Pseudomonas spp.-induced systemic resistance to Botrytis cinerea is associated with induction and priming of defence responses in grapevine

Journal of Experimental Botany

Volumn 61, Issue 1, 2010, Pages 249-260

  Verhagen, Bas W M ^a   Trotel Aziz, Patricia ^a   Couderchet, Michel ^a   Höfte, Monica ^b   Aziz, Aziz ^a,c  

^a UNIVERSITÉ DE REIMS CHAMPAGNE ARDENNE   (France)

^b GHENT UNIVERSITY   (Belgium)

^c Ministry for Primary Industries   (New Zealand)

Author keywords

Induced resistance; Oxidative burst; Phytoalexins; Priming; Pseudomonas spp.; Rhizobacteria; Siderophores; Vitis vinifera

Indexed keywords

PHYTOALEXINS; REACTIVE OXYGEN METABOLITE; TERPENE;

ARTICLE; BOTRYTIS; CULTURE MEDIUM; CYTOLOGY; GRAPE; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; MICROBIOLOGY; OXIDATIVE STRESS; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PLANT ROOT; PSEUDOMONAS; RHIZOBIUM;

BOTRYTIS; CULTURE MEDIA; IMMUNITY, INNATE; OXIDATIVE STRESS; PLANT DISEASES; PLANT LEAVES; PLANT ROOTS; PSEUDOMONAS; REACTIVE OXYGEN SPECIES; RHIZOBIUM; TERPENES; VITIS;

BACTERIA (MICROORGANISMS); BOTRYOTINIA FUCKELIANA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS FLUORESCENS; PSEUDOMONAS PUTIDA; RHIZOBIALES; VITACEAE; VITIS; VITIS VINIFERA;

EID: 72049109752     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erp295     Document Type: Article

References (55)

1. Audenaert K, Pattery T, Cornelis P, Hofte M. 2002. Induction of systemic resistance to Botrytis cinerea in tomato by Pseudomonas aeruginosa 7NSK2: role of salicylic acid, pyochelin, and pyocyanin. Molecular Plant-Microbe Interactions 15, 1147-1156.
2. Aziz A, Gauthier A, Bézier A, Poinssot B, Joubert JM, Pugin A, Heyraud A, Baillieul F. 2007. Elicitor and resistance-inducing activities of b-1,4 cellodextrins in grapevine, comparison with b-1,3 glucans and a-1,4 oligogalacturonides. Journal of Experimental Botany 58, 1463-1472.
3. Aziz A, Heyraud A, Lambert B. 2004. Oligogalacturonide signal transduction, induction of defense-related responses and protection of grapevine against Botrytis cinerea. Planta 218, 767-774.
4. Aziz A, Poinssot B, Daire X, Adrian M, Bézier A, Lambert B, Joubert JM, Pugin A. 2003. Laminarin elicits defense responses in grapevine and induces protection against Botrytis cinerea and Plasmopara viticola. Molecular Plant-Microbe Interactions 16, 1118-1128.
5. Aziz A, Trotel-Aziz P, Dhuicq L, Jeandet P, Couderchet M, Vernet G. 2006. Chitosan oligomers and copper sulfate induce grapevine defense reactions and resistance to gray mold and downy mildew. Phytopathology 96, 1188-1194.
6. Bakker PAHM, Pieterse CMJ, Van Loon LC. 2007. Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97, 239-243.
7. 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.
8. Busam G, Kassemeyer HH, Matern U. 1997. Differential expression of chitinase in Vitis vinifera L. responding to systemic acquired resistance activators or fungal challenge. Plant Physiology 115, 1029-1038.
9. Chen C, Bélanger RR, Benhamou N, Paulitz TC. 2000. Defense enzymes induced in cucumber roots by treatment with plant growth-promoting rhizobacteria (PGPR) and Pythium aphanidermatum. Physiological and Molecular Plant Pathology 56, 13-23.
10. 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.
11. Conrath U, Pieterse CMJ, Mauch-Mani B. 2002. Priming in plant-pathogen interactions. Trends in Plant Science 7, 210-216.
12. Coutos-Thevenot P, Poinssot B, Bonomelli A, Yean H, Breda C, Buffard D, Esnault R, Hain R, Boulay M. 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 PR 10 promoter. Journal of Experimental Botany 52, 901-910.
13. Delaunois B, Cordelier S, Conreux A, Clément C, Jeandet P. 2009. Molecular engineering of resveratrol in plants. Plant Biotechnology Journal 7, 2-12.
14. De Meyer G, Audenaert K, Hö fte M. 1999. Pseudomonas aeruginosa 7NSK2-induced systemic resistance in tobacco depends on in planta salicylic acid accumulation, but is not associated with PR-1a expression. European Journal of Plant Pathology 105, 513-517.
15. De Meyer G, Hö fte 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.
16. De Vleesschauwer D, Cornelis P, Hö fte M. 2006. Redox-active pyocyanin secreted by Pseudomonas aeruginosa 7NSK2 triggers systemic resistance to Magnaporthe grisea but enhances Rhizoctonia solani susceptibility in rice. Molecular Plant-Microbe Interactions 19, 1406-1419.
17. De Vleesschauwer D, Djavaheri M, Bakker PAHM, Höfte M. 2008. Pseudomonas fluorescens WCS374r-induced resistance in rice against Magnaporthe oryzae is based on pseudobactin-mediated priming for a salicylic acid-repressible multifaceted defense response. Plant Physiology 148, 1996-2012.
18. Duijff BJ, Gianinazzi-Pearson V, Lemanceau P. 1997. Involvement of the outer membrane lipopolysaccharides in the endophytic colonization of tomato roots by biocontrol Pseudomonas fluorescens strain WCS417r. New Phytologist 135, 325-334.
19. Geels FP, Schippers B. 1983. Selection of antagonistic fluorescent Pseudomonas spp. and their root colonization and persistence following treatment of seed potatoes. Phytopathologisches Zeitschrift 108, 193-206.
20. Hamiduzzaman MM, Jakab G, Barnavon L, Neuhaus JM, Mauch-Mani B. 2005. b-Aminobutyric acid-induced resistance against downy mildew in grapevine acts through the potentiation of callose formation and jasmonic acid signalling. Molecular Plant-Microbe Interactions 18, 819-829
21. Hö fte M, Buysens S, Koedam N, Cornelis P. 1993. Zinc affects siderophore-mediated high affinity iron uptake systems in the rhizosphere Pseudomonas aeruginosa 7NSK2. Biometals 6, 85-91.
22. Iavicoli A, Boutet E, Buchala A, Metraux JP. 2003. Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Molecular Plant-Microbe Interactions 16, 851-858.
23. Iswandi A, Bossier P, Vandenabeele J, Verstraete W. 1987. Effect of seed inoculation with the rhizopseudomonas strain 7NSK2 on the root microbiota of maize (Zea mays) and barley (Hordeum vulgare). Biology and Fertility of Soils 3, 153-158.
24. Jeandet P, Douillet-Breuil AC, Bessis R, Debord S, Sbaghi M, Adrian M. 2002. Phytoalexins from the Vitaceae: biosynthesis, phytoalexin gene expression in transgenic plants, antifungal activity, and metabolism. Journal of Agricultural and Food Chemistry 50, 2731-2741.
25. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444, 323-329.
26. King EO, Ward MK, Raney DE. 1954. Two simple media for the demonstration of phycocyanin and fluorescin. Journal of Laboratory and Clinical Medicine 44, 301-307.
27. Lamb C, Dixon RA. 1997. The oxidative burst in plant disease resistance. Annual Review of Plant Physiology and Plant Molecular Biology 48, 251-275.
28. Lamers JG, Schippers B, Geels FP. 1988. Soil-borne disease of wheat in the Netherlands and results of seed bacterization with pseudomonads against Gaeumannomyces graminis var. tritici, associated with disease resistance. In: Jorna ML, Slootmaker LAJ, eds. Cereal breeding related to integrated cereal production. Pudoc, Wageningen, The Netherlands 134-139.
29. Langcake P. 1981. Disease resistance of Vitis spp. and the production of the stress metabolites resveratrol, epsilon-viniferin, alpha-viniferin and pterostilbene. Physiological and Plant Pathology 18, 213-226.
30. Leeman M, Van Pelt JA, Den Ouden FM, Heinsbroek M, Bakker PAHM, Schippers B. 1995. Induction of systemic resistance against fusarium wilt of radish by lipopolysaccharides of Pseudomonas fluorescens. Phytopathology 85, 1021-1027.
31. Levine A, Tenhaken R, Dixon R, Lamb C. 1994. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79, 583-593.
32. Magnin-Robert M, Trotel-Aziz P, Quantinet D, Biagianti S, Aziz A. 2007. Biological control of Botrytis cinerea by selected grapevine-associated bacteria and stimulation of chitinase and b-1,3 glucanase activities under field conditions. European Journal of Plant Pathology 118, 43-57.
33. Meziane H, Van der Sluis I, Van Loon LC, Hö fte M, Bakker PAHM. 2005. Determinants of Pseudomonas putida WCS358 involved in inducing systemic resistance in plants. Molecular Plant Pathology 6, 177-185.
34. Murashige T, Skoog F. 1962. A revised medium for rapid growth and bioassays with tobacco cultures. Physiologia Plantarum 15, 473-496.
35. Nitsch JP, Nitsch C. 1969. Haploid plants from pollen grains. Science 169, 85-87.
36. Ongena M, Jourdan E, Adam A, Paquot M, Brans A, Joris B, Arpigny JL, Thonart P. 2007. Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environmental Microbiology 9, 1084-1090.
37. Pezet R, Gindro K, Viret O, Spring JL. 2004. Glycosylation and oxidative dimerzation of resveratrol are respectively associated to sensitivity and resistance of grapevine cultivars to downy mildew. Physiological and Molecular Plant Pathology 65, 297-303.
38. Pieterse CMJ, Van Wees SCM, Hoffland E, Van Pelt JA, Van Loon LC. 1996. Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. The Plant Cell 8, 1225-1237.
39. Raaijmakers JM, Bonsall RF, Weller DM. 1999. Effect of population density of Pseudomonas fluorescens on production of 2,4-diacetylphloroglucinol in the rhizosphere of wheat. Phytopathology 89, 470-475.
40. Raaijmakers JM, Leeman M, Van Oorschot MMP, Van der Sluis I, Schippers B, Bakker PAHM. 1995. Dose-response relationships in biological control of fusarium wilt of radish by Pseudomonas spp. Phytopathology 85, 1075-1081.
41. Raaijmakers JM, Weller DM, Thomashow LS. 1997. Frequency of antibiotic producing Pseudomonas spp. in natural environments. Applied and Environmental Microbiology 63, 881-887.
42. 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.
43. Ton J, Pieterse CMJ, Van Loon LC. 1999. Identification of a locus in Arabidopsis controlling both the expression of rhizobacteria-mediated induced systemic resistance (ISR) and basal resistance against Pseudomonas syringae pv. tomato. Molecular Plant-Microbe Interactions 12, 911-918.
44. Ton J, Van Pelt JA, Van Loon LC, Pieterse CMJ. 2002. Differential effectiveness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis. Molecular Plant-Microbe Interactions 15, 27-34.
45. Tran H, Ficke A, Asiimwe T, Hö fte M, Raaijmakers JM. 2007. Role of the cyclic lipopeptide massetolide A in biological control of Phytophthora infestans and in colonization of tomato plants by Pseudomonas fluorescens. New Phytologist 175, 731-742.
46. Trotel-Aziz P, Couderchet M, Biagianti S, Aziz A. 2008. Characterization of new bacterial biocontrol agents Acinetobacter, Bacillus, Pantoea and Pseudomonas spp. mediating grapevine resistance against Botrytis cinerea. Environmental and Experimental Botany 64, 21-32.
47. Trouvelot S, Varnier A-L, Allè gre M, et al. 2008. A b-1,3 glucan sulfate induces resistance in grapevine against Plasmopara viticola through priming of defense responses, including HR-like cell death. Molecular Plant-Microbe Interactions 21, 232-243.
48. Vandelle E, Poinssot B, Wendehenne D, Bentéjac M, Pugin A. 2006. Integrated signalling network involving calcium, nitric oxide, and active oxygen species but not mitogen-activated protein kinases in BcPG1-elicited grapevine defenses. Molecular Plant-Microbe Interactions 19, 429-440.
49. Van Hulten M, Pelser M, Van Loon LC, Pieterse CM, Ton J. 2006. Costs and benefits of priming for defense in Arabidopsis. Proceedings of the National Academy of Sciences, USA 103, 5602-5607.
50. Van Loon LC, Bakker PAHM, Van Der Heijdt WHW, Wendehenne D, Pugin A. 2008. Early responses of tobacco suspension cells to rhizobacterial elicitors of induced systemic resistance. Molecular Plant-Microbe Interactions 21, 1609-1621.
51. Van Peer R, Niemann GJ, Schippers B. 1991. Induced resistance and phytoalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas sp. WCS417r. Phytopathology 81, 728-734.
52. Van Wees SCM, Pieterse CMJ, Trijssenaar A, Van 't Westende YAM, Hartog F, Van Loon LC. 1997. Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria. Molecular Plant-Microbe Interactions 10, 716-724.
53. Varnier A-L, Sanchez L, Vatsa P, et al. 2009. Bacterial rhamnolipids are novel MAMPs conferring resistance to Botrytis cinerea in grapevine. Plant, Cell and Environment 32, 178-193.
54. Verhagen BWM, Glazebrook J, Zhu T, Van Loon LC, Pieterse CMJ. 2004. The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Molecular Plant-Microbe Interactions 17, 895-908.
55. Voisard CC, Bull T, Keel C, Laville J, Maurhofer M, Schnider U, De'fago G, Haas D. 1994. Biocontrol of root diseases by Pseudomonas fluorescens CHA0: current concepts and experimental approaches. In: O'Gara F, Dowling DN, Boesten B, eds. Molecular ecology of the rhizosphere micro-organisms. Weinheim, Germany: VCH, 67-89.