Advertisement

European Journal of Plant Pathology

, Volume 118, Issue 1, pp 43–57 | Cite as

Biological control of Botrytis cinerea by selected grapevine-associated bacteria and stimulation of chitinase and β-1,3 glucanase activities under field conditions

  • Maryline Magnin-Robert
  • Patricia Trotel-Aziz
  • Daniel Quantinet
  • Sylvie Biagianti
  • Aziz Aziz
Full Research Paper

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.

Keywords

Biocontrol Grey mould Induced resistance Rhizobacteria Vitis vinifera

Notes

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).

References

  1. 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.PubMedGoogle Scholar
  2. Asaka, O. & Shoda, M. (1996) Biocontrol of Rhizoctonia solani damping off of Tomato with Bacillus subtilis RB14. Applied and Environmental Microbiology, 62, 4081–4085.Google Scholar
  3. 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.PubMedCrossRefGoogle Scholar
  4. 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.Google Scholar
  5. Baker, C. J., Stavely, J. R., & Mock, N. (1985) Biocontrol of bean rust by Bacillus subtilis under field conditions. Plant Disease, 69, 770–772.Google Scholar
  6. 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.Google Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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.CrossRefGoogle Scholar
  9. 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.Google Scholar
  10. 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.PubMedCrossRefGoogle Scholar
  11. 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.Google Scholar
  12. 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.PubMedCrossRefGoogle Scholar
  13. Cook, R. J. (1993) Making greater use of introduced microorganisms for biological control of plant pathogens. Annual Review of Phytopathology, 31, 53–80.CrossRefPubMedGoogle Scholar
  14. 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.CrossRefGoogle Scholar
  15. 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.CrossRefGoogle Scholar
  16. 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.PubMedGoogle Scholar
  17. Dowling, D. N., & O’Gara, F. (1994) Metabolites of Pseudomonas involved in the biocontrol of plant disease. Trends in Biotechnology, 12, 133–141.CrossRefGoogle Scholar
  18. 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.CrossRefGoogle Scholar
  19. Elmer, P. A. G., & Reglinski, T. (2006) Biosuppression of Botrytis cinerea in grapes. Plant Pathology, 55, 155–177.CrossRefGoogle Scholar
  20. 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.CrossRefGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. 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.Google Scholar
  23. 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.Google Scholar
  24. 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.PubMedGoogle Scholar
  25. 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.CrossRefGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. 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.PubMedCrossRefGoogle Scholar
  28. 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.CrossRefGoogle Scholar
  29. 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.CrossRefGoogle Scholar
  30. 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.CrossRefGoogle Scholar
  31. 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.PubMedCrossRefGoogle Scholar
  32. 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.PubMedCrossRefGoogle Scholar
  33. 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.PubMedCrossRefGoogle Scholar
  34. 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.CrossRefGoogle Scholar
  35. 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.CrossRefGoogle Scholar
  36. 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.PubMedGoogle Scholar
  37. 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.PubMedGoogle Scholar
  38. 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.Google Scholar
  39. 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.Google Scholar
  40. 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.CrossRefGoogle Scholar
  41. 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.PubMedCrossRefGoogle Scholar
  42. 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.CrossRefGoogle Scholar
  43. 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.Google Scholar
  44. 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.Google Scholar
  45. Whipps, J. M. (2001) Microbial interactions and biocontrol in the rhizosphere. Journal of Experimental Botany, 52, 487–511.PubMedGoogle Scholar
  46. 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.CrossRefGoogle Scholar
  47. 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.PubMedCrossRefGoogle Scholar

Copyright information

© KNPV 2007

Authors and Affiliations

  • Maryline Magnin-Robert
    • 1
    • 2
  • Patricia Trotel-Aziz
    • 1
    • 2
  • Daniel Quantinet
    • 3
  • Sylvie Biagianti
    • 1
  • Aziz Aziz
    • 1
    • 2
  1. 1.Laboratoire d’Eco-Toxicologie, URVVC—EA 2069Université de ReimsReims cedex 2France
  2. 2.Laboratoire de Plantes, Pesticides et Développement Durable, URVVC—EA 2069Université de ReimsReims cedex 2France
  3. 3.GDV de la MarneInstitut Technique de ChampagneEpernay cedexFrance

Personalised recommendations