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.
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References
Asaka, O, Shoda, M (1996) Biocontrol of Rhizoctonia solani damping-off of tomato with Bacillus subtilis rb14. Appl Environ Microbiol 62: 4081–4085
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
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
Bohman, S, Staal, J, Thomma, BPHJ, Wang, M, Dixelius, C (2004) Characterisation of an Arabidopsis–Leptosphaeria maculans pathosystem: resistance partially requires camalexin biosynthesis and is independent of salicylic acid, ethylene and jasmonic acid signalling. Plant J 37: 9–20
Bostock, RM (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu Rev Phytopathol 43: 545–580
Denison, RF, Kiers, ET (2004) Lifestyle alternatives for rhizobia: mutualism, parasitism, and forgoing symbiosis. FEMS Microbiol Lett 237: 187–193
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
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
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
Handelsman, J, Stabb, EV (1996) Biocontrol of soilborne plant pathogens. Plant Cell 8: 1855–1869
Howlett, BJ, Idnurm, A, Pedras, MSC (2001) Leptosphaeria maculans, the causal agent of blackleg disease of Brassicas. Fungal Genet Biol 33: 1–14
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
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
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
Lindow, SE, Brandl, MT (2003) Microbiology of the Phyllosphere. Appl Environ Microbiol 69: 1875–1883
Lucy, M, Reed, E, Glick, BR (2004) Applications of free living plant growth-promoting rhizobacteria. Antonie Van Leeuwenhoek 86: 1–25
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
Nejad, P, Johnson, PA (2000) Endophytic bacteria induce growth promotion and wilt disease suppression in oilseed rape and tomato. Biol Control 18: 208–215
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
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
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
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
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
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
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
Thomma, BPHJ (2003) Alternaria spp.: from general saprophyte to specific parasite. Mol Plant Pathol 4: 225–236
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
van Loon, LC, Bakker, PAHM, Pieterse, CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36: 453–483
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
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
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
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
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
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
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
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
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.
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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
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DOI: https://doi.org/10.1007/s00248-006-9181-2