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European Journal of Plant Pathology

, Volume 121, Issue 3, pp 233–242 | Cite as

Priming: it’s all the world to induced disease resistance

  • Katharina Goellner
  • Uwe Conrath
Article

Abstract

After infection by a necrotising pathogen, colonisation of the roots with certain beneficial microbes, or after treatment with various chemicals, many plants establish a unique physiological situation that is called the ‘primed’ state of the plant. In the primed condition, plants are able to ‘recall’ the previous infection, root colonisation or chemical treatment. As a consequence, primed plants respond more rapidly and/or effectively when re-exposed to biotic or abiotic stress, a feature that is frequently associated with enhanced disease resistance. Though priming has been known as a component of induced resistance for a long time, most progress in the understanding of the phenomenon has been made over the past few years. Here we summarize the current knowledge of priming and its relevance for plant protection in the field.

Keywords

Benzothiadiazole 2,6-dichloroisonicotinic acid Potentiation of defence responses Salicylic acid Sensitisation Stress resistance 

Abbreviations

BABA

β-aminobutyric acid

IR

induced resistance

ISR

induced systemic resistance

MAMP

microbe-associated molecular pattern

SA

salicylic acid

SAR

systemic acquired resistance

Notes

Acknowledgements

Research on priming in the Plant Biochemistry & Molecular Biology Group is supported by BASF, BASF Plant Science, Bayer CropScience, the German Science Foundation (DFG) and the Peter and Traudl Engelhorn Foundation.

References

  1. Agrawal, A. A., Strauss, S. Y., & Stout, M. J. (1999). Costs of induced responses and tolerance to herbivory in male and female fitness components of wild radish. Evolution, 53, 1093–1104.CrossRefGoogle Scholar
  2. Ahn, I.-P., Kim, S., & Lee, Y.-H. (2005). Vitamin B1 functions as an activator of plant disease resistance. Plant Physiology, 138, 1505–1515.PubMedCrossRefGoogle Scholar
  3. Ahn, I.-P., Kim, S., Lee, Y.-H., & Suh, S.-C. (2007). Vitamin B1-induced priming is dependent on hydrogen peroxide and the NPR1 gene in Arabidopsis. Plant Physiology, 143, 838–848.PubMedCrossRefGoogle Scholar
  4. Baldwin, I. T. (1998). Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proceedings of the National Academy of Sciences of the USA, 95, 8113–8118.PubMedCrossRefGoogle Scholar
  5. Baldwin, I. T., & Schultz, J. C. (1983). Rapid changes in tree chemistry induced by damage: evidence for communication between plants. Science, 221, 277–279.PubMedCrossRefGoogle Scholar
  6. Bartlett, D. W., Clough, J. M., Godwin, J. R., Hall, A. A., Hamer, M., & Parr-Dobrzanski, B. (2002). The strobilurin fungicides. Pest Management Science, 58, 649–662.PubMedCrossRefGoogle Scholar
  7. Boch, J., Verbsky, M. L., Robertson, T. L., Larkin, J. C., & Kunkel, B. N. (1998). Analysis of resistance gene-mediated defence responses in Arabidopsis thaliana plants carrying a mutation in CPR5. Molecular Plant-Microbe Interactions, 12, 1196–1206.CrossRefGoogle Scholar
  8. Bowling, S. A., Clarke, J. D., Liu, Y., Klessig, D. F., & Dong, X. (1997). The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell, 9, 1573–1584.PubMedCrossRefGoogle Scholar
  9. Bowling, S. A., Guo, A., Cao, H., Gordon, A. S., Klessig, D., & Dong, X. (1994). A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell, 6, 1845–1857.PubMedCrossRefGoogle Scholar
  10. Cao, H., Bowling, S. A., Gordon, A. S., & Dong, X. (1994). Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell, 8, 1583–1592.CrossRefGoogle Scholar
  11. Cipollini, D. F. (2002). Does competition magnify the fitness costs of induced responses in Arabidopsis thaliana? A manipulative approach. Oecologia, 131, 514–520.CrossRefGoogle Scholar
  12. Cohen, Y. R. (2002). β-Aminobutyric acid-induced resistance against plant pathogens. Plant Disease, 86, 448–457.CrossRefGoogle Scholar
  13. Conrath, U. (2006). Systemic acquired resistance. Plant Signaling & Behavior, 1, 179–184.Google Scholar
  14. Conrath, U., Beckers, G. J. M., Flors, V., García-Agustín, P., Jakab, G., Mauch, F., Prime-A-Plant Group, et al. (2006). Priming: getting ready for battle. Molecular Plant-Microbe Interactions 2006, 19, 1062–1071.CrossRefGoogle Scholar
  15. Conrath, U., Chen, Z., Ricigliano, J. R., & Klessig, D. F. (1995). Two inducers of plant defence responses, 2,6-dichloroisonicotinic acid and salicylic acid, inhibit catalase activity in tobacco. Proceedings of the National Academy of Sciences of the USA, 92, 7143–7147.PubMedCrossRefGoogle Scholar
  16. Conrath, U., Pieterse, C. M. J., & Mauch-Mani, B. (2002). Priming in plant–pathogen interactions. Trends in Plant Sciences, 7, 210–216.CrossRefGoogle Scholar
  17. Cools, H. J., & Ishii, H. (2002). Pretreatment of cucumber plants with acibenzolar-S-methyl systemically primes a phenylalanine ammonia-lyase (PAL1) for enhanced expression upon attack with a pathogenic fungus. Physiological and Molecular Plant Pathology, 61, 273–280.CrossRefGoogle Scholar
  18. Delaney, T. P., Friedrich, L., & Ryals, J. A. (1995). Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proceedings of the National Academy of Sciences of the USA, 92, 6602–6606.PubMedCrossRefGoogle Scholar
  19. Delaney, T. P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., et al. (1994). A central role of salicylic acid in plant disease resistance. Science, 266, 1247–1249.PubMedCrossRefGoogle Scholar
  20. Dong, X. (2001). Genetic dissection of systemic acquired resistance. Current Opinion in Plant Biology, 4, 309–314.PubMedCrossRefGoogle Scholar
  21. Durrant, W. E., & Dong, X. (2004). Systemic acquired resistance. Annual Review of Phytopathology, 42, 185–209.PubMedCrossRefGoogle Scholar
  22. Engelberth, J., Alborn, H. T., Schmelz, E. A., & Tumlinson, J. H. (2004). Airborne signals prime plants against insect herbivore attack. Proceedings of the National Academy of Sciences of the USA, 101, 1781–1785.PubMedCrossRefGoogle Scholar
  23. Friedrich, L., Lawton, K., Ruess, W., Masner, P., Specker, N., Gut-Rella, M., et al. (1996). A benzothiadiazole derivative induces systemic acquired resistance in tobacco. Plant Journal, 10, 61–70.CrossRefGoogle Scholar
  24. Frye, C. A., & Innes, R. W. (1998). An Arabidopsis mutant with enhanced resistance to powdery mildew. Plant Cell, 10, 947–956.PubMedCrossRefGoogle Scholar
  25. Fuster, M. D., García-Puig, D., Ortuño, A., Botía, J. M., Sabater, F., Porras, I., et al. (1995). Selection of Citrus highly productive in secondary metabolites of industrial interest. Modulation of synthesis and/or accumulation processes. In C. García-Viguera, M. Castañer, M. I. Gil, F. Ferreres, & F. A. Tomás-Barberán (Eds.) Current trends in fruit and vegetable phytochemistry (pp. 81–85). Madrid: CSIC.Google Scholar
  26. Gaffney, T., Friedrich, L., Vernoij, B., Negrotto, D., Nye, G., Uknes, S., et al. (1993). Requirement of salicylic acid for the induction of systemic acquired resistance. Science, 261, 754–756.PubMedCrossRefGoogle Scholar
  27. Görlach, J., Volrath, S., Knauf-Beiter, G., Hengy, G., Beckhove, U., Kogel, K.-H., et al. (1996). Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell, 8, 629–643.PubMedCrossRefGoogle Scholar
  28. He, C. Y., Hsiang, T., & Wolyn, D. J. (2002). Induction of systemic disease resistance and pathogen defence responses in Asparagus officinalis inoculated with non-pathogenic strains of Fusarium oxysporum. Plant Pathology, 51, 225–230.CrossRefGoogle Scholar
  29. He, P., Warren, R. F., Zhao, T., Shan, L., Zhu, L., Tang, X., et al. (2001). Overexpression of PTI5 in tomato potentiates pathogen-induced defence gene expression and enhances disease resistance to Pseudomonas syringae pv. tomato. Molecular Plant-Microbe Interactions, 14, 1453–1457.PubMedCrossRefGoogle Scholar
  30. He, C. Y., & Wolyn, D. J. (2005). Potential role for salicylic acid in induced resistance of asparagus roots to Fusarium oxysporum f.sp. asparagi. Plant Pathology, 54, 227–232.CrossRefGoogle Scholar
  31. Heidel, A. J., Clarke, J. D., Antonovics, J., & Dong, X. (2004). Fitness costs of mutations affecting the systemic acquired resistance pathway in Arabidopsis thaliana. Genetics, 168, 2197–2206.PubMedCrossRefGoogle Scholar
  32. Heil, M., Hilpert, A., Kaiser, W., & Linsenmair, K. E. (2000). Reduced growth and seed set following chemical induction of pathogen defence: Does systemic acquired resistance (SAR) incur allocation costs? Journal of Ecology, 88, 645–654.CrossRefGoogle Scholar
  33. Heil, M., & Kost, C. (2006). Priming of indirect defences. Ecology Letters, 9, 813–817.PubMedCrossRefGoogle Scholar
  34. Heil, M., & Silva Bueno, J. C. (2007). Within-plant signalling by volatiles leads to induction and priming of an indirect plant defence in nature. Proceedings of the National Academy of Sciences of the USA, 104, 5467–5472.PubMedCrossRefGoogle Scholar
  35. Herms, S., Seehaus, K., Koehle, H., & Conrath, U. (2002). A strobilurin fungicide enhances the resistance of tobacco against Tobacco mosaic virus and Pseudomonas syringae pv. tabaci. Plant Physiology, 130, 120–127.PubMedCrossRefGoogle Scholar
  36. Jakab, G., Ton, J., Flors, V., Zimmerli, L., Métraux, J.-P., & Mauch-Mani, B. (2005). Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiology, 139, 267–274.PubMedCrossRefGoogle Scholar
  37. Katz, V. A., Thulke, O. U., & Conrath, U. (1998). A benzothiadiazole primes parsley cells for augmented elicitation of defence responses. Plant Physiology, 117, 1333–1339.PubMedCrossRefGoogle Scholar
  38. Kauss, H., Franke, R., Krause, K., Conrath, U., Jeblick, W., Grimmig, B., et al. (1993). Conditioning of parsley (Petroselinum crispum) suspension cells increases elicitor-induced incorporation of cell wall phenolics. Plant Physiology, 102, 459–466.PubMedGoogle Scholar
  39. Kauss, H., & Jeblick, W. (1995). Pretreatment of parsley suspension cultures with salicylic acid enhances spontaneous and elicited production of H2O2. Plant Physiology, 108, 1171–1178.PubMedGoogle Scholar
  40. Kauss, H., Theisinger-Hinkel, E., Mindermann, R., & Conrath, U. (1992). Dichloroisonicotinic and salicylic acid, inducers of systemic acquired resistance, enhance fungal elicitor responses in parsley cells. Plant Journal, 2, 655–660.Google Scholar
  41. Kessler, A., Halitschke, R., Diezel, C., & Baldwin, I. T. (2006). Priming of plant defence responses in nature by airborne signalling between Artemisia tridentata and Nicotiana attenuata. Oecologia, 148, 280–292.PubMedCrossRefGoogle Scholar
  42. Kessmann, H., Staub, T., Hofmann, C., Maetzke, T., Herzog, J., Ward, E., et al. (1994). Induction of systemic acquired disease resistance in plants by chemicals. Annual Review of Phytopathology, 32, 439–459.PubMedCrossRefGoogle Scholar
  43. Kim, H. K., Oh, S.-R., Lee, H.-K., & Huh, H. (2001). Benzothiadiazole enhances the elicitation of rosmarinic acid production in a suspension culture of Agastache rugosa. Biotechnology Letters, 23, 55–60.CrossRefGoogle Scholar
  44. Koehle, H., Conrath, U., Seehaus, K., Niedenbrueck, M., Tavares-Rodrigues, M.-A., Sanchez, W., et al. (2006). Method of inducing virus tolerance of plants. US Patent 20060172887.Google Scholar
  45. Koehle, H., Herms, S., & Conrath, U. (2003). Method for immunizing plants against bacterioses. Patent Application No. WO2003075663.Google Scholar
  46. Koganezawa, H., Sato, T., & Sasaya, T. (1998). Effects of Probenazole and saccharin on symptom appearance of Tobacco mosaic virus in tobacco. Annals of the Phytopathological Society of Japan, 64, 80–84.Google Scholar
  47. Kohler, A., Schwindling, S., & Conrath, U. (2002). Benzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis. Plant Physiology, 128, 1046–1056.PubMedCrossRefGoogle Scholar
  48. Korves, T., & Bergelson, J. (2004). A novel cost of R gene resistance in the presence of disease. The American Naturalist, 163, 489–504.PubMedCrossRefGoogle Scholar
  49. Kuć, J. (1987). Translocated signals for plant immunization. Annals of the New York Academy of Sciences, 494, 221–223.CrossRefGoogle Scholar
  50. Kuć, J. (2001). Concepts and direction of induced systemic resistance in plants and its application. European Journal of Plant Pathology, 107, 7–12.Google Scholar
  51. Latunde-Dada, A. O., & Lucas, J. A. (2001). The plant defence activator acibenzolar-S-methyl primes cowpea [Vignia unguiculata (L.) Walp.] seedlings for rapid induction of resistance. Physiological and Molecular Plant Pathology, 58, 199–208.CrossRefGoogle Scholar
  52. Lawton, K. A., Friedrich, L., Hunt, M., Weymann, K., Delaney, T., Kessmann, H., et al. (1996). Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant Journal, 10, 71–82.PubMedCrossRefGoogle Scholar
  53. Leeman, M., van Pelt, J. A., Hendrickx, M. J., Scheffer, R. J., Bakker, P. A. H. M., & Schippers, B. (1995). Biocontrol of Fusarium wilt of radish in commercial greenhouse trials by seed treatment with Pseudomonas fluorescens WCS374. Phytopathology, 85, 1301–1305.CrossRefGoogle Scholar
  54. Maleck, K., Levine, A., Eulgem, T., Morgan, A., Schmid, J., Lawton, K. A., et al. (2000). The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nature Genetics, 26, 403–410.PubMedCrossRefGoogle Scholar
  55. Mauch, F., Mauch-Mani, B., Gaille, C., Kull, B., Haas, D., & Reimmann, C. (2001). Manipulation of salicylate content in Arabidopsis thaliana by the expression of an engineered bacterial salicylate synthase. Plant Journal, 25, 66–67.CrossRefGoogle Scholar
  56. Mur, L. A. J., Brown, I. R., Darby, R. M., Bestwick, C. S., Bi, Y.-M., Mansfield, J. W., et al. (2000). A loss of resistance to avirulent bacterial pathogens in tobacco is associated with the attenuation of a salicylic acid-potentiated oxidative burst. Plant Journal, 23, 609–621.PubMedCrossRefGoogle Scholar
  57. Mur, L. A. J., Naylor, G., Warner, S. A. J., Sugars, J. M., White, R. F., & Draper, J. (1996). Salicylic acid potentiates defence gene expression in tissue exhibiting acquired resistance to pathogen attack. Plant Journal, 9, 559–571.CrossRefGoogle Scholar
  58. Newmann, M.-A., Dow, J. M., Molinaro, A., & Parrilli, M. (2007). Priming, induction and modulation of plants defence responses by bacterial lipopolysaccharides. Journal of Endotoxin Research, 13, 69–84.CrossRefGoogle Scholar
  59. Ortuño, A., Botia, J. M., Fuster, M. D., Porras, I., García-Lidón, A., & del Río, J. A. (1997). Effect of scoparone (6–7-dimethoxicoumarin) biosynthesis on the resistance of tangelo Nova, Citrus paradisi and Citrus aurantium fruits against Phytophthora parasitica. Journal of Agriculture and Food Chemistry, 45, 2740–2743.CrossRefGoogle Scholar
  60. Paré, P. W., & Tumlinson, J. H. (1999). Plant volatiles as a defence against insect herbivores. Plant Physiology, 121, 325–332.PubMedCrossRefGoogle Scholar
  61. Pieterse, C. M. J., van Wees, S. C. M., van Pelt, J. A., Knoester, M., Laan, G., Gerrits, H., et al. (1998). A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell, 10, 1571–1580.PubMedCrossRefGoogle Scholar
  62. Pozo, M. J., Van Loon, L. C., & Pieterse, C. M. J. (2005). Jasmonates – Signals in plant–microbe interactions. Journal of Plant Growth Regulation, 23, 211–222.Google Scholar
  63. Prats, E., Rubiales, D., & Jorrín, J. (2002). Acibenzolar-methyl-induced resistance to sunflower rust (Puccinia helianthi) is associated with enhancement of coumarins on foliar surface. Physiological and Molecular Plant Pathology, 60, 155–162.CrossRefGoogle Scholar
  64. Rai, M., Acharya, D., Singh, A., & Varma, A. (2001). Positive growth responses of the medicinal plants Spilanthes calva and Withania somnifera to inoculation by Piriformospora indica in a field trial. Mycorrhiza, 11, 123–128.CrossRefGoogle Scholar
  65. Ruess, W., Mueller, K., Knauf-Beiter, G., Kunz, W., & Staub, T. (1996). Plant activator CGA 245704: An innovative approach for disease control in cereals and tobacco. Proceedings of the Brighton Crop Protect Conference – Pests and Diseases, 53–60.Google Scholar
  66. Ryals, J. A., Neuenschwander, U. H., Willits, M. G., Molina, A., Steiner, H.-Y., & Hunt, M. D. (1996). Systemic acquired resistance. Plant Cell, 8, 1809–1819.PubMedCrossRefGoogle Scholar
  67. Sauter, H. (2007). Strobilurins and other complex III inhibitors. In W. Krämer, & U. Schirmer (Eds.) Modern crop protection compounds (pp. 341–366). Weinheim: VCH-Wiley.Google Scholar
  68. Shirasu, K., Nakajima, H., Rajasekhar, K., & Dixon, R. A. (1997). Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defence mechanisms. Plant Cell, 9, 261–270.PubMedCrossRefGoogle Scholar
  69. Siegrist, J., Muehlenbeck, S., & Buchenauer, H. (1998). Cultured parsley cells, a model system for the rapid testing of abiotic and natural substances as inducers of systemic acquired resistance. Physiological and Molecular Plant Pathology, 53, 223–238.CrossRefGoogle Scholar
  70. Stennis, M. J., Chandra, S., Ryan, C. A., & Low, P. S. (1998). Systemin potentiates the oxidative burst in cultured tomato cells. Plant Physiology, 117, 1031–1036.PubMedCrossRefGoogle Scholar
  71. Thielert, W. (2006). A unique product: The story of the Imidacloprid stress shield. Pflanzenschutz-Nachrichten Bayer, 59, 73–86.Google Scholar
  72. Thulke, O. U., & Conrath, U. (1998). Salicylic acid has a dual role in the activation of defence-related genes in parsley. Plant Journal, 14, 35–42.PubMedCrossRefGoogle Scholar
  73. Tian, D., Traw, M. B., Chen, J. Q., Kreitman, M., & Bergelson, J. (2003). Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature, 423, 74–77.PubMedCrossRefGoogle Scholar
  74. Ton, J., D’Allessandro, M., Jourdie, V., Jakab, G., Karlen, D., Held, M., et al. (2006). Priming by airborne signals boosts direct and indirect resistance in maize. Plant Journal, 49, 16–26.PubMedCrossRefGoogle Scholar
  75. Van Dam, N. M., & Baldwin, I. T. (2001). Competition mediates costs of jasmonate-induced defences, nitrogen acquisition and transgenerational plasticity in Nicotiana attenuata. Functional Ecology, 15, 406–415.CrossRefGoogle Scholar
  76. Van Hulten, M., Pelser, M., van Loon, L. C., Pieterse, C. M. J., & Ton, J. (2006). Costs and benefits of priming for defense in Arabidopsis. Proceedings of the National Academy of Sciences of the USA, 103, 5602–5607.PubMedCrossRefGoogle Scholar
  77. Van Loon, L. C., Bakker, P. A. H. M., & Pieterse, C. M. J. (1998). Systemic resistance induced by rhizosphere bacteria. Annual Review of Phytopathology, 36, 453–483.PubMedCrossRefGoogle Scholar
  78. Verhagen, B. W. M., Glazebrook, J., Zhu, T., Chang, H.-S., van Loon, L. C., & Pieterse, C. M. J. (2004). The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Molecular Plant-Microbe Interactions, 17, 895–908.PubMedCrossRefGoogle Scholar
  79. Waller, F., Ahatz, B., Baltruschat, H., Fodor, J., Becker, K., Fischer, M., et al. (2005). The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proceedings of the National Academy of Sciences of the USA, 102, 13386–13391.PubMedCrossRefGoogle Scholar
  80. Yoshioka, K., Nakashita, H., Klessig, D. F., & Yamaguchi, I. (2001). Probenazole induces systemic acquired resistance in Arabidopsis with a novel type of action. Plant Journal, 25, 149–157.PubMedCrossRefGoogle Scholar
  81. Zimmerli, L., Jakab, G., Métraux, J.-P., & Mauch-Mani, B. (2000). Potentiation of pathogen-specific defence mechanisms in Arabidopsis by β-aminobutyric acid. Proceedings of the National Academy of Sciences of the USA, 97, 12920–12925.PubMedCrossRefGoogle Scholar

Copyright information

© KNPV 2007

Authors and Affiliations

  1. 1.Plant Biochemistry & Molecular Biology Group, Department of Plant PhysiologyRWTH Aachen UniversityAachenGermany

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