Abstract
In this study, the biocontrol ability of seven grapevine-associated bacteria, previously reported as efficient against Botrytis cinerea under in vitro conditions, was evaluated in two vineyard orchards with the susceptible cv. Chardonnay during four consecutive years (2002–2005). It was shown that the severity of disease on grapevine leaves and berries was reduced to different levels, depending on the bacterial strain and inoculation method. Drenching the plant soil with these bacteria revealed a systemic resistance to B. cinerea, even without renewal of treatment. Accordingly, this resistance was associated with a stimulation of some plant defense responses such as chitinase and β-1,3-glucanase activities in both leaves and berries. In leaves, chitinase activity increased before veraison (end-July) while β-1,3-glucanase reached its maximum activity at ripening (September). Reverse patterns were observed in berries, with β-1,3-glucanase peaking at full veraison (end-August) and chitinase at a later development stage. Highest activities were observed with Acinetobacter lwoffii PTA-113 and Pseudomonas fluorescens PTA-CT2 in leaves, and with A. lwoffii PTA-113 and Pantoea agglomerans PTA-AF1 in berries. These results have demonstrated an induced protection of grapevine against B. cinerea by selected bacteria under field conditions, and suggest that induced resistance could be related to a stimulation of plant defense reactions in a successive manner.
Similar content being viewed by others
References
Amellal, N., Burtin, G., Bartoli, F., & Heulin, T. (1998) Colonization of wheat roots by an exopolysaccharide-producing Pantoea agglomerans strain and its effect on rhizosphere soil aggregation. Applied and Environmental Microbiology, 64, 3740–3747.
Asaka, O. & Shoda, M. (1996) Biocontrol of Rhizoctonia solani damping off of Tomato with Bacillus subtilis RB14. Applied and Environmental Microbiology, 62, 4081–4085.
Aziz, A., Heyraud, A., & Lambert, B. (2004) Oligogalacturonide signal transduction, induction of defence related responses and protection of grapevine against Botrytis cinerea. Planta, 218, 767–774.
Aziz, A., Poinssot, B., Daire, X., Adrian, M., Bézier, A., Lambert, B., Joubert, J. M., & Pugin, A. (2003) Laminarin elicits defence responses in grapevine and induces protection against Botrytis cinerea and Plasmopara viticola. Molecular Plant-Microbe Interaction, 16, 1118–1128.
Baker, C. J., Stavely, J. R., & Mock, N. (1985) Biocontrol of bean rust by Bacillus subtilis under field conditions. Plant Disease, 69, 770–772.
Bargabus, R. L., Zidack, N. K., Sherwood, J. E., & Jacobsen, B. J. (2003) Oxidative burst elicited by Bacillus lycoides isolate Bac J, a biological control agent, occurs independently of hypersensitive cell death in sugar beet. Molecular Plant-Microbe Interaction, 16, 1145–1153.
Barka, E. A., Gognies, S., Nowak, J., Audran, J. C., & Belarbi, A. (2002) Inhibitory effect of endophyte bacteria on Botrytis cinerea and its influence to promote the grapevine growth. Biological Control, 24, 135–142.
Bézier, A., Lambert, B., & Baillieul, F. (2002) Study of defense-related gene expression in grapevine leaves and berries infected with Botrytis cinerea. European Journal of Plant Pathology, 108, 111–120.
Bonomelli, A., Mercier, L., Franchel, J., Baillieul, F., Benizri, E., & Mauro, M. C. (2004) Response of grapevine defenses to UV-C exposure. American Journal of Enology and Viticulture, 55, 51–59.
Busam, G., Kassemeyer, H. H., & Matern, U. (1997) Differential expression of chitinases in Vitis vinifera L. responding to systemic acquired resistance activators or fungal challenge. Plant Physiology, 115, 1029–1038.
Chanway, C. P. (2002) Plant growth promotion by Bacillus and relatives. In: R. Berkeley, M. Heyndrickx, N. Logan & P. De Vos (Eds.) B. subtilis for biocontrol in variety of plants (pp. 219–235). Malden, MA: Blackwell Publishing.
Compant, S., Reiter, B., Sessitsch, A., Nowak, J., Clement, C., & Aït Barka, E. (2005) Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Applied and Environmental Microbiology, 71, 1685–1693.
Cook, R. J. (1993) Making greater use of introduced microorganisms for biological control of plant pathogens. Annual Review of Phytopathology, 31, 53–80.
Coutos-Thévenot, P., Poinssot, B., Bonomelli, A., Yean, H., Breda, C., Buffard, D., et al. (2001). In vitro tolerance to Botrytis cinerea of grapevine 41B rootstock in transgenic plants expressing the stilbene synthase Vst1 gene under the control of a pathogen-inducible PR10 promoter. Journal of Experimental Botany, 358, 901–910.
Derckel, J. P., Audran, J. C., Haye, B., Lambert, B., & Legendre, L. (1998) Characterization, induction by wounding and salicylic acid, and activity against Botrytis cinerea of chitinases and β-1,3-glucanases of ripening grape berries. Physiologia Plantarum, 104, 56–64.
Derckel, J. P., Baillieul, F., Manteau, S., Audran, J. C., Haye, B., Lambert, B., & Legendre, L. (1999) Differential induction of grapevine defenses by two strains of Botrytis cinerea. Phytopathology, 89, 197–203.
Dowling, D. N., & O’Gara, F. (1994) Metabolites of Pseudomonas involved in the biocontrol of plant disease. Trends in Biotechnology, 12, 133–141.
Duijff, B. J., 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 Phytologist, 135, 325–334.
Elmer, P. A. G., & Reglinski, T. (2006) Biosuppression of Botrytis cinerea in grapes. Plant Pathology, 55, 155–177.
Giannakis, C., Bucheli, C. S., Skene, K. G. M., Robinson, S. P., & Scott, S. N. (1998) Chitinase and ß-1,3-glucanase in grapevine leaves: A possible defense against powdery mildew infection. Australian Journal of Grape Wine Research, 4, 14–22.
Hoffland, E., Pieterse, C. M. J., Bik, L., & van Pelt, J. A. (1995) Induced systemic resistance in radish is not associated with accumulation of pathogenesis-related proteins. Physiological and Molecular Plant Pathology, 46, 309–320.
Holz, G., Gütschow, M., Coertze, S., & Calitz, F. J. (2003) Occurrence of Botrytis cinerea and subsequent disease expression at different positions on leaves and Bunches of grape. Plant Disease, 87, 351–358.
Iavicoli, A., Boutet, E., Buchala, A., & Métraux, J. P. (2003) Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Molecular Plant-Microbe Interaction, 16, 851–858.
Landa, B. B., Navas-Cortés, J. A., Hervas, A., & Jiménez-Diaz, R. M. (2001) Influence of temperature and inoculum density of Fusarium oxysporum f.sp. ciceris on suppression of fusarium wilt of chickpea by rhizosphere bacteria. Phytopathology, 91, 807–816.
Leeman, M., van Pelt, J. A., den Ouden, F. M., Heinsbroek, M., Bakker, P. A. H. M., & Schippers, B. (1995) Induction of systemic resistance by Pseudomonas fluorescens in radish cultivars differing in susceptibility to fusarium wilt, using a novel bioassay. European Journal of Plant Pathology, 101, 655–664.
Leroux, P., Chapeland, F., Desbrosses, D., & Gredt, M. (1999) Patterns of cross-resistance to fungicides in Botryotinia fuckeliana (Botrytis cinerea) isolates from French vineyards. Crop Protection, 18, 687–697.
Mauch, F., Mauch-Mani, B., & Boller, T. (1988) Antifungal hydrolases in pea tissue: II. Inhibition of fungal growth by combinations of chitinase and ß-1,3-glucanase. Plant Physiology, 88, 936–942.
Maurhofer, M., Hase, C., Meuwly, P., Métraux, J. P., & Defago, G. (1994) Induction of systemic resistance of tobacco necrosis virus by the root-colonizing Pseudomonas fluorescens strain CHA0: Influence of the gacA gene and of pyoverdine production. Phytopathology, 84, 139–146.
Mazzola, M., Stahlman, P. W., & Leach, J. E. (1995) Application method affects the distribution and efficacy of rhizobacteria suppressive of downy brome (Bromus tectorum). Soil Biology and Biochemistry, 27, 1271–1278.
Meziane, H., van der Sluis, I., van Loon, L. C., Höfte, M., & Bakker, P. A. H. (2005) Determinants of Pseudomonas putida WCS358 involved in inducing systemic resistance in plants. Molecular Plant Pathology, 6, 177–185.
Montero, C., Cristescu, S. M., Jiménez, J. B., Orea, J. M., Lintel Hekkert, S. T., Harren, F. J. M., & Gonzalez, U. A. (2003) Trans-resveratrol and grape resistance. A dynamic study by high-resolution laser-based techniques. Plant Physiology, 131, 129–138.
Pieterse, C. M. J., van Wees, S. C. M., Hoffland, E., van Pelt, J. A., & van Loon, L. C. (1996) Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salycilic acid accumulation and pathogenesis-related gene expression. The Plant Cell, 8, 1225–1237.
Pieterse, C. M. J., van Wees, S. C. M., van Pelt, J. A., Knoester, M., Laan, R., Gerrits, H., Weisbeek, P. J., & van Loon, L. C. (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. The Plant Cell, 10, 1571–1580.
Raaijmakers, J. M., Leeman, M., van Oorschot, M. M. P., van der Sluis, I., Schippers, B., & Bakker, P. A. H. M. (1995) Dose-response relationships in biological control of Fusarium wilt of radish by Pseudomonas spp. Phytopathology, 85, 1075–1081.
Robert, N., Roche, K., Lebeau, Y., Breda, C., Boulay, M., Esnault, R., & Buffard, D. (2002) Expression of grapevine chitinase genes in berries and leaves infected by fungal or bacterial pathogens. Plant Science, 162, 389–400.
Schmidt, C. S., Agostini, F., Killham, K. K., & Mullins, C. E. (2004) Influence of soil temperature and matric potential on sugar beet seedling colonization and suppression of Pythium damping-off by the antagonistic bacteria Pseudomonas fluorescens and Bacillus subtilis. Phytopathology, 94, 351–363.
Stockwell, V. O., Johnson, K. B., Sugar, D., & Loper, J. E. (2002) Antibiosis contributes to biological control of fire blight by Pantoea agglomerans strain Eh252 in orchards. Phytopathology, 92, 1202–1209.
Tjamos, S. E., Flemetakis, E., Paplomatas, E. J., & Katinakis, P. (2005) Induction of resistance to Verticillium dahliae in Arabidopsis thaliana by the biocontrol agent K-165 and pathogenesis-related proteins gene expression. Molecular Plant-Microbe Interaction, 18, 555–561.
Trotel-Aziz, P., Aziz, A., Magnin-Robert, M., Aït Barka, E., & Gogniès, S. (2006a) Bactéries présentant une activité protectrice de la vigne contre Botrytis cinerea. French patent 06.06.513.
Trotel-Aziz, P., Couderchet, M., Vernet, G., & Aziz, A. (2006b) Chitosan stimulates defense reactions in grapevine leaves and inhibits development of Botrytis cinerea. European Journal of Plant Pathology, 114, 405–413.
van Loon, L. C., Bakker, P. A. H., & Pieterse, C. M. J. (1998) Systemic resistance induced by rhizosphere bacteria. Annual Review of Phytopathology, 36, 453–483.
van Loon, L. C., & van Strien, E. A. (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiological and Molecular Plant Pathology, 55, 85–97.
van Peer, R., Niemann, G. J., & Schippers, B. (1991) Induced resistance and phytoalexin accumulation in biological control of fusarium wilt of carnation by Pseudomonas sp. Strain WCS417r. Phytopathology, 81, 728–734.
van Wees, S. C. M., Pieterse, C. M. J., Trijssenaar, A., van’t Westende, Y. A. M., Hartog, F., & van Loon, L. C. (1997) Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria. Molecular Plant-Microbe Interaction, 10, 716–724.
Whipps, J. M. (2001) Microbial interactions and biocontrol in the rhizosphere. Journal of Experimental Botany, 52, 487–511.
Wirth, S. J., & Wolf, A. G. (1992) Microplate colorimetric assay for andoacting cellulase, xylanase, chitinase, ß-1,3-glucanase and amylase extracted from forest soil horizons. Soil Biology and Biochemistry, 24, 511–519.
Wright, S. A. I., Zumoff, C. H., Schneider, L., & Beer, S. V. (2001) Pantoea agglomerans strain Eh318 produces two antibiotics that inhibit Erwinia amylovora in vitro. Applied and Environmental Microbiology, 67, 284–292.
Acknowledgements
We thank A. Conreux for her technical assistance and the GDV members for their help with disease evaluation in vineyards. We also gratefully acknowledge financial support from Europôl’Agro (Reims-France).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Magnin-Robert, M., Trotel-Aziz, P., Quantinet, D. et al. Biological control of Botrytis cinerea by selected grapevine-associated bacteria and stimulation of chitinase and β-1,3 glucanase activities under field conditions. Eur J Plant Pathol 118, 43–57 (2007). https://doi.org/10.1007/s10658-007-9111-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-007-9111-2