Systemic Acquired Resistance of Pepper to Microbial Pathogens

Journal of Phytopathology

Volumn 159, Issue 6, 2011, Pages 393-400

  Choi, Hyong Woo ^a   Hwang, Byung Kook ^a  

^a Korea University   (South Korea)

Author keywords

Capsicum annuum; Defence related genes; Disease management; Inducible defence responses; Salicylic acid; Systemic acquired resistance

Indexed keywords

BIOCHEMICAL COMPOSITION; BIOCONTROL AGENT; BIOLOGICAL CONTROL; DISEASE RESISTANCE; GENE EXPRESSION; IMMUNITY; MICROBIAL ACTIVITY; MOLECULAR ANALYSIS; PATHOGENICITY; SALICYLIC ACID; SIGNALING;

CAPSICUM ANNUUM;

EID: 79954589598     PISSN: 09311785     EISSN: 14390434     Source Type: Journal    
DOI: 10.1111/j.1439-0434.2010.01781.x     Document Type: Review

References (82)

1. Abbasi PA, Soltani N, Cuppels DA, Lazarovits G. (2002) Reduction of bacterial spot disease severity on tomato and pepper plants with foliar applications of ammonium lignosulfonate and potassium phosphate. Plant Dis 86:1232-1236.
2. Amzalek E, Cohen Y. (2007) Comparative efficacy of systemic acquired resistance-inducing compounds against rust infection in sunflower plants. Phytopathology 97:179-186.
3. Apel K, Hirt H. (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373-399.
4. Arasimowicz M, Floryszak-Wieczorek J. (2007) Nitric oxide as a bioactive signalling molecule in plant stress responses. Plant Sci 172:876-887.
5. Asai S, Ohta K, Yoshioka H. (2008) MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative burst in Nicotiana benthamiana. Plant Cell 20:1390-1406.
6. Baysal Ö, Turgut C, Mao G. (2005) Acibenzolar-S-methyl induced resistance to Phytophthora capsici in pepper leaves. Biol Plant 49:599-604.
7. Bindschedler LV, Dewdney J, Blee KA et al. (2006) Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J 47:851-863.
8. Buonaurio R, Scarponi L, Ferrara M, Sidoti P, Bertona A. (2002) Induction of systemic acquired resistance in pepper plants by acibenzolar-S-methyl against bacterial spot disease. Eur J Plant Pathol 108:41-49.
9. Cho BH, Smedegaard-Petersen V. (1986) Induction of resistance to Erysiphe graminis f. sp. hordei in near isogenic barley lines. Phytopathology 76:301-305.
10. Choi HW, Kim YJ, Lee SC, Hong JK, Hwang BK. (2007) Hydrogen peroxide generation by the pepper extracellular peroxidase CaPO2 activates local and systemic cell death and defense response to bacterial pathogens. Plant Physiol 145:890-904.
11. Choi HW, Lee BG, Kim NH, Park Y, Lim CW, Song HK, Hwang BK. (2008) A role for a menthone reductase in resistance against microbial pathogens in plants. Plant Physiol 148:383-401.
12. Choi HW, Lee DH, Hwang BK. (2009) The pepper calmodulin gene CaCaM1 is involved in reactive oxygen species and nitric oxide generation required for cell death and the defense response. Mol Plant-Microbe Interact 22:1389-1400.
13. Cohen Y. (1994) 3-Aminobutyric acid induces systemic resistance against Peronospora tabacina. Physiol Mol Plant Pathol 44:273-288.
14. 14C-DL-3-aminobutyric acid in tomato plants in relation to induced resistance against Phytophthora infestans. Physiol Mol Plant Pathol 45:441-446.
15. Cohen Y, Reuveni M, Baider A. (1999) Local and systemic activity of BABA (DL-3-aminobutyric acid) against Plasmopara viticola in grapevines. Eur J Plant Pathol 105:351-361.
16. Conrath U, Beckers GJ, Flors V et al. (2006) Priming: getting ready for battle. Mol Plant-Microbe Interact 19:1062-1071.
17. Díaz J, Silvar C, Varela MM, Berneal A, Merino F. (2005) Fusarium confers protection against several mycelial pathogens of pepper plants. Plant Pathol 54:773-780.
18. Görlach J, Volrath S, Knauf-Beiter G 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.
19. Gozzo F. (2003) Systemic acquired resistance in crop protection: from nature to a chemical approach. J Agric Food Chem 51:4487-4503.
20. Grant MR, Jones JD. (2009) Hormone (dis)harmony moulds plant health and disease. Science 324:750-752.
21. Grant M, Lamb C. (2006) Systemic immunity. Curr Opin Plant Biol 9:414-420.
22. den Hond F. (1998) Systemic acquired resistance: a case of innovation in crop protection. Pestic Outlook 9:18-23.
23. Hong JK, Hwang BK. (2005) Functional characterization of PR-1 protein, β-1, 3-glucanase and chitinase genes during defense response to biotic and abiotic stresses in Capsicum annuum. Plant Pathol J 21:195-206.
24. Hong JK, Hwang BK, Kim CH. (1999) Induction of local and systemic resistance to Colletotrichum coccodes in pepper plants by DL-β-amino-n-butyric acid. J Phytopathol 147:193-198.
25. Hong JK, Jung HW, Kim YJ, Hwang BK. (2000) Pepper gene encoding a basic class II chitinase is inducible by pathogen and ethephon. Plant Sci 159:39-49.
26. Hong JK, Lee SC, Hwang BK. (2005) Activation of pepper basic PR-1 gene promoter during defense signaling to pathogen, abiotic and environmental stresses. Gene 356:169-180.
27. Hunt MD, Neuenschwander UH, Delaney TP, Weymann KB, Friedrich LB, Lawton KA, Steiner HY, Ryals JA. (1996) Recent advances in systemic acquired resistance research-a review. Gene 179:89-95.
28. Hwang BK. (2001) Cytology, physiology and molecular genetics of resistance to Phytophthora blight in pepper plants. Plant Pathol J 17:9-21.
29. Hwang BK, Heitefuss R. (1982) Induced resistance of spring barley to Erysiphe graminis f.sp. hordei. J Phytopathol 103:41-47.
30. Hwang IS, Hwang BK. (2010) The pepper 9-lipoxygenase gene CaLOX1 functions in defense and cell death responses to microbial pathogens. Plant Physiol 152:948-967.
31. Hwang BK, Kim ES. (1992) Protection of pepper plants against Phytophthora blight by an avirulent isolate of Phytophthora capsici. Korean J Plant Pathol 8:1-7.
32. Hwang BK, Kim CH. (1995) Phytophthora blight of pepper and its control in Korea. Plant Dis 79:221-227.
33. Hwang BK, Sung NK. (1989) Effect of metalaxyl on capsidiol production in stems of pepper plants infected with Phytophthora capsici. Plant Dis 73:748-751.
34. Hwang BK, Kim WB, Kim WK. (1989) Ultrastructure at the host-parasite interface of Phytophthora capsici in roots and stems of Capsicum annuum. J Phytopathol 127:305-315.
35. Hwang BK, Sunwoo JY, Kim YJ, Kim BS. (1997) Accumulation of β-1, 3-glucanase isoforms, and salicylic acid in the DL-β-amino-n-butyric acid-induced resistance response of pepper stems to Phytophthora capsici. Physiol Mol Plant Pathol 51:305-322.
36. Jakab G, Cottier V, Toquin V, Rigoli G, Zimmerli L, Métraux JP, Mauch-Mani B. (2001) β-Aminobutyric acid-induced resistance in plants. Eur J Plant Pathol 107:29-37.
37. Jung HW, Hwang BK. (2000) Pepper gene encoding a basic β-1, 3-glucanase is differentially expressed in pepper tissues upon pathogen infection and ethephon or methyl jasmonate. Plant Sci 159:97-106.
38. Jung HW, Kim W, Hwang BK. (2003) Three pathogen-inducible genes encoding lipid transfer protein from pepper are differentially activated by pathogens, abiotic, and environmental stresses. Plant Cell Environ 26:915-928.
39. Jung HW, Kim KD, Hwang BK. (2005) Identification of pathogen-responsive regions in the promoter of a pepper lipid transfer protein gene (CALTPI) and the enhanced resistance of the CALTPI transgenic Arabidopsis against pathogen and environmental stresses. Planta 221:361-373.
40. Keshavarzi M, Soylu S, Brown I, Bonas U, Nicole M, Rossiter J, Mansfield J. (2004) Basal defenses induced in pepper by lipopolysaccharides are suppressed by Xanthomonas campestris pv. vesicatoria. Mol Plant-Microbe Interact 17:805-815.
41. Kessmann H, Staub T, Hofmann C, Maetzke T, Herzog J. (1994) Induction of systemic acquired disease resistance in plants by chemicals. Annu Rev Phytopathol 32:439-459.
42. Kim YJ, Hwang BK. (2000) Pepper gene encoding a basic pathogenesis-related 1 protein is pathogen and ethylene inducible. Physiol Plant 108:51-60.
43. Kim NH, Choi HW, Hwang BK. (2010) Xanthomonas campestris pv. vesicatoria effector AvrBsT induces cell death in pepper but suppresses defense responses in tomato. Mol Plant-Microbe Interact 23:1069-1082.
44. Lamb CJ, Dixon RA. (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251-275.
45. Leadbeater A, Staub T. (2007) Exploitation of induced resistance: a commercial perspective. In: Walters D, Newton A, Lyon G. (eds) Induced Resistance for Plant Defence: A Sustainable Approach to Crop Protection. Oxford, UK, Blackwell Publishing, pp 229-242.
46. Lee SC, Hwang BK. (2005) Induction of some defense-related genes and oxidative burst is required for the establishment of systemic acquired resistance in Capsicum annuum. Planta 221:790-800.
47. Lee JY, Kim BS, Lim SW, Lee BK, Kim CH, Hwang BK. (1999) Field control of Phytophthora blight of pepper plants with antagonistic rhizo-bacteria and DL-β-amino-n-butyric acid. Plant Pathol J 15:217-222.
48. Lee YK, Hong JK, Hippe-Sanwald S, Hwnag BK. (2000) Histological and ultrastructural comparisons of compatible, incompatible and DL-β-amino-n-butyric acid-induced resistance responses of pepper stems to Phytophthora capsici. Physiol Mol Plant Pathol 57:269-280.
49. Lee SC, Kim YJ, Hwang BK. (2001) A pathogen-induced chitin-binding protein gene from pepper: its isolation and differential expression in pepper tissues treated with pathogens, ethephon, methyl jasmonate or wounding. Plant Cell Physiol 42:1321-1330.
50. Lee SC, Hwang IS, Choi HW, Hwang BK. (2008) Involvement of the pepper antimicrobial protein CaAMP1 gene in broad spectrum disease resistance. Plant Physiol 148:1004-1020.
51. Lee S, Hong JC, Jeon WB, Chung YS, Sung S, Choi D, Joung YH, Oh BJ. (2009) The salicylic acid-induced protection of non-climacteric unripe pepper fruit against Colletotrichum gloeosporioides is similar to the resistance of ripe fruit. Plant Cell Rep 28:1573-1580.
52. Lefebvre V, Palloix A. (1996) Both epistatic and additive effects of QTLs are involved in polygenic induced resistance to disease: a case study, the interaction pepper-Phytophthora capsici Leonian. Theor Appl Genet 93:503-511.
53. Madhusudhan KN, Deepak SA, Prakash HS, Agrawal GK, Jwa NS, Rakwal R. (2008) Acibenzolar-S-methyl (ASM)-induced resistance against tobamoviruses involves induction of RNA-dependent RNA polymerase (RdRp) and alternative oxidase (AOX) genes. J Crop Sci Biotech 11:127-134.
54. Matheron ME, Porchas M. (2002) Suppression of Phytophthora root and crown rot on pepper plants treated with acibenzolar-S-methyl. Plant Dis 86:292-297.
55. Métraux JP. (2001) Systemic acquired resistance and salicylic acid: current state of knowledge. Eur J Plant Pathol 107:13-18.
56. Métraux JP, Signer H, Ryals J, Ward E, Wyss-Benz M, Gaudin J, Raschdorf K, Schmid E, Blum W, Inverardi B. (1990) Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250:1004-1006.
57. Murray DC, Walters DR. (1992) Increased photosynthesis and resistance to rust infection in upper, uninfected leaves of rusted broad bean (Vicia faba L.). New Phytol 120:235-242.
58. Newman MA, von Roepenack-Lahaye E, Parr A, Daniels MJ, Dow JM. (2002) Prior exposure to lipopolysaccharide potentiates expression of plant defenses in response to bacteria. Plant J 29:487-495.
59. Obrdovic A, Jones JB. (2004) Management of tomato bacterial spot in the field by foliar application of bacteriophages and SAR inducers. Plant Dis 88:736-740.
60. Oka Y, Cohen Y, Spiegel Y. (1999) Local and systemic induced resistance to the root-knot nematode in tomato by DL-β-amino-n-butyric acid. Phytopathology 89:1138-1143.
61. Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF. (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318:113-116.
62. Pieterse CM, Van Loon LC. (2007) Signaling cascades involved in induced resistance. In: Walters D, Newton A, Lyon G. (eds) Induced Resistance for Plant Defence: A Sustainable Approach to Crop Protection. Oxford, UK, Blackwell Publishing, pp 65-88.
63. Reignault P, Walters D. (2007). Topical application of inducers for disease control. In: Walters D, Newton A, Lyon G. (eds) Induced Resistance for Plant Defence: A Sustainable Approach to Crop Protection. Oxford, UK, Blackwell Publishing, pp 179-200.
64. Reuveni R, Dor G, Reuveni M. (1998) Local and systemic control of powdery mildew (Leveillula taurica) on pepper plants by foliar spray of mono-potassium phosphate. Crop Prot 17:703-709.
65. Romeiro RS, Kimura O. (1997) Induced resistance in pepper leaves infiltrated with purified bacterial elicitors from Xanthomonas campestris pv. vesicatoria. J Phytopathol 145:11-12.
66. Romero AM, Kousik CS, Ritchie DF. (2001) Resistance to bacterial spot in bell pepper induced by acibenzolar-S-methyl. Plant Dis 85:189-194.
67. Rustérucci C, Espunya MC, Díaz M, Chabannes M, Martínez MC. (2007) S-nitrosoglutathione reductase affords protection against pathogens in Arabidopsis, both locally and systemically. Plant Physiol 143:1282-1392.
68. Ryals J, Uknes S, Ward E. (1994) Systemic acquired resistance. Plant Physiol 104:1109-1112.
69. Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD. (1996) Systemic acquired resistance. Plant Cell 8:1809-1819.
70. Sahin F, Miller SA. (1998) Resistance in Capsicum pubescens to Xanthomonas campestris pv. vesicatoria Pepper Race 6. Plant Dis 82:794-799.
71. Sang MK, Kim JG, Kim KD. (2010) Biocontrol activity and induction of systemic resistance in pepper by compost water extracts against Phytophthora capsici. Phytopathology 100:774-783.
72. Sarowar S, Kim YJ, Kim KD, Hwang BK, Ok SH, Shin JS. (2009) Overexpression of lipid transfer protein (LTP) genes enhances resistance to plant pathogens and LTP functions in long-distance systemic signaling in tobacco. Plant Cell Rep 28:419-427.
73. Siegrist J, Orober M, Buchenauer H. (2000) β-aminobutyric acid-mediated enhancement of resistance in tobacco to tobacco mosaic virus depends on the accumulation of salicylic acid. Physiol Mol Plant Pathol 56:95-106.
74. Silvar C, Merino F, Díaz Z. (2008) Resistance in pepper plants induced by Fusarium oxysporum f.sp. lycopersici involves different defense-related genes. Plant Biol 11:68-74.
75. Sunwoo JY, Lee YK, Hwang BK. (1996) Induced resistance against Phytophthora capsici in pepper plants in response to DL-β-amino-n-butyric acid. Eur J Plant Pathol 102:663-670.
76. Torres MA, Jones JDG., Dangl JL. (2005) Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat Genet 37:1130-1134.
77. Uthairatanakij A, da Silva JAT, Obsuwan K. (2007) Chitosan for improving orchid production and quality. Orchid Sci and Biotechnol 1:1-5.
78. Vlot AC, Dempsey DA, Klessig DF. (2009) Salicylic Acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177-206.
79. Walters DR, Walsh D, Newton AC, Lyon GD. (2005) Induced resistance for plant disease control: maximising the efficacy of resistance elicitors. Phytopathology 95:1368-1373.
80. Ward ER, Uknes SJ, Williams SC, Dincher SS, Wiederhold DL, Alexander DC, Ahl-Goy P, Métraux JP, Ryals JA. (1991) Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3:1085-1094.
81. Xuei XL, Järlfors U, Kuć J. (1998) Ultrastructural changes associated with induced systemic resistance of cucumber to disease: host response and development of Colletotrichum lagenarium in systemically protected leaves. Can J Bot 66:1028-1038.
82. Yusuf Y, Sally M. (2004) Effect of treating pepper with benzothiadiazole derivative and non-pathogenic Xanthomonas campestris pathovars on the level of disease caused by Sclerotinia sclerotiorum. Plant Pathol J 3:52-55.