Induced resistance in plants and the role of pathogenesis-related proteins

European Journal of Plant Pathology

Volumn 103, Issue 9, 1997, Pages 753-765

  Van Loon, L C ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Induced systemic resistance; Pathogenesis related proteins; Plant growth promoting rhizobacteria; Salicylic acid; Systemic acquired resistance

Indexed keywords

PATHOGENESIS; PLANT; PROTEIN; RESISTANCE MANAGEMENT;

EID: 0031417776     PISSN: 09291873     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1008638109140     Document Type: Short Survey

References (107)

1. Agrios GN (1988) Plant Pathology, 3rd Ed. Academic Press Inc., San Diego USA
2. Ahl P and Gianinazzi S (1982) b-Protein as a constitutive component in highly (TMV) resistant interspecific hybrids of Nicotiana glutinosa x Nicotiana debneyi. Plant Science Letters 26: 173-181
3. Alexander D, Goodman RM, Gut-Rella M, Glascock C, Weyman K, Friedrich L, Maddox D, Ahl-Goy P, Luntz T, Ward E and Ryals J (1993) Increased tolerance to two oomycete pathogens intransgenic tobacco expressing pathogenesis-related protein 1a. Proceedings of the National Academy of Sciences USA 90: 7327-7331
4. Bowling SA, Guo A, Cao H, Gordon AS, Klessig DF and Dong X (1994) A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. The Plant Cell 6: 1845-1857
5. Bozarth RF and Ross AF (1964) Systemic resistance induced by localized virus infections: extent of changes in uninfected plant parts. Virology 24: 446-455
6. Brederode FT, Linthorst HJM and Bol JF (1991) Differential induction of acquired resistance and PR gene expression in tobacco by virus infection, ethephon treatment, UV light and wounding. Plant Molecular Biology 17: 1117-1125
7. Broekaert WF, Terras FRG, Cammue BPA and Osborn RW (1995) Plant defensins: novel antimicrobial peptides as components of the host defense system. Plant Physiology 108: 1353-1358
8. Broglie K, Chet I, Holliday M, Cressman R, Biddle P, Knowlton S, Mauvais CJ and Broglie R (1991) Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science 254: 1194-1197
9. Cameron RK, Dixon R and Lamb C (1994) Biologically induced systemic acquired resistance in Arabidopsis thaliana. The Plant Journal 5: 715-725
10. Cao H, Bowling SA, Gordon AS and Dong X (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. The Plant Cell 6: 1583-1592
11. Crute IR and Pink DAC (1996) Genetics and utilization of pathogen resistance in plants. The Plant Cell 8: 1747-1755
12. Davis RE and Ross AF (1968) Increased hypersensitivity induced in tobacco by systemic infection by potato virus Y. Virology 34: 509-520
13. De Laat AMM and Van Loon LC (1983) The relationship between stimulated ethylene production and symptom expression in virus-infected tobacco leaves. Physiological Plant Pathology 22: 261-273
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
15. Dean RA and Kuc J (1987) Rapid lignification in response to wounding and infection as a mechanism for induced systemic protection in cucumber. Physiological and Molecular Plant Pathology 31: 69-81
16. Delaney TP, Uknes S, Vernooij B, Friedrich L, Weymann K, Negrotto D, Gaffney T, Gut-Rella M, Kessmann H, Ward E and Ryals J (1994). A central role of salicylic acid in plant disease resistance. Science 266: 1247-1250
17. Delaney T, Friedrich L and Ryals J (1995) Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proceedings of the National Academy of Sciences USA 92: 6602-6606
18. Dietrich RA, Delaney TP, Uknes SJ, Ward ER, Ryals JA and Dangl JL (1994) Arabidopsis mutants simulating disease resistance response. Cell 77: 565-577
19. Doss M and Hevisi M (1981) Systemic acquired resistance of cucumber to Pseudomonas lachrymans as expressed in suppression of symptoms, but not in multiplication of bacteria. Acta Phytopathologica Academiae Scientiarum Hungaricae 16: 269-272
20. Duijff BJ, Gianinazzi-Pearson V and 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
21. Eyal Y and Fluhr R (1991) Cellular and molecular biology of pathogenesis related proteins. Oxford Surveys of Plant Molecular & Cell Biology 7: 223-254
22. Fraser RSS (1979) Systemic consequences of the local lesion reaction to tobacco mosaic virus in a tobacco variety lacking the N gene for hypersensitivity. Physiological Plant Pathology 14: 383-394
23. Fraser RSS (1982) Are 'pathogenesis-related' proteins involved in acquired systemic resistance of tobacco plants to tobacco mosaic virus? Journal of General Virology 58: 305-313
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
25. Gianinazzi S and Ahl P (1983) The genetic and molecular basis of b-proteins in the genus Nicotiana. Netherlands Journal of Plant Pathology 89: 275-281
26. Greenberg JT, Guo A, Klessig DF and Ausubel FM (1994) Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell 77: 551-563
27. Hammerschmidt R and Kuc J (1995) Induced Resistance to Disease in Plants. Kluwer Academic Publishers, Dordrecht, The Netherlands
28. Hammond-Kosack KE and Jones JDG (1996) Resistance gene-dependent plant defense responses. The Plant cell 8: 1773-1791
29. Heino P, Sandman G, Lang V, Nordin K and Palva ET (1990) Abscisic acid deficiency prevents development of freezing tolerance in Arabidopsis thaliana (L.) Heynh.. Theoretical and Applied Genetics 79: 801-806
30. Hejgaard J, Jacobsen S, Björn S and Kragh KM (1992) Antifungal activity of chitin-binding PR-4 type proteins from barley grain and stressed leaf. FEBS Letters 307: 389-392
31. Hoffland E, Pieterse CMJ, Bik L and Van Pelt JA (1995) Induced systemic resistance in radish is not associated with accumulation of pathogenesis-related proteins. Physiological and Molecular Plant Pathology 46: 309-320
32. Hoffland E, Hakulinen J and Van Pelt JA (1996) Comparison of systemic resistance induced by avirulent and non-pathogenic Pseudomonas species. Phytopathology 86: 757-762
33. Jach G, Görnhardt B, Mundy J, Logemann J, Pinsdorf E, Leah R, Schell J and Maas C (1995) Enhanced quantitative resistance against fungal disease by combinatorial expression of different barley antifungal proteins in transgenic tobacco. Plant Journal 8: 97-109
34. Jongedijk E, Tigelaar H, Van Roekel JSC, Bres-Vloemans SA, Dekker I, Van den Elzen PJM, Cornelissen BJC and Melchers LS (1995) Synergistic activity of chitinases and β-1,3-glucanases enhances fungal resistance in transgenic tomato plants. Euphytica 85: 173-180
35. Kader JC (1997) Lipid-transfer proteins: a puzzling family of plant proteins. Trends in Plant Science 2: 66-70
36. Kassanis B, Gianinazzi S and White RF (1974) A possible explanation of the resistance of virus-infected tobacco to second infection. Journal of General Virology 23: 11-16
37. Kauffmann S, Legrand M, Geoffroy P and Fritig B (1987) Biological function of 'pathogenesis-related' proteins: four PR proteins of tobacco have 1,3-β-glucanase activity. The EMBO Journal 6: 3209-3212
38. Kessmann H, Staub T, Ligon J, Oostendorp M and Ryals J (1994) Activation of systemic acquired disease resistance in plants. European Journal of Plant Pathology 100: 359-369
39. Kloepper JW, Tuzun S and Kuc JA (1992) Proposed definitions related to induced disease resistance. Biocontrol Science and Technology 2: 349-351
40. Kovats K, Binder A and Hohl HR (1991) Cytology of induced systemic resistance of cucumber to Colletotrichum lagenarium. Planta 183: 484-490
41. Kuc J (1982) Induced immunity to plant disease. Bioscience 32: 854-860
42. Kuc J (1983) Induced systemic resistance in plants to diseases caused by fungi and bacteria. In: Bailey JA and Deverall BJ (eds) The Dynamics of Host Defence (pp. 191-221) Academic Press Australia, North Ryde, NSW 2113
43. Lawton K, Uknes S, Friedrich L, Gaffney T, Alexander D, Goodman R, Métraux JP, Kessmann H, Ahl-Goy P, Gut Rella M, Ward E and Ryals J (1993) The molecular biology of systemic acquired resistance. In: Fritig B and Legrand M (eds) Mechanisms of Plant Defense Responses (pp. 422-432) Kluwer Academic Publishers, Dordrecht, the Netherlands
44. Leeman M, Van Pelt JA, Den Ouden FM, Heinsbroek M, Bakker PAHM and Schippers B (1995a) 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
45. Leeman M, Van Pelt JA, Den Ouden FM, Heinsbroek M, Bakker PAHM and Schippers B (1995b) Induction of systemic resistance against fusarium wilt of radish by lipopolysaccharides of Pseudomonas fluorescens. Phytopathology 85: 1021-1027
46. Leeman M, Den Ouden FM, Van Pelt JA, Dirkx FPM, Steijl H, Bakker PAHM and Schippers B (1996) Iron availability affects induction of systemic resistance to fusarium wilt of radish by Pseudomonas fluorescens. Phytopathology 86: 149-155
47. Linthorst HJM (1991) Pathogenesis-related proteins of plants. Critical Reviews in Plant Sciences 10: 123-150
48. Liu D, Raghothama KG, Hasegawa PM and Bressan RA (1994) Osmotin overexpression in potato delays development of disease symptoms. Proceedings of the National Academy of Sciences USA 91: 1888-1892
49. Liu L, Kloepper JW and Tuzun S (1995a) Induction of systemic resistance in cucumber against fusarium wilt by plant growth-promoting rhizobacteria. Phytopathology 85: 695-698
50. Liu L, Kloepper JW and Tuzun S (1995b) Induction of systemic resistance in cucumber against angular leaf spot by plant growth-promoting rhizobacteria. Phytopathology 85: 843-847
51. Lynch JM (1976) Products of soil microorganisms in relation to plant growth. CRC Critical Reviews in Microbiology 5: 67-107
52. Mauch F and Staehelin LA (1989) Functional implications of the subcellular localization of ethylene-induced chitinase and β-1,3-glucanase in bean leaves. The Plant Cell 1: 447-457
53. Maurhofer M, Hase C, Meuwly P, Métraux JP and Défago G (1994) Induction of systemic resistance of tobacco to tobacco necrosis virus by the root-colonizing Pseudomonas fluorescens strain CHAO: Influence of the gacA gene and of pyoverdine production. Phytopathology 84: 139-146
54. Mohapatra SS, Poole RJ and Dhindsa RS (1988) Abscisic acid-regulated gene expression in relation to freezing tolerance in alfalfa. Plant Physiology 87: 468-473
55. Mölders W, Buchala A and Métraux JP (1996) Transport of salicylic acid in tobacco necrosis virus-infected cucumber plants. Plant Physiology 112: 787-792
56. Murakishi HH and Carlson PS (1976) Regeneration of virus-free plants from dark green islands of tobacco mosaic virus-infected tobacco leaves. Phytopathology 66: 931-932
57. Neuhaus JM, Ahl-Goy P, Hinz U, Flores S and Meins FJ (1991) High-level expression of a tobacco chitinase gene in Nicotiana sylvestris: susceptibility of transgenic plants to Cercospora nicotianae infection. Plant Molecular Biology 16: 141-151
58. Niderman T, Genetet I, Bruyère T, Gees R, Stintzi A, Legrand M, Fritig B and Mösinger E (1995) Pathogenesis-related PR-1 proteins are antifungal; isolation and characterization of three 14-kilodalton proteins of tomato and of a basic PR-1 of tobacco with inhibitory activity against Phytophthora infestans. Plant Physiology 108: 17-27
59. Nielsen KK, Mikkelsen JD, Kragh KM and Bojsen K (1993) An acidic class III chitinase in sugar beet: induction by Cercospora beticola, characterization, and expression in transgenic tobacco plants. Molecular Plant-Microbe Interactions 6: 496-506
60. Osbourn AE (1996) Preformed antimicrobial compounds and plant defense against fungal attack. The Plant Cell 8: 1821-1831
61. Pieterse CMJ, Van Wees SCM, Hoffland E, Van Pelt JA and 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
62. Ponstein AS, Bres-Vloemans SA, Sela-Buurlage MB, Van den Elzen, PJM, Melchers LS and Cornelissen BJC (1994) A novel pathogen- and wound-inducible tobacco (Nicotiana tabacum) protein with antifungal activity. Plant Physiology 104: 109-118
63. Raaijmakers JM, Van der Sluis I, Van den Hout M, Bakker PAHM and Schippers B (1995a) Dispersal of wild-type and genetically-modified Pseudomonas spp from treated seeds or soil to aerial parts of radish plants. Soil Biology and Biochemistry 27: 1473-1478
64. Raaijmakers JM, Leeman M, Van Oorschot MMP, Van der Sluis I, Schippers B and Bakker PAHM (1995b) Dose-response relationships in biological control of fusarium wilt of radish by Pseudomonas spp. Phytopathology 85: 1075-1081
65. Rasmussen JB, Hammerschmidt R and Zook MN (1991) Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv. syringae. Plant Physiology 97: 1342-1347
66. Ricci P, Bonnet P, Huet JC, Sallantin M, Beauvais-Cante F, Bruneteau M, Billard V, Michel G and Pernollet JC (1989) Structure and activity of proteins from pathogenic fungi Phytophthora eliciting necrosis and acquired resistance in tobacco. European Journal of Biochemistry 183: 555-563
67. Roberts DA (1982) Systemic acquired resistance induced in hyper-sensitive plants by nonnecrotic localized viral infections. Virology 122: 207-209
68. Ross AF (1961a) Localized acquired resistance to plant virus infection in hypersensitive hosts. Virology 14: 329-339
69. Ross AF (1961b) Systemic acquired resistance induced by localized virus infections in plants. Virology 14: 340-358
70. Ross AF (1966) Systemic effects of local lesion formation. In: Beemster ABR and Dijkstra J (eds) Viruses of Plants (pp. 127-150) North Holland Publ Comp, Amsterdam, The Netherlands
71. Ryals J, Uknes S and Ward E (1994) Systemic acquired resistance. Plant Physiology 104: 1109-1112
72. Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY and Hunt MD (1996) Systemic acquired resistance. The Plant Cell 8: 1809-1819
73. Ryan CA (1990) Proteinase inhibitors in plants: genes for improving defenses against insects and pathogens. Annual Review of Phytopathology 28: 425-449
74. Schlumbaum AF, Mauch F, Vögeli U and Boller T (1986) Plant chitinases are potent inhibitors of fungal growth. Nature 324: 365-367
75. Shulaev V, Leon J and Raskin I (1995) Is salicylic acid a transported signal of systemic acquired resistance in tobacco? The Plant Cell 7: 1691-1701
76. Singh NK, Bracker CA, Hasegawa PM, Handa AK, Buckel S, Hermodson MA, Pfankoch E, Regnier FE and Bressan RA (1987) Characterization of osmotin: a thaumatin-like protein associated with osmotic adaptation in plant cells. Plant Physiology 85: 529-536
77. Skriver K and Mundy J (1990) Gene expression in response to abscisic acid and osmotic stress. The Plant Cell 2: 503-512
78. Stintzi A, Heitz T, Kauffmann S, Legrand M and Fritig B (1991) Identification of a basic pathogenesis-related, thaumatin-like protein of virus-induced tobacco as osmotin. Physiological and Molecular Plant Pathology 38: 137-146
79. Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S, Dincher S, Chandler D, Slusarenko A, Ward E and Ryals J (1992) Acquired resistance in Arabidopsis. The Plant Cell 4: 645-656
80. Urban LA, Sherwood JL, Rezende JAM and Melcher U (1990) Examination of mechanisms of cross protection with non-transgenic plants. In: Fraser RSS (ed) Recognition and Response in Plant-Virus Interactions (pp. 415-426) Springer-Verlag, Berlin Heidelberg, Germany
81. Van den Elzen PJM, Jongedijk E, Melchers LS and Cornelissen BJC (1993) Virus and fungal resistance: from laboratory to field. Philosophical Transactions of the Royal Society London B 342: 271-278
82. Van Kan JAL, Cornelissen BJC and Bol JF (1988) A virus-inducible tobacco gene encoding a glycine-rich protein shares putative regulatory elements with the ribulose bisphosphate carboxylase small subunit gene. Molecular Plant-Microbe Interactions 1: 107-112
83. Van Loon LC (1975) Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var. 'Samsun' and 'Samsun NN' IV. Similarity of qualitative changes of specific proteins after infection with different viruses and their relationship to acquired resistance. Virology 67: 566-575
84. Van Loon LC (1977) Induction by 2-chloroethylphosphonic acid of viral-like lesions, associated proteins, and systemic resistance in tobacco. Virology 80: 417-420
85. Van Loon LC (1983a) Mechanisms of resistance in virus-infected plants. In: Bailey JA and Deverall BJ (eds) The Dynamics of Host Defence (pp. 123-190) Academic Press Australia, North Ryde, NSW 2113
86. Van Loon LC (1983b) The induction of pathogenesis-related proteins by pathogens and specific chemicals. Netherlands Journal of Plant Pathology 89: 265-273
87. Van Loon LC (1989) Stress proteins in infected plants. In: Kosuge T and Nester EW (eds) Plant-Microbe Interactions, Molecular and Genetic Perspectives Vol 3 (pp. 198-237) MacGraw-Hill Publ Comp, New York, USA
88. Van Loon LC and Antoniw JF (1982) Comparison of the effects of salicylic acid and ethephon with virus-induced hypersensitivity and acquired resistance in tobacco. Netherlands Journal of Plant Pathology 88: 237-256
89. Van Loon LC and Gerritsen YAM (1989) Localization of pathogenesis-related proteins in infected and non-infected leaves of Samsun NN tobacco during the hypersensitive reaction to tobacco mosaic virus. Plant Science 63: 131-140
90. Van Loon LC and Van Kammen A (1970) Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var. 'Samsun' and 'Samsun NN' II. Changes in protein constitution after infection with tobacco mosaic virus. Virology 40: 199-211
91. Van Loon LC, Pierpoint WS, Boller T and Conejero V (1994) Recommendations for naming plant pathogenesis-related proteins. Plant Molecular Biology Reporter 12: 245-264
92. Van Peer R, Niemann GJ 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
93. Van Peer R and Schippers B (1992) Lipopolysaccharides of plant-growth promoting Pseudomonas sp. strain WCS417r induce resistance in carnation to fusarium wilt. Netherlands Journal of Plant Pathology 98: 129-139
94. Van Wees SCM, Pieterse CMJ, Trijssenaar A, Van 't Westende Y, Hartog F and Van Loon LC (1997) Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria. Molecular Plant-Microbe Interactions 10: 716-724
95. Vernooij B, Friedrich L, Morse A, Reist R, Kolditz-Jawhar 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. The Plant Cell 6: 959-965
96. Vierheilig H, Alt M, Neuhaus JM, Boller T and Wiemken A (1993) Colonization of transgenic Nicotiana sylvestris plants, expressing different forms of Nicotiana tabacum chitinase, by the root pathogen Rhizoctonia solani and by the mycorrhizal symbiont Glomus mossae. Molecular Plant-Microbe Interactions 6: 261-264
97. Vierling E (1991) The roles of heat shock proteins in plants. Annual Review of Plant Physiology and Plant Molecular Biology 42: 579-620
98. Vigers AJ, Roberts WK and Selitrennikof CP (1991) A new family of plant antifungal proteins. Molecular Plant-Microbe Interactions 4: 315-323
99. Vigers AJ, Wiedema S, Roberts WK, Legrand M, Selitrennikoff CP and Fritig B (1992) Thaumatin-like pathogenesis-related proteins are antifungal. Plant Science 83: 155-161
100. Ward ER, Uknes SJ, Williams SC, Dincher SS, Wiederhold DL, Alexander DC, Ahl-Goy P, Métraux JP and Ryals JA (1991) Coordinate gene activity in response to agents that induce systemic acquired resistance. The Plant Cell 3: 1085-1094
101. Wei G, Kloepper JW 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
102. Whenham RJ and Fraser RSS (1981) Effect of systemic and locallesion-forming strains of tobacco mosaic virus on abscisic acid concentration in tobacco leaves: consequences for the control of leaf growth. Physiological Plant Pathology 18: 267-278
103. Xu Y, Chang PFL, Liu D, Narasimhan ML, Raghothama KG, Hasegawa PM and Bressan RA (1994) Plant defense genes are synergistically induced by ethylene and methyl jasmonate. The Plant Cell 6: 1077-1085
104. Yalpani N, Leon J, Lawton M and Raskin I (1993) Pathway of salicylic acid biosynthesis in healthy and virus-inoculated tobacco. Plant Physiology 103: 315-321
105. Ye XS, Järlfors U, Tuzun S, Pan SQ and Kuc J (1992) Biochemical changes in cell walls and cellular responses of tobacco leaves related to systemic resistance to blue mold (Peronospora tabacina) induced by tobacco mosaic virus. Canadian Journal of Botany 70: 49-57
106. Zhu BL, Chen THH and Li PH (1996) Analysis of late-blight disease resistance and freezing tolerance in transgenic potato plants expressing sense and antisense genes for an osmotin-like protein. Planta 198: 70-77
107. Zhu Q, Maher EA, Masoud S, Dixon RA and Lamb CJ (1994) Enhanced protection against fungal attack by constitutive coexpression of chitinase and glucanase genes in transgenic tobacco. BioTechnology 12: 807-812