Advertisement

Induced Systemic Resistance as a Mechanism of Disease Suppression by Rhizobacteria

  • L.C. Van Loon
  • P.A.H.M. Bakker

Abstract

Plant growth-promoting rhizobacteria can suppress diseases through antagonism between the bacteria and soil-borne pathogens, as well as by inducing a systemic resistance in the plant against both root and foliar pathogens. The generally non-specific character of induced resistance constitutes an increase in the level of basal resistance to several pathogens simultaneously, which is of benefit under natural conditions where multiple pathogens may be present. Specific Pseudomonas strains induce systemic resistance in e.g. carnation, cucumber, radish, tobacco and Arabidopsis, as evidenced by an enhanced defensive capacity upon challenge inoculation. Although some bacterial strains are equally effective in inducing resistance in different plant species, others show specificity, indicating specific recognition between bacteria and plants at the root surface. In carnation, radish and Arabidopsis, the O-antigenic side chain of the bacterial outer membrane lipopolysaccharide acts as an inducing determinant, but other bacterial traits are also involved. Pseudobactin siderophores have been implicated in the induction of resistance in tobacco and Arabidopsis, and another siderophore, pseudomonine, may explain induction of resistance associated with salicylic acid (SA) in radish. Although SA induces phenotypically similar systemic acquired resistance (SAR), it is not necessary for the systemic resistance induced by most rhizobacterial strains. Instead, rhizobacteria-mediated induced systemic resistance (ISR) is dependent on jasmonic acid (JA) and ethylene signaling in the plant. Upon challenge inoculation of induced Arabidopsis plants with a pathogen, leaves expressing SAR exhibit a primed expression of SA-, but not JA/ethylene-responsive defense-related genes, whereas leaves expressing ISR are primed to express JA/ethylene-, but not SA-responsive genes. Combination of ISR and SAR can increase protection against pathogens that are resisted through both pathways, as well as extend protection to a broader spectrum of pathogens than ISR or SAR alone.

Key words

disease suppression ISR PGPR SAR 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Achuo, E. A., Audenaert, K., Meziane, H., and Höfte, M., 2004, The salicylic acid-dependent defence pathway is effective against different pathogens in tomato and tobacco. Plant Pathol. 53:65–72.CrossRefGoogle Scholar
  2. Alonso, J. M., Hirayama, T., Roman, G., Nourizadeh, S., and Ecker, J. R., 1999, EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284:2148–2152.CrossRefPubMedGoogle Scholar
  3. Asai, T., Tena, G., Plotnikova, J., Willmann, M.R., Chiu, W. L., Gómez-Gómez, L., Boller, T., Ausubel, F.M., and Sheen, J., 2002, MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–983.CrossRefPubMedGoogle Scholar
  4. Audenaert, K., Pattery, T., Cornelis, P., and Höfte, M., 2002, Induction of systemic resistance to Botrytis cinerea in tomato by Pseudomonas aeruginosa 7NSK2: role of salicylic acid, pyochelin, and pyocyanin. Mol. Plant-Microbe Interact. 15:1147–1156.PubMedGoogle Scholar
  5. Bakker, P. A. H. M., Ran, L. X., Pieterse, C. M. J., and Van Loon, L. C., 2003, Understanding the involvement of rhizobacteria-mediated induction of systemic resistance in biocontrol of plant diseases. Can. J. Plant Pathol. 25:5–9.Google Scholar
  6. Barcelo, A. R., 1997, Lignification in plant cell walls. Int. Rev. Cytol. 176:87–132.Google Scholar
  7. Benhamou, N., and Nicole, M., 1999, Cell biology of plant immunization against microbial infection: the potential of induced resistance in controlling plant diseases. Plant Physiol. Biochem. 37:703–719.CrossRefGoogle Scholar
  8. Bigirimana, J., and Höfte, M., 2002, Induction of systemic resistance to Colletotrichum lindemuthianum in bean by a benzothiadiazole derivative and rhizobacteria. Phytoparasitica 30:159–168.Google Scholar
  9. Bozarth, R. F., and Ross, A. F., 1964, Systemic resistance induced by localized virus infections: extent of changes in uninfected plant parts. Virology 24:446–455.CrossRefPubMedGoogle Scholar
  10. Cao, H., Glazebrook, J., Clarke, J. D., Volko, S., and Dong, X., 1997, The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57–63.CrossRefPubMedGoogle Scholar
  11. Cartieaux, F., Thibaud, M. C., Zimmerli, L., Lessard, P., Sarrobert, C., David, P., Gerbaud, A., Robaglia, C., Somerville, S., and Nussaume, L., 2003, Transcriptome analysis of Arabidopsis colonized by a plant-growth promoting rhizobacterium reveals a general effect on disease resistance. Plant J. 36:177–188.CrossRefPubMedGoogle Scholar
  12. Conrath, U., Pieterse, C. M. J., and Mauch-Mani, B., 2002, Priming in plant-pathogen interactions. Trends Plant Sci. 7:210–216.CrossRefPubMedGoogle Scholar
  13. Coventry, H. S., and Dubery, I. A., 2001, Lipopolysaccharides from Burkholderia cepacia contribute to an enhanced defensive capacity and the induction of pathogenesis-related proteins in Nicotianae tabacum. Physiol. Mol. Plant Pathol. 58:149–158.CrossRefGoogle Scholar
  14. De Meyer, G., and Höfte, 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.Google Scholar
  15. De Meyer, G., Audenaert, K., and Höfte, M., 1999a, Pseudomonas aeruginosa 7NSK2-induced systemic resistance in tobacco depends on in planta salicylic acid accumulation but is not associated with PR1a expression. Eur.J.Plant Pathol. 105:513–517.Google Scholar
  16. De Meyer, G., Capieau, K., Audenaert, K., Buchala, A., Métraux, J. P., and Höfte, M., 1999b, Nanogram amounts of salicylic acid produced by the rhizobacterium Pseudomonas aeruginosa 7NSK2 activate the systemic acquired resistance pathway in bean. Mol.Plant-Microbe Interact. 12:450–458.PubMedGoogle Scholar
  17. Dong, X., 2004, NPR1, all things considered. Curr. Opin. Plant Biol. 7:547–552.CrossRefPubMedGoogle Scholar
  18. Duijff, B. J., Meijer, J. W., Bakker, P. A. H. M., and Schippers, B., 1993, Siderophore-mediated competition for iron and induced resistance in the suppression of fusarium wilt of carnation by fluorescent Pseudomonas spp. Neth. J. Plant Pathol. 99:277–289.Google Scholar
  19. Duijff, B. J., Pouhair, D., Olivain, C., Alabouvette, C., and Lemanceau, P., 1998, Implication of systemic induced resistance in the suppression of fusarium wilt of tomato by Pseudomonas fluorescens WCS417r and by nonpathogenic Fusarium oxysporum Fo47. Eur.J.Plant Pathol. 104:903–910.CrossRefGoogle Scholar
  20. Durrant, W. E., and Dong, X., 2004, Systemic acquired resistance. Annu. Rev. Phytopathol. 42:185–209CrossRefPubMedGoogle Scholar
  21. Ebel, J., and Mithöfer, A., 1998, Early events in the elicitation of plant defence. Planta 206:335–348.CrossRefGoogle Scholar
  22. Erbs, G., and Newman, M. A., 2003, The role of lipopolysaccharides in induction of plant defence responses. Mol. Plant Pathol. 4:421–425.CrossRefGoogle Scholar
  23. Felix, G., Duran, J. D., Volko, S., and Boller, T., 1999, Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18:265–276.CrossRefPubMedGoogle Scholar
  24. Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H., and Ryals, J., 1993, Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754–756.Google Scholar
  25. Garbeva, P., Van Veen, J. A., and Van Elsas, J. D., 2004, Microbial diversity in soil: selection of microbial populations by plant and soil type and implications for disease suppressiveness. Annu. Rev. Phytopathol. 42:243–270.CrossRefPubMedGoogle Scholar
  26. Glick, B. R., Patten, C. L., Holguin, G., and Penrose, D. M., 1999, Biochemical and genetic mechanisms used by plant growth promoting bacteria. Imperial College Press, London.Google Scholar
  27. Gómez-Gómez, L., 2004, Plant perception systems for pathogen recognition and defence. Mol. Immunol. 41:1055–1062.PubMedGoogle Scholar
  28. Gómez-Gómez, L., and Boller, T., 2000, FLS2: a LRR receptor-like kinase involved in recognition of the flagellin elicitor in Arabidopsis. Mol. Cell 5:1003–1020.PubMedGoogle Scholar
  29. Gómez-Gómez, L., and Boller, T., 2002, Flagellin perception: a paradigm for innate immunity. Trends Plant Sci. 7:251–256.PubMedGoogle Scholar
  30. Guo, H., and Ecker, J. R., 2004, The ethylene signalling pathway: new insights. Curr. Opin. Plant Biol. 7:40–49.CrossRefPubMedGoogle Scholar
  31. Handelsman, J., and Stabb, E. V., 1996, Biocontrol of soilborne plant pathogens. Plant Cell 8:1855–1869.CrossRefPubMedGoogle Scholar
  32. Hase, S., Van Pelt, J. A., Van Loon, L. C., and Pieterse, C. M. J., 2003, Colonization of Arabidopsis roots by Pseudomonas fluorescens primes the plant to produce higher levels of ethylene upon pathogen infection. Physiol. Mol. Plant Pathol. 62:219–226.CrossRefGoogle Scholar
  33. Heil, M., 2002, Ecological costs of induced resistance. Curr. Opin. Plant Biol. 5:345–350.CrossRefPubMedGoogle Scholar
  34. Hoffland, E., Hakulinen, J., and Van Pelt, J. A., 1996, Comparison of systemic resistance induced by avirulent and nonpathogenic Pseudomonas species. Phytopathology 86:757–762.Google Scholar
  35. Höfte, M., 1993, Classes of microbial siderophores. In: Iron chelation in plants and soil microorganisms, Barton, L. L., and Hemming, B. C. (eds), Academic Press, San Diego, pp 3–26.Google Scholar
  36. Iavicoli, A., Boutet, E., Buchala, A., and Métraux, 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.PubMedGoogle Scholar
  37. Kessmann, H., Staub, T., Ligon, J., Oostendorp, M., and Ryals, J., 1994, Activation of systemic acquired disease resistance in plants. Eur. J. Plant Pathol. 100:359–369.CrossRefGoogle Scholar
  38. Kim, M. S., Kim, Y. C., and Cho, B. H., 2004, Gene expression analysis in cucumber leaves primed by root colonization with Pseudomonas chlororaphis O6 upon challenge-inoculation with Corynespora cassiicola. Plant Biol. 6:105–108.PubMedGoogle Scholar
  39. Kloepper, J. W., Leong, J., Teintze, M., and Schroth, M. N., 1980, Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286:885–886.CrossRefGoogle Scholar
  40. Kloepper, J. W., Lifshitz, R., and Zablotowicz, R. M., 1989, Free-living bacterial inocula for enhancing crop productivity. Trends Biotechnol. 7:39–43.CrossRefGoogle Scholar
  41. Kloepper, J. W., Zablotowicz, R. M., Tipping, E. M., and Lifshitz, R., 1991, Plant growth promotion mediated by bacterial rhizosphere colonizers. In: The rhizosphere and plant growth. Keister, D. L., and Cregan, P. B. (eds), Kluwer, Dordrecht, pp 315–326.Google Scholar
  42. Kloepper, J. W., Ryu, C. M., and Zhang, S., 2004, Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266.Google Scholar
  43. Knoester, M., Pieterse, C. M. J., Bol, J. F., and Van Loon, L. C., 1999, Systemic resistance in Arabidopsis induced by rhizobacteria requires ethylene-dependent signaling at the site of application. Mol. Plant-Microbe Interact. 12:720–727.PubMedGoogle Scholar
  44. Leeman, M., Van Pelt, J. A., Den Ouden, F. M., Heinsbroek, M., Bakker, P. A. H. M., and Schippers, B., 1995a, Induction of systemic resistance by Pseudomonas fluorescens in radish cultivars differing in susceptibility to fusarium wilt, using a novel bioassay. Eur. J. Plant Pathol. 101:655–664.CrossRefGoogle Scholar
  45. Leeman, M., Van Pelt, J. A., Den Ouden, F. M., Heinsbroek, M., Bakker, P. A. H. M., and Schippers, B., 1995b, Induction of systemic resistance against fusarium wilt of radish by lipopolysaccharides of Pseudomonas fluorescens. Phytopathology 85:1021–1027.Google Scholar
  46. Leeman, M., Van Pelt, J. A., Hendrickx, M. J., Scheffer, R. J., Bakker, P. A. H. M., and Schippers, B., 1995c, Biocontrol of fusarium wilt of radish in commercial greenhouse trials by seed treatment with Pseudomonas fluorescens WCS374. Phytopathology 85:1301–1305.Google Scholar
  47. Leeman, M., Den Ouden, F. M., Van Pelt, J. A., Dirkx, F. P. M., Steijl, H., Bakker, P. A. H. M., and Schippers, B., 1996, Iron availability affects induction of systemic resistance against fusarium wilt of radish by Pseudomonas fluorescens. Phytopathology 86:149–155.Google Scholar
  48. Liu, L., Kloepper, J. W., and Tuzun, S., 1995, Induction of systemic resistance in cucumber by plant growth-promoting rhizobacteria: duration of protection and effect of host resistance on protection and root colonization. Phytopathology 85:1064–1068.Google Scholar
  49. Luschnig, C., Gaxiola, R. A., Grisafi, P., and Fink, G. R., 1998, EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 12:2175–2187.PubMedGoogle Scholar
  50. Lynch, J. M., and Whipps, J. M., 1991, Substrate flow in the rhizosphere. In: The rhizosphere and plant growth, Keister, D. L., and Cregan, P.B. (eds), Kluwer, Dordrecht, pp 15–24.Google Scholar
  51. Malamy, J., Carr, J. P., Klessig, D. F., and Raskin, I., 1990, Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250:1002–1004.Google Scholar
  52. Maurhofer, M., Hase, C., Meuwly, P., Métraux, J. P., and Défago, G., 1994, Induction of systemic resistance of tobacco to tobacco necrosis virus by the root-colonizing Pseudomonas fluorescens strain CHA0: influence of the gacA gene and of pyoverdine production. Phytopathology 84:139–146.Google Scholar
  53. Maurhofer, M., Reimmann, C., Schmidli-Sacherer, P., Heeb, S., Haas, D., and Défago, G., 1998, Salicylic acid biosynthetic genes expressed in Pseudomonas fluorescens strain P3 improve the induction of systemic resistance in tobacco against tobacco necrosis virus. Phytopathology 88:678–684.Google Scholar
  54. Mercado-Blanco, J., Van der Drift, K. M. G. M., Olsson, P. E., Thomas-Oates, J. E., Van Loon, L. C., and Bakker, P. A. H. M., 2001, Analysis of the pmsCEAB gene cluster involved in biosynthesis of salicylic acid and the siderophore pseudomonine in the biocontrol strain Pseudomonas fluorescens WCS374. J. Bacteriol. 183:1909–1920.CrossRefPubMedGoogle Scholar
  55. Métraux, J. P., Signer, H., Ryals, J., Ward, E., Wyss-Benz, M., Gaudin, J., Raschdorf, K., Schmid, E., Blum, W., and Inverardi, B., 1990, Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250:1004–1006.Google Scholar
  56. Meziane, H., Van der Sluis, I., Van Loon, L. C., Höfte, M., and Bakker, P. A. H. M., 2005, Determinants of Pseudomonas putida WCS358 involved in inducing systemic resistance in plants. Mol. Plant Pathol. 6:177–185.CrossRefGoogle Scholar
  57. Nürnberger, T., Brunner, F., Kemmerling, B., and Piater, L., 2004, Innate immunity in plants and animals: striking similarities and obvious differences. Immunol. Rev. 198:249–266.PubMedGoogle Scholar
  58. Park, K. S., and Kloepper, J. W., 2000, Activation of PR-1a promoter by rhizobacteria which induce systemic resistance in tobacco against Pseudomonas syringae pv. tabaci. Biol. Control 18:2–9.CrossRefGoogle Scholar
  59. Pieterse, C. M. J., Van Wees, S. C. M., Hoffland, E., Van Pelt, J. A., and Van Loon, L. C., 1996, Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 8:1225–1237.CrossRefPubMedGoogle Scholar
  60. Pieterse, C. M. J., Van Wees, S. C. M., Van Pelt, J. A., Knoester, M., Laan, R., Gerrits, H., Weisbeek, P. J., and Van Loon, L. C., 1998, A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580.CrossRefPubMedGoogle Scholar
  61. Pieterse, C. M. J., Van Pelt, J. A., Ton, J., Parchmann, S., Mueller, M. J., Buchala, A. J., Métraux, J. P., and Van Loon, L. C., 2000, Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis requires sensitivity to jasmonate and ethylene but is not accompanied by an increase in their production. Physiol. Mol. Plant Pathol. 57:123–134.CrossRefGoogle Scholar
  62. Press, C. M., Wilson, M., Tuzun, S., and Kloepper, J. W., 1997, Salicylic acid produced by Serratia marcescens 90–166 is not the primary determinant of induced systemic resistance in cucumber or tobacco. Mol. Plant-Microbe Interact. 10:761–768.Google Scholar
  63. Raaijmakers, J. M., Leeman, M., Van Oorschot, M. P. M., Van der Sluis, I., Schippers, B., and Bakker, P. A. H. M., 1995, Dose-response relationships in biological control of fusarium wilt of radish by Pseudomonas spp. Phytopathology 85:1075–1081.Google Scholar
  64. Ramamoorthy, V., Viswanathan, R., Raguchander, T., Prakasam, V., and Samiyappan, R., 2001, Induction of systemic resistance by plant growth promoting rhizobacteria in crop plants against pests and diseases. Crop Protection 20:1–11.CrossRefGoogle Scholar
  65. Rasmussen, J. B., Hammerschmidt, R., and Zook, M. N., 1991, Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv. syringae. Plant Physiol. 97:1342–1347.Google Scholar
  66. Reitz, M., Oger, P., Meyer, A., Niehaus, K., Farrand, S. K., Hallmann, J., and Sikora, R. A. 2002, Importance of the O-antigen, core-region and lipid A of rhizobial lipopolysaccharides for the induction of systemic resistance in potato to Globodera pallida. Nematology 4:73–79.CrossRefGoogle Scholar
  67. Roberts, D. A., 1983, Acquired resistance to tobacco mosaic virus transmitted to the progeny of hypersensitive tobacco. Virology 124:161–163.CrossRefGoogle Scholar
  68. Roman, G., Lubarsky, B., Kieber, J. J., Rothenberg, M., and Ecker, J. R., 1995, Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway. Genetics 139:1393–1409.PubMedGoogle Scholar
  69. Ross, A. F., 1961, Systemic acquired resistance induced by localized virus infections in plants. Virology 14:340–358.PubMedGoogle Scholar
  70. Ryals, J. A., Neuenschwander, U. H., Willits, M. G., Molina, A., Steiner, H. Y., and Hunt, M. D., 1996, Systemic acquired resistance. Plant Cell 8:1809–1819.CrossRefPubMedGoogle Scholar
  71. Ryu, C. M., Hu, C. H., Reddy, M. S., and Kloepper, J. W., 2003, Different signaling pathways of induced resistance by rhizobacteria in Arabidopsis thaliana against two pathovars of Pseudomonas syringae. New Phytol. 160:413–420.CrossRefGoogle Scholar
  72. Ryu, C. M., Farag, M. A., Hu, C. H., Reddy, M. S., Kloepper, J. W., and Paré, P. W., 2004, Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol. 134:1017–1026.CrossRefPubMedGoogle Scholar
  73. Schippers, B., Bakker, A. W., and Bakker, P. A. H. M., 1987, Interactions of deleterious and beneficial rhizosphere micro-organisms and the effect of cropping practices. Annu. Rev. Phytopathol. 25:339–358.CrossRefGoogle Scholar
  74. Schippers, B., Bakker, A.W., Bakker, P. A. H. M., and Van Peer, R., 1991, Beneficial and deleterious effects of HCN-producing pseudomonads on rhizosphere interactions. In The rhizosphere and plant growth, Keister, D. L., and Cregan, P.B. (eds), Kluwer, Dordrecht, pp 211–219.Google Scholar
  75. Shulaev, V., Leon, J., and Raskin, I., 1995, Is salicylic acid a transported signal of systemic acquired resistance in tobacco? Plant Cell 7:1691–1701.CrossRefPubMedGoogle Scholar
  76. Siddiqui, I. A., and Shaukat, S. S., 2003, Suppression of root-knot disease by Pseudomonas fluorescens CHA0 in tomato: importance of bacterial secondary metabolite, 2,4-diacetylpholoroglucinol. Soil Biol. Biochem. 35:1615–1623.Google Scholar
  77. Siddiqui, I. A., and Shaukat, S. S., 2004, Systemic resistance in tomato induced by biocontrol bacteria against the root-knot nematode, Meloidogyne javanica is independent of salicylic acid production. J.Phytopathol. 152:48–54.CrossRefGoogle Scholar
  78. Singh, D. P., Moore, C. A., Gilliland, A., and Carr, J. P., 2004, Activation of multiple antiviral defence mechanisms by salicylic acid. Mol. Plant Pathol. 5:57–63.CrossRefGoogle Scholar
  79. Somers, E., Vanderleijden, J., and Srinivasan, M., 2004, Rhizosphere bacterial signalling: a love parade beneath our feet. Crit. Rev. Microbiol. 30:205–240.CrossRefPubMedGoogle Scholar
  80. Spencer, M., Ryu, C. M., Yang, K. Y., Kim, Y. C., Kloepper, J. W., and Anderson, A. J., 2003, Induced defence in tobacco by Pseudomonas chlororaphis strain O6 involves at least the ethylene pathway. Physiol. Mol. Plant Pathol. 63:27–34.CrossRefGoogle Scholar
  81. Staswick, P. E., and Tiryaki, I., 2004, The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–2127.CrossRefPubMedGoogle Scholar
  82. Sticher, L., Mauch-Mani, B., and Métraux, J. P., 1997, Systemic acquired resistance. Annu. Rev. Phytopathol. 35:235–270.CrossRefPubMedGoogle Scholar
  83. Thomma, B. P. H. J., Eggermont, K., Broekaert, W. F., and Cammue, B. P. A., 2000, Disease development of several fungi on Arabidopsis can be reduced by treatment with methyl jasmonate. Plant Physiol. Biochem. 38:421–427.CrossRefGoogle Scholar
  84. Thomma, B. P. H. J., Tierens, K. F. M., Penninckx, I. A. M. A., Mauch-Mani, B., Broekaert, W. F., and Cammue, B. P. A., 2001, Different micro-organisms differentially induce Arabidopsis disease response pathways. Plant Physiol. Biochem. 39:673–680.CrossRefGoogle Scholar
  85. Timmusk, S., and Wagner, E. G. H., 1999, The plant-growth-promoting rhizobacterium Paenibacillus polymyxa induces changes in Arabidopsis thaliana gene expression: a possible connection between biotic and abiotic stress responses. Mol. Plant-Microbe Interact. 12:951–959.PubMedGoogle Scholar
  86. Ton, J., Pieterse, C. M. J., and Van Loon, L. C., 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. Mol. Plant-Microbe Interact. 12:911–918.PubMedGoogle Scholar
  87. Ton, J., Van Pelt, J. A., Van Loon, L. C., and Pieterse, C. M. J., 2002, Differential effectiveness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis. Mol. Plant-Microbe Interact. 15:27–34.PubMedGoogle Scholar
  88. Turlier, M. F., Eparvier, A., and Alabouvette, C., 1994, Early dynamic interactions between Fusarium oxysporum f.sp. lini and the roots of Linum usitatissimum as revealed by transgenic GUS-marked hyphae. Can. J. Bot. 72:1605–1612.Google Scholar
  89. Van Loon, L. C., 1997, Induced resistance in plants and the role of pathogenesis-related proteins. Eur. J. Plant Pathol. 103:753–765.Google Scholar
  90. Van Loon, L. C., 2000, Systemic induced resistance. In: Mechanisms of resistance to plant diseases, Slusarenko, A. J., Fraser. R. S. S., and Van Loon, L. C. (eds), Kluwer, Dordrecht, pp 521–574.Google Scholar
  91. Van Loon, L. C., and Antoniw, J. F., 1982, Comparison of the effects of salicylic acid and ethephon with virus-induced hypersensitivity and acquired resistance in tobacco. Neth. J. Plant Pathol. 88:237–256.Google Scholar
  92. Van Loon, L. C., and Bakker, P. A. H. M., 2003, Signalling in rhizobacteria-plant interactions. In: Root ecology, De Kroon, H., and Visser, E. J. W. (eds), Springer-Verlag, Berlin Heidelberg, pp 297–330.Google Scholar
  93. Van Loon, L. C., and Glick, B. R., 2004, Increased plant fitness by rhizobacteria. In: Molecular ecotoxicology of plants, Sandermann, H. (ed), Springer-Verlag, Berlin Heidelberg, pp 177–205.Google Scholar
  94. Van Loon, L. C., and Van Strien, E. A., 1999, The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol. Mol. Plant Pathol 55:85–97.Google Scholar
  95. Van Loon, L. C., Bakker, P. A. H. M., and Pieterse, C. M. J., 1998, Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36:453–483.PubMedGoogle Scholar
  96. Van Peer, R., and Schippers, B., 1992, Lipopolysaccharides of plant-growth promoting Pseudomonas sp. strain WCS417r induce resistance in carnation to fusarium wilt. Neth. J. Plant Pathol. 98:129–139.Google Scholar
  97. Van Peer, R., Niemann, G. J., and 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
  98. Van Wees, S. C. M., Pieterse, C. M. J., Trijssenaar, A., Van’ t Westende, Y., Hartog, F., and Van Loon, L. C., 1997, Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria. Mol. Plant-Microbe Interact. 10:716–724.PubMedGoogle Scholar
  99. Van Wees, S. C. M., Luijendijk, M., Smoorenburg, I., Van Loon, L. C., and Pieterse, C. M. J., 1999, Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis is not associated with a direct effect on expression of known defense-related genes but stimulates the expression of the jasmonate-inducible gene Atvsp upon challenge. Plant Mol. Biol. 41:537–549.PubMedGoogle Scholar
  100. Van Wees, S. C. M., De Swart, E. A. M., Van Pelt, J. A., Van Loon, L. C., and Pieterse, C. M. J., 2000, Enhancement of induced disease resistance by simultaneous activation of salicylate-and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 97:8711–8716.PubMedGoogle Scholar
  101. Verberne, M. C., Hoekstra, J., Bol, J. F., and Linthorst, H. J. M., 2003, Signaling of systemic acquired resistance in tobacco depends on ethylene perception. Plant J. 35:27–32.CrossRefPubMedGoogle Scholar
  102. Verhagen, B. W. M., Glazebrook, J., Zhu, T., Chang, H. S., Van Loon, L. C., and Pieterse, C. M. J., 2004, The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Mol. Plant-Microbe Interact. 17:895–908.PubMedGoogle Scholar
  103. Vernooij, B., Friedrich, L., Morse, A., Reist, R., Kolditz-Jahwar, R., Ward, E., Uknes, S., Kessmann, H., and Ryals, J., 1994, Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell 6:959–965.CrossRefPubMedGoogle Scholar
  104. Vidal, S., Eriksson, A. R. B., Montesano, M., Denecke, J., and Palva, E. T., 1998, Cell walldegrading enzymes from Erwinia carotovora cooperate in the salicylic acid-independent induction of a plant defense response. Mol. Plant-Microbe Interact. 11:23–32.Google Scholar
  105. Wei, G., Kloepper, J. W., and Tuzun, S., 1991, Induction of systemic resistance of cucumber to Colletotrichum orbiculare by select strains of plant growth-promoting rhizobacteria. Phytopathology 81:1508–1512.Google Scholar
  106. Weller, D. M., Raaijmakers, J. M., McSpadden Gardiner, B. B., and Thomashow, L. S., 2002, Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu. Rev. Phytopathol. 40:309–348.CrossRefPubMedGoogle Scholar
  107. Weller D. M., Van Pelt, J. A., Mavrodi, D. V., Pieterse, C. M. J., Bakker, P. A. H. M., and Van Loon, L. C., 2004, Induced systemic resistance (ISR) in Arabidopsis against Pseudomonas syringae pv. tomato by 2,4-diacetylphloroglucinol (DAPG)-producing Pseudomonas fluorescens. Phytopathology 94:S108.Google Scholar
  108. Whipps, J. M., 2001, Microbial interactions and biocontrol in the rhizosphere. J. Exp. Bot. 52:487–511.PubMedGoogle Scholar
  109. Yan, Z., Reddy, M. S., Ryu, C. M., McInroy, J. A., Wilson, M., and Kloepper, J. W., 2002, Induced systemic protection against tomato late blight elicited by plant growth-promoting rhizobacteria. Phytopathology 92:1329–1333.Google Scholar
  110. Zhang, S., Moyne, A. L., Reddy, M. S., and Kloepper, J. W., 2002, The role of salicylic acid in induced systemic resistance elicited by plant growth-promoting rhizobacteria against blue mold of tobacco. Biol. Control 25:288–296.CrossRefGoogle Scholar
  111. Zipfel, C., Robatzek, S., Navarro. L., Oakeley, E. J., Jones, J. D. G., Felix, G., and Boller, T., 2004, Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–767.CrossRefPubMedGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • L.C. Van Loon
    • 1
  • P.A.H.M. Bakker
    • 1
  1. 1.Faculty of Biology, Section PhytopathologyUtrecht UniversityUtrechtThe Netherlands

Personalised recommendations