468–474

    Article  Google Scholar 

  18. Nejad, P, Johnson, PA (2000) Endophytic bacteria induce growth promotion and wilt disease suppression in oilseed rape and tomato. Biol Control 18: 208–215

    Article  Google Scholar 

  19. Ongena, M, Duby, F, Jourdan, E, Beaudry, T, Jadin, V, Dommes, J, Thonart, P (2005) Bacillus subtilis M4 decreases plant susceptibility towards fungal pathogens by increasing host resistance associated with differential gene expression. Appl Microbiol Biotechnol 67: 692–698

    Article  PubMed  CAS  Google Scholar 

  20. Reva, ON, Dixelius, C, Meijer, J, Priest, FG (2004) Taxonomic characterization and plant colonizing abilities of some bacteria related to Bacillus amyloliquefaciens and Bacillus subtilis. FEMS Microbiol Ecol 48: 249–259

    Article  CAS  Google Scholar 

  21. Reva, ON, Smirnov, VV, Pettersson, B, Priest, FG (2002) Bacillus endophyticus sp. nov., isolated from the inner tissues of cotton plants (Gossypium sp.). Int J Syst Evol Microbiol 52: 101–107

    PubMed  CAS  Google Scholar 

  22. Risøen, PA, Rønning, P, Hegna, IK, Kolstø, A-B (2004) Characterization of a broad range antimicrobial substance from Bacillus cereus. J Appl Microbiol 96: 648–655

    Article  PubMed  Google Scholar 

  23. Ryu, C-M, Farag, MA, Hu, C-H, Reddy, MS, Wei, H-X, Pare, PW, Kloepper, JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 100: 4927–4932

    Article  PubMed  CAS  Google Scholar 

  24. Ryu, C-M, Murphy, JF, Mysore, KS, Kloepper, JW (2004) Plant growth-promoting rhizobacteria systemically protect Arabidopsis thaliana against Cucumber mosaic virus by a salicylic acid and NPR1-independent and jasmonic acid-dependent signaling pathway. Plant J 39: 381–392

    Article  PubMed  CAS  Google Scholar 

  25. Smith, KP, Handelsman, J, Goodman, RM (1999) Genetic basis in plants for interactions with disease-suppressive bacteria. Proc Natl Acad Sci USA 96: 4786–4790

    Article  PubMed  CAS  Google Scholar 

  26. Thomma, BPHJ (2003) Alternaria spp.: from general saprophyte to specific parasite. Mol Plant Pathol 4: 225–236

    Article  CAS  Google Scholar 

  27. Ton, J, De Vos, M, Robben, C, Buchala, A, Metraux, J-P, Van Loon, LC, Pieterse, CMJ (2002) Characterization of Arabidopsis enhanced disease susceptibility mutants that are affected in systemically induced resistance. Plant J 29: 11–21

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  29. Walker, R, Powell, AA, Seddon, B (1998) Bacillus isolates from the spermosphere of peas and dwarf French beans with antifungal activity against Botrytis cinerea and Pythium species. J Appl Microbiol 84: 791–801

    Article  PubMed  CAS  Google Scholar 

  30. Walker, TS, Bais, HP, Deziel, E, Schweizer, HP, Rahme, LG, Fall, R, Vivanco, JM (2004) Pseudomonas aeruginosa—plant root interactions. pathogenicity, biofilm formation, and root exudation. Plant Physiol 134: 320–331

    Article  PubMed  CAS  Google Scholar 

  31. Whipps, JM (1987) Effect of media on growth and interactions between a range of soilborne glasshouse pathogens and antagonistic fungi. New Phytol 107: 127–142

    Article  Google Scholar 

  32. Wulff, EG, Mguni, CM, Mansfeld-Giese, K, Fels, J, Lubeck, M, Hockenhull, J (2002) Biochemical and molecular characterization of Bacillus amyloliquefaciens, B. subtilisand B. pumilus isolates with distinct antagonistic potential against Xanthomonas campestris pv. campestris. Plant Pathol 51: 574–584

    Article  CAS  Google Scholar 

  33. Wulff, EG, Mguni, CM, Mortensen, CN, Keswani, CL, Hockenhull, J (2002) Biological control of black rot (Xanthomonas campestris pv. campestris) of Brassicas with an antagonistic strain of Bacillus subtilis in Zimbabwe. Eur J Plant Pathol 108: 317–325

    Article  Google Scholar 

  34. Yu, GY, Sinclair, JB, Hartman, GL, Bertagnolli, BL (2002) Production of iturin A by Bacillus amyloliquefaciens suppressing Rhizoctonia solani. Soil Biol Biochem 34: 955–963

    Article  CAS  Google Scholar 

  35. Zehnder, G, Kloepper, J, Tuzun, S, Yao, C, Wei, G, Chambliss, O, Shelby, R (1997) Insect feeding on cucumber mediated by rhizobacteria-induced plant resistance. Entomol Exp Appl 83: 81–85

    Article  Google Scholar 

  36. Zehnder, GW, Yao, C, 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

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by grants from SLU-IMOP, Helge Ax:son Johnsons Stiftelse and Stiftelsen Oscar och Lili Lamms minne. We are grateful to Prof. Christina Dixelius and Gunilla Swärdh for provision of fungal strains and advice on cultivation and to Prof. Christina Dixelius for comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jesper Danielsson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Danielsson, J., Reva, O. & Meijer, J. Protection of Oilseed Rape (Brassica napus) Toward Fungal Pathogens by Strains of Plant-associated Bacillus amyloliquefaciens . Microb Ecol 54, 134–140 (2007). https://doi.org/10.1007/s00248-006-9181-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-006-9181-2

Keywords

Navigation