Up-regulation of antioxidants in tobacco by low concentrations of H 2O 2 suppresses necrotic disease symptoms

Phytopathology

Volumn 102, Issue 9, 2012, Pages 848-856

  Hafez, Yaser Mohamed ^a,b   Bacsó, Renáta ^a   Király, Zoltán ^a   Künstler, András ^a   Király, Lóránt ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b Kafrelsheikh University   (Egypt)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; HYDROGEN PEROXIDE; PLANT RNA; VEGETABLE PROTEIN;

ARTICLE; CLASSIFICATION; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; PLANT DISEASE; PLANT LEAF; PSEUDOMONAS; TOBACCO; TOBACCO MOSAIC VIRUS; UPREGULATION; VIROLOGY;

ANTIOXIDANTS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; HYDROGEN PEROXIDE; PLANT DISEASES; PLANT LEAVES; PLANT PROTEINS; PSEUDOMONAS; RNA, PLANT; TOBACCO; TOBACCO MOSAIC VIRUS; UP-REGULATION;

EID: 84865441601     PISSN: 0031949X     EISSN: None     Source Type: Journal    
DOI: 10.1094/PHYTO-01-12-0012-R     Document Type: Article

References (69)

1. Baker, C. J., and Orlandi, E. W. 1995. Active oxygen in plant pathogenesis. Annu. Rev. Phytopathol. 33:299-321.
2. Barba-Espin, G., Diaz-Vivancos, P., Clemente-Moreno, M. J., Albacete, A., Faize, L., Faize, M., Pérez-Alfocea, F., and Hernández, J. A. 2010. Interaction between hydrogen peroxide and plant hormones during germination and the early growth of pea seedlings. Plant Cell Environ. 33:981-994.
3. Barna, B., Ádám, A., and Király, Z. 1993. Juvenility and resistance of a superoxide-tolerant plant to diseases and other stresses. Naturwissenschaften 80:420-422.
4. Barna, B., Smigocki, A. C., and Baker, J. C. 2008. Transgenic production of cytokinin suppresses bacterially induced hypersensitive response symptoms and increases antioxidative enzyme levels in Nicotiana spp. Phytopathology 98:1242-1247.
5. Bendahmane, A., Kanyuka, K., and Baulcombe, D. C. 1999. The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell 11:781-791.
6. Chamnongpol, S., Willekens, H., Moeder, W., Langebartels, C., Sandermann, H., Van Montagu, M., Inzé, D., and Van Camp, W. 1998. Defense activation and enhanced pathogen tolerance induced by H2O2 in transgenic tobacco. Proc. Natl. Acad. Sci. USA 95:5818-5823.
7. Chaouch, S., and Noctor, G. 2010. Myo-inositol abolishes salicylic aciddependent cell death and pathogen defence responses triggered by peroxisomal hydrogen peroxide. New Phytol. 188:711-718.
8. Chivasa, S., Murphy, A. M., Naylor, M., and Carr, J. P. 1997. Salicylic acid interferes with tobacco mosaic virus replication via a novel salicylhydroxamic acid-sensitive mechanism. Plant Cell 9:547-557.
9. Cole, A. B., Király, L., Lane, L. C., Wiggins, E. B., Ross, K., and Schoelz, J. E. 2004. Temporal expression of PR-1 and enhanced mature plant resistance to virus infection is controlled by a single dominant gene in a new Nicotiana hybrid. Mol. Plant-Microbe Interact. 17:976-985.
10. Cole, A. B., Király, L., Ross, K., and Schoelz, J. E. 2001. Uncoupling resistance from cell death in the hypersensitive response of Nicotiana species to Cauliflower mosaic virus infection. Mol. Plant-Microbe Interact. 14:31-41.
11. Coll, N. S., Vercammen, D., Smidler, A., Clover, C., van Breusegem, F., Dangl, J. L., and Epple, P. 2010. Arabidopsis Type I metacaspases control cell death. Science 330:1393-1397.
12. Delaney, T. P., Uknes, S., Vernooij, B., Friedrich, L., Wyman, K., Negrotto, D., Gaffney, T., Gut-Rella, M., Kesssman, H., Ward, E., and Ryals, J. A. 1994. A central role of salicylic acid in plant disease resistance. Science 226:1247-1250.
13. El-Zahaby, H. M., Hafez, Y. M., and Király, Z. 2004. Effect of reactive oxygen species on plant pathogens in planta and on disease symptoms. Acta Phytopathol. Entomol. Hung. 39:325-345.
14. Flor, H. H. 1971. Current status of the gene for gene concept. Annu. Rev. Phytopathol. 9:275-296.
15. Fodor, J., Gullner, G., Ádám, A. L., Barna, B., K?míves, T., and Király, Z. 1997. Local and systemic responses of antioxidants to tobacco mosaic virus infection and to salicylic acid. Plant Physiol. 114:1443-1451.
16. Fung, R. W. M., Gonzalo, M., Fekete, C., Kovacs, L. G., He, Y., Marsh, E., McIntyre, L. M., Schachtman, D. P., and Qiu, W. 2008. Powdery mildew induces defense-oriented reprogramming of the transcriptome in a susceptible but not in a resistant grapevine. Plant Physiol. 146:236-249.
17. Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessman, H., and Ryals, J. 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754-756.
18. Gassmann, W. 2005. Natural variation in the Arabidopsis response to the avirulence gene hopPsyA uncouples the hypersensitive response from disease resistance. Mol. Plant-Microbe Interact. 18:1054-1060.
19. Gechev, T., Gadjev, I., Van Breusegem, F., Inzé, D., Dukiandjiev, S., Toneva, V., and Minkov, I. 2002. Hydrogen peroxide protects tobacco from oxidative stress by inducing a set of antioxidant enzymes. Cell. Mol. Life Sci. 59:708-714.
20. Goodman, R. N., and Novacky, A. J. 1994. The Hypersensitive Reaction in Plants to Pathogens. American Phytopathological Society, St. Paul, MN
21. Greenberg, J. T., and Yao, N. 2004. The role and regulation of programmed cell death in plant-pathogen interactions. Cell. Microbiol. 6:201-211.
22. Hafez, Y. M. 2010. Control of Botrytis cinerea by the resistance inducers benzothiadiazole (BTH) and hydrogen peroxide on white pepper fruits under postharvest storage. Acta Phytopathol. Entomol. Hung. 45:13-29.
23. Hafez, Y. M., and Király, Z. 2003. Role of hydrogen peroxide in symptom expression of barley susceptible and resistant to powdery mildew. Acta Phytopathol. Entomol. Hung. 38:227-236.
24. Halim, V. A., Eschen-Lippold, L., Altmann, S., Birschwilks, M., Scheel, D., and Rosahl, S. 2007. Salicylic acid is important for basal defense of Solanum tuberosum against Phytophthora infestans. Mol. Plant-Microbe Interact. 20:1346-1352.
25. Halliwell, B., and Gutteridge, J. M. C. 1999. Free Radicals in Biology and Medicine. Oxford University Press, Inc., New York.
26. Höller, K., Király, L., Künstler, A., Müller, M., Gullner, G., Fattinger, M., and Zechmann, B. 2010. Enhanced glutathione metabolism is correlated with sulfur induced resistance in Tobacco mosaic virus-infected genetically susceptible Nicotiana tabacum plants. Mol. Plant-Microbe Interact. 23:1448-1459.
27. Hückelhoven, R., and Kogel, K.-H. 2003. Reactive oxygen intermediates in plant-microbe interactions: Who is who in powdery mildew resistance? Planta 216:891-902.
28. Jones, A. M., and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329.
29. Király, L., Hafez, Y. M., Fodor, J., and Király, Z. 2008. Suppression of tobacco mosaic virus-induced hypersensitive-type necrotisation in tobacco at high temperature is associated with down-regulation of NADPH oxidase and superoxide and stimulation of dehydroascorbate reductase. J. Gen. Virol. 89:799-808.
30. Király, L., and Király, Z. 2006. To die or not to die - Is cell death dispensable for resistance during the plant hypersensitive response? Acta Phytopathol. Entomol. Hung. 41:11-21.
31. Király, Z., Barna, B., and Érsek, T. 1972. Hypersensitivity as a consequence, not the cause, of plant resistance to infection. Nature 239:456- 458.
32. Király, Z., Barna, B., Kecskés, A., and Fodor, J. 2002. Down-regulation of antioxidative capacity in a transgenic tobacco which fails to develop acquired resistance to necrotization caused by tobacco mosaic virus. Free Rad. Res. 36:981-991.
33. Király, Z., Hevesi, M., and Klement, Z. 1977. Inhibition of bacterial multiplication in incompatible host-parasite relationships in the absence of the hypersensitive necrosis. Acta Phytopathol. Hung. 12:247-256.
34. Lacombe, S., Rougon-Cardoso, A., Sherwood, E., Peeters, N., Dahlbeck, D., van Esse, H. P., Smoker, M., Rallapalli, G., Thomma, B. P. H. J., Staskawicz, B., Jones, J. D. G., and Zipfel, C. 2010. Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat. Biotechnol. 28:365-369.
35. Laurie-Berry, N., Joardar, V., Street, I. H., and Kunkel, B. N. 2006. The Arabidopsis thaliana JASMONATE INSENSITIVE 1 gene is required for suppression of salicylic acid-dependent defenses during infection by Pseudomonas syringae. Mol. Plant-Microbe Interact. 19:789-800.
36. Lee, H., and Raskin, I. 1999. Purification, cloning, and expression of a pathogen inducible UDP-glucose:salicylic acid glucosyltransferase from tobacco. J. Biol. Chem. 274:36637-36642.
37. Lee, Y. H., Yoon, I. S., Suh, S. C., and Kim, H. I. 2002. Enhanced disease resistance in transgenic cabbage and tobacco expressing a glucose oxidase gene from Aspergillus niger. Plant Cell Rep. 20:857-863.
38. Levine, A., Tenhaken, R., Dixon, R., and Lamb, C. 1994. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583-593.
39. Maruthasalam, S., Liu, Y. L., Sun, C. M., Chen, P. Y., Yu, C. W., Lee, P. F., and Lin, C. H. 2010. Constitutive expression of a fungal glucose oxidase gene in transgenic tobacco confers chilling tolerance through the activation of antioxidative defence system. Plant Cell Rep. 29:1035-1048.
40. McDowell, J. M., and Dangl, J. L. 2000. Signal transduction in the plant immune response. Trends Biochem. Sci. 25:79-82.
41. Meuwly, P., and Métraux, J.-P. 1993. Ortho-anisic acid as internal standard for the simultaneous quantitation of salicylic acid and its putative biosynthetic precursors in cucumber leaves. Anal. Biochem. 214:500-505.
42. Mittler, R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7:405-410.
43. Murphy, A. M., and Carr, J. P. 2002. Salicylic acid has cell-specific effects on Tobacco mosaic virus replication and cell-to-cell movement. Plant Physiol. 128:552-563.
44. Murray, S., Thomson, C., Chini, A., Read, N., and Loake, G. 2002. Characterization of a novel, defense-related Arabidopsis mutant, cir1, isolated by luciferase imaging. Mol. Plant-Microbe Interact. 15:557-566.
45. Nakjarung, K., Mongkolsuk, S., and Vattanaviboon, P. 2003. The oxyR from Agrobacterium tumefaciens: Evaluation of its role in the regulation of catalase and peroxide responses. Biochem. Biophys. Res. Commun. 304:41-47.
46. Ott, P. G., Varga, G. J., Szatmári, Á., Bozsó, Z., Klement, É., Medzihradszky, K. F., Besenyei, E., Czelleng, A., and Klement, Z. 2006. Novel extracellular chitinases rapidly and specifically induced by general bacterial elicitors and suppressed by virulent bacteria as a marker of early basal resistance in tobacco. Mol. Plant-Microbe Interact. 19:161-172.
47. Prasad, B. D., Creissen, G., Lamb, C., and Chatoo, B. B. 2009. Overexpression of rice (Oryza sativa L.) OsCDR1 leads to constitutive activation of defense responses in rice and Arabidopsis. Mol. Plant- Microbe Interact. 22:1635-1644.
48. Rivas, S., and Thomas, C. M. 2005. Molecular interactions between tomato and the leaf mold pathogen Cladosporium fulvum. Annu. Rev. Phytopathol. 43:395-436.
49. Schiffer, R., Görg, R., Jarosch, B., Beckhove, U., Bahrenberg, G., Kogel, K.-H., and Schulze-Lefert, P. 1997. Tissue dependence and differential cordycepin sensitivity of race-specific resistance responses in the barleypowdery mildew interaction. Mol. Plant-Microbe Interact. 10:830-839.
50. Schmitz, G., Reinhold, T., Göbel, C., Feussner, I., Ekkehard-Neuhaus, H., and Conrath, U. 2010. Limitation of nocturnal ATP import into chloroplasts seems to affect hormonal crosstalk, prime defense, and enhance disease resistance in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 23:1584-1591.
51. Shetty, N. P., Mehrabi, R., Lütken, H., Haldrup, A., Kema, G. H. J., Collinge, D. B., and Jørgensen, H. J. L. 2007. Role of hydrogen peroxide during the interaction between the hemibiotrophic fungal pathogen Septoria tritici and wheat. New Phytol. 174:637-647.
52. Song, J. T., Koo, Y. J., Seo, H. S., Kim, M. C., Choi, Y. D., and Kim, J. H. 2008. Overexpression of AtSGT1, an Arabidopsis salicylic acid glucosyltransferase, leads to increased susceptibility to Pseudomonas syringae. Phytochemistry 69:1128-1134.
53. Temme, N., and Tudzynski, P. 2009. Does Botrytis cinerea ignore H2O2- induced oxidative stress during infection? Characterization of Botrytis Activator Protein 1. Mol. Plant-Microbe Interact. 22:987-998.
54. Torres, M. A., Jones, J. D. G., and Dangl, J. L. 2006. Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141:373-378.
55. Tudzynski, P., and Kokkelink, L. 2008. Botrytis cinerea: Molecular aspects of a necrotrophic life-style. Pages 29-50 in: The Mycota, Vol. V Plant Relationships. H. Deising, ed. Springer, Heidelberg, Germany.
56. Umemura, K., Satou, J., Iwata, M., Uozumi, N., Koga, J., Kawano, T., Koshiba, T., Anzai, H., and Mitomi, M. 2009. Contribution of salicylic acid glucosyltransferase, OsSGT1, to chemically induced disease resistance in rice plants. Plant J. 57:463-472.
57. Uppalapati, S. R., Ishiga, Y., Wangdi, T., Kunkel, B. N., Anand, A., Mysore, K. S., and Bender, C. L. 2007. The phytotoxin coronatine contributes to pathogen fitness and is required for suppression of salicylic acid accumulation in tomato inoculated with Pseudomonas syringae pv. tomato DC3000. Mol. Plant-Microbe Interact. 20:955-965.
58. Vandenabeele, S., Van Der Kelen, K., Dat, J., Gadjev, I., Boonefaes, T., Morsa, S., Rottiers, P., Slooten, L., Van Montagu, M., Zabeau, M., Inzé, D., and Van Breusegem, F. 2003. A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. Proc. Natl. Acad. Sci. USA 100:16113-16118.
59. Verberne, M. C., Verpoorte, R., Bol, J. F., Mercado-Blanco, J., and Linthorst, H. J. M. 2000. Overproduction of salicylic acid in plants by bacterial transgenes enhances pathogen resistance. Nat. Biotechnol. 18:779-783.
60. Vlot, A. C., Dempsey, D. A., and Klessig, D. F. 2009. Salicylic acid, a multifaceted hormone to combat disease. Annu. Rev. Phytopathol. 47:177-206.
61. von Tiedemann, A. 1997. Evidence for a primary role of active oxygen species in induction of host cell death during infection of bean leaves with Botrytis cinerea. Physiol. Mol. Plant Pathol. 50:151-166.
62. Wan, X., Tan, J., Lu, S., Lin, C., Hu, Y., and Guo, Z. 2009. Increased tolerance to oxidative stress in transgenic tobacco expressing a wheat oxalate oxidase gene via induction of antioxidant enzymes is mediated by H2O2. Physiol. Plant. 136:30-44.
63. Wildermuth, M. C., Dewdney, J., Wu, G., and Ausubel, F. M. 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562-571.
64. Wu, G. S., Shortt, B. J., Lawrence, E. B., León, J., Fitzsimmons, K. C., Levine, E. B., Raskin, I., and Shah, D. M. 1997. Activation of host defense mechanisms by elevated production of H2O2 in transgenic plants. Plant Physiol. 115:427-435.
65. Wu, G., Shortt, B. J., Lawrence, E. B., Levine, E. B., Fitzsimmons, K. C., and Shah, D. M. 1995. Disease resistance conferred by expression of a gene encoding H2O2-generating glucose oxidase in transgenic potato plants. Plant Cell 7:1357-1368.
66. Xia, Y., Suzuki, H., Borevitz, J., Blount, J., Guo, Z., Patel, K., Dixon, R. A., and Lamb, C. 2004. An extracellular aspartic protease functions in Arabidopsis disease resistance signaling. EMBO J. 23:980-988.
67. Yu, I. C., Parker, J., and Bent, A. F. 1998. Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc. Natl. Acad. Sci. USA 95:7819-7824.
68. Zipfel, C. 2009. Early molecular events in PAMP-triggered immunity. Curr. Opin. Plant Biol. 12:414-420.
69. 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.