Nicotiana benthamiana gp91phox homologs Nbrboha and Nbrbohb participate in H2O2 accumulation and resistance to Phytophthora infestans

Plant Cell

Volumn 15, Issue 3, 2003, Pages 706-718

  Yoshioka, Hirofumi ^a   Numata, Noriko ^a   Nakajima, Kazumi ^a   Katou, Shinpei ^a   Kawakita, Kazuhito ^a   Rowland, Owen ^b   Jones, Jonathan D G ^b   Doke, Noriyuki ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b JOHN INNES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; DNA; GENES; PROTEINS; VIRUSES;

ACTIVE OXYGEN SPECIES (AOS);

MICROBIOLOGY;

EUKARYOTA; NICOTIANA BENTHAMIANA; PHYTOPHTHORA; PHYTOPHTHORA INFESTANS; SOLANUM TUBEROSUM;

ACETIC ACID DERIVATIVE; COMPLEMENTARY DNA; CYBB PROTEIN, HUMAN; CYCLOPENTANE DERIVATIVE; HYDROGEN PEROXIDE; JASMONIC ACID METHYL ESTER; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE; OXIDOREDUCTASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SALICYLIC ACID; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; CHEMISTRY; DNA SEQUENCE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; INNATE IMMUNITY; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MULTIGENE FAMILY; MUTATION; PHYLOGENY; PHYSIOLOGY; PHYTOPHTHORA; PLANT LEAF; SEQUENCE HOMOLOGY; TOBACCO;

ACETIC ACIDS; AMINO ACID SEQUENCE; APOPTOSIS; CYCLOPENTANES; DNA, COMPLEMENTARY; GENE EXPRESSION REGULATION, PLANT; HYDROGEN PEROXIDE; IMMUNITY, NATURAL; MEMBRANE GLYCOPROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; MUTATION; NADH, NADPH OXIDOREDUCTASES; NADPH OXIDASE; PHYLOGENY; PHYTOPHTHORA; PLANT LEAVES; PLANT PROTEINS; REACTIVE OXYGEN SPECIES; SALICYLIC ACID; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; TOBACCO;

EID: 0037343106     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.008680     Document Type: Article

References (75)

1. Allan, A.C., and Fluhr, R. (1997). Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. Plant Cell 9, 1559-1572.
2. Amicucci, E., Gaschler, K., and Ward, J.M. (1999). NADPH oxidase genes from tomato (Lycopersicon esculentum) and curly-leaf pondweed (Potamogeton crispus). Plant Biol. 1, 524-528.
3. Apostol, I., Heinstein, P.F., and Low, P.S. (1989). Rapid stimulation of an oxidative burst during elicitation of cultured plant cells: Role in defense and signal transduction. Plant Physiol. 90, 109-116.
4. Asai, T., Tena, G., Plotnikova, J., Willmann, M.R., Chiu, W.-L., Gomez-Gomez, L., Boller, T., Ausubel, F.M., and Sheen, J. (2002). MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977-983.
5. 2 by Phytophthora elicitor-stimulated rose cells. Plant Physiol. 107, 1241-1247.
6. Baulcombe, D.C. (1999). Fast forward genetics based on virus-induced gene silencing. Curr. Opin. Plant Biol. 2, 109-113.
7. Baulcombe, D.C., Chapman, S., and Cruz, S.S. (1995). Jellyfish green fluorescent protein as a reporter for virus infections. Plant J. 7, 1045-1053.
8. Bhalla, U.S., Ram, P.T., and Lyengar, R. (2002). MAP kinase phosphatase as a locus of flexibility in a mitogen-activated protein kinase signaling network. Science 297, 1018-1023.
9. Bokoch, G.M. (1994). Regulation of the human neutrophil NADPH oxidase by the RacGTP-binding proteins. Curr. Opin. Cell Biol. 6, 212-218.
10. Bourque, S., Binet, M.N., Ponchet, M., Pugin, A., and Lebrun-Garcia, A. (1999). Characterization of the cryptogein binding sites on plant plasma membranes. J. Biol. Chem. 274, 34699-34705.
11. Bradley, D.J., Kjellbom, P., and Lamb, C.J. (1992). Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: A novel, rapid defense response. Cell 70, 21-30.
12. 2+ fluxes during elicitation of the oxidative burst in aequorin-transformed tobacco cells. J. Biol. Chem. 272, 28274-28280.
13. Chapman, S., Kavanagh, T., and Baulcombe, D.C. (1992). Potato virus X as a vector for gene expression in plants. Plant J. 2, 549-557.
14. Chen, Z., Silva, H., and Klessig, D.F. (1993). Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262, 1883-1886.
15. Dangl, J.L., and Jones, J.D.G. (2001). Plant pathogens and integrated defense responses to infection. Nature 411, 826-833.
16. Delledonne, M., Xia, Y., Dixon, R.A., and Lamb, C. (1998). Nitric oxide functions as a signal in plant disease resistance. Nature 394, 585-588.
17. Delledonne, M., Zeier, J., Marocco, A., and Lamb, C. (2001). Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc. Natl. Acad. Sci. USA 98, 13454-13459.
18. Desikan, R., Burnett, E.C., Hancock, J.T., and Neill, S.J. (1998). Harpin and hydrogen peroxide induce the expression of a homologue of gp91-phox in Arabidopsis thaliana suspension cultures. J. Exp. Bot. 49, 1767-1771.
19. Desikan, R., A.-H.-Mackerness, S., Hancock, J.T., and Neill, S.J. (2001). Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol. 127, 159-172.
20. Dietrich, R.A., Richberg, M.H., Schmidt, R., Dean, C., and Dangl, J.L. (1996). A novel zinc finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death. Cell 88, 685-694.
21. Doke, N. (1983). Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol. Plant Pathol. 23, 345-357.
22. - generation in membrane fractions isolated from wounded potato tubers inoculated with Phytophthora infestans. Physiol. Plant Pathol. 27, 311-322.
23. - generating system in a plasma membrane-rich fraction of potato tuber tissues by treatment with an elicitor from Phytophthora infestans or with digitonin. Physiol. Mol. Plant Pathol. 46, 17-28.
24. Durner, J., Wendehenne, D., and Klessig, D.F. (1998). Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc. Natl. Acad. Sci. USA 95, 10328-10333.
25. Finegold, A.A., Shatwell, K.P., Segal, A.W., Klausner, R.D., and Dancis, A. (1996). Intramembrane bis-heme motif for transmembrane electron transport conserved in a yeast iron reductase and the human NADPH oxidase. J. Biol. Chem. 271, 31021-31024.
26. Grant, J.J., Yun, B.-W., and Loake, G.J. (2000). Oxidative burst and cognate redox signalling reported by luciferase imaging: Identification of a signal network that functions independently of ethylene, SA and Me-JA but is dependent on MAPKK activity. Plant J. 24, 569-582.
27. Groom, Q.J., Torres, M.A., Fordham-Skelton, A.P., Hammond-Kosack, K.E., Robinson, N.J., and Jones, J.D.G. (1996). rbohA, a rice homologue of the mammalian gp91 phox respiratory burst oxidase gene. Plant J. 10, 515-522.
28. Hellens, R.P., Edwards, A.E., Leyland, N.R., Bean, S., and Mullineaux, P.M. (2000). pGreen: A versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 42, 819-832.
29. Huet, J.C., Salle-Tourne, M., and Pernollet, J.C. (1994). Amino acid sequence and toxicity of the alpha elicitin secreted with ubiquitin by Phytophthora infestans. Mol. Plant-Microbe Interact. 7, 302-304.
30. Jabs, T., Dietrich, R.A., and Dangl, J.L. (1996). Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273, 1853-1856.
31. Jones, J.D.G., Shlumukov, L., Carland, F., English, J., Scofield, S., Bishop, G., and Harrison, K. (1992). Effective vectors for transformation, expression of heterologous genes, and assaying transposon excision in transgenic plants. Transgenic Res. 1, 285-297.
32. Kamoun, S., Honée, G., Weide, R., Laugé, R., Kooman-Gersmann, M., de Groot, K., Govers, F., and de Wit, P.J.G.M. (1999). The fungal gene Avr9 and the oomycete gene inf1 confer avirulence to potato virus X on tobacco. Mol. Plant-Microbe Interact. 12, 459-462.
33. Kamoun, S., van West, P., de Jong, A.J., de Groot, K.E., Vleeshouwers, V.G.A.A., and Govers, F. (1997). A gene encoding a protein elicitor of Phytophthora infestans is down-regulated during infection of potato. Mol. Plant-Microbe Interact. 10, 13-20.
34. Kamoun, S., van West, P., Vleeshouwers, V.G.A.A., de Groot, K.E., and Govers, F. (1998). Resistance of Nicotiana benthamiana to Phytophthora infestans is mediated by the recognition of the elicitor protein INF1. Plant Cell 10, 1413-1425.
35. Kamoun, S., Young, M., Glascock, C.B., and Tyler, B.M. (1993). Extracellular protein elicitors from Phytophthora: Host-specificity and induction of resistance to bacterial and fungal phytopathogens. Mol. Plant-Microbe Interact. 6, 15-25.
36. Katou, S., Senda, K., Yoshioka, H., Doke, N., and Kawakita, K. (1999). A 51 kDa protein kinase of potato activated with hyphal wall components from Phytophthora infestans. Plant Cell Physiol. 40, 825-831.
37. 2. Plant Physiol. 108, 1171-1178.
38. Kawano, T., Sahashi, N., Takahashi, K., Uozumi, N., and Muto, S. (1998). Salicylic acid induces extracellular superoxide generation followed by an increase in cytosolic calcium ion in tobacco suspension culture: The earliest events in salicylic acid signal transduction. Plant Cell Physiol. 39, 721-730.
39. Kawasaki, T., Henmi, K., Ono, E., Hatakeyama, S., Iwano, M., Satoh, H., and Shimamoto, K. (1999). The small GTP-binding protein Rac is a regulator of cell death in plants. Proc. Natl. Acad. Sci. USA 96, 10922-10926.
40. 2+ binding motifs. Plant Cell 10, 255-266.
41. Kovtun, Y., Chiu, W.-L., Tena, G., and Sheen, J. (2000). Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc. Natl. Acad. Sci. USA 97, 2940-2945.
42. Kretsinger, R.H. (1996). EF-hands reach out. Nat. Struct. Biol. 3, 12-15.
43. Lamb, C., and Dixon, R.A. (1997). The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 251-275.
44. Léon, J., Lawton, M.A., and Raskin, I. (1995). Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol. 108, 1673-1678.
45. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79, 583-593.
46. Miura, Y., Yoshioka, H., and Doke, N. (1995). An autophotographic determination of the active oxygen generation in potato tuber discs during hypersensitive response to fungal infection or elicitor. Plant Sci. 105, 45-52.
47. Murray, M.G., and Thompson, W.F. (1980). Rapid isolation of high-molecular-weight plant DNA. Nucleic Acids Res. 8, 4321-4325.
48. Noritake, T., Kawakita, K., and Doke, N. (1996). Nitric oxide induces phytoalexin accumulation in potato tuber tissues. Plant Cell Physiol. 37, 113-116.
49. Peart, J.R., et al. (2002). Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants. Proc. Natl. Acad. Sci. USA 99, 10865-10869.
50. Peng, M., and Kuc, J. (1992). Peroxidase-generated hydrogen peroxide as a source of antifungal activity in vitro and on tobacco leaf discs. Phytopathology 82, 696-699.
51. Piedras, P., Hammond-Kosack, K.E., Harrison, K., and Jones, J.D.G. (1998). Rapid, Cf-9 and Avr9-dependent, production of active oxygen species in tobacco suspension cultures. Mol. Plant-Microbe Interact. 11, 1155-1166.
52. Ren, D., Yang, H., and Zhang, S. (2002). Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J. Biol. Chem. 277, 559-565.
53. Ricci, P., Bonnet, P., Huet, J.-C., Sallantin, M., Beauvais-Cante, F., Bruneteau, M., Billard, V., Michel, G., and Pernollet, J.-C. (1989). Structure and activity of proteins from pathogenic fungi Phytophthora eliciting necrosis and acquired resistance in tobacco. Eur. J. Biochem. 183, 555-563.
54. Romeis, T., Ludwig, A.A., Martin, R., and Jones, J.D.G. (2001). Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J. 20, 5556-5567.
55. Rustérucci, C., Stallaert, V., Milat, M.-L., Pugin, A., Ricci, P., and Blein, J.-P. (1996). Relationship between active oxygen species, lipid peroxidation, necrosis, and phytoalexin production induced by elicitins in Nicotiana. Plant Physiol. 111, 885-891.
56. phox NADPH oxidase: Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol. 126, 1281-1290.
57. Saitou, N., and Nei, M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
58. Sasabe, M., Takeuchi, K., Kamoun, S., Ichinose, Y., Govers, F., Toyoda, K., Shiraishi, T., and Yamada, T. (2000). Independent pathways leading to apoptotic cell death, oxidative burst and defense gene expression in response to elicitin in tobacco cell suspension culture. Eur. J. Biochem. 267, 5005-5013.
59. -245 is a flavocytochrome containing FAD and the NADPH-binding site of the microbicidal oxidase of phagocytes. Biochem. J. 284, 781-788.
60. Shirasu, K., Nakajima, H., Rajasekhar, V.K., Dixon, R.A., and Lamb, C. (1997). Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9, 261-270.
61. Simon-Plas, F., Elmayan, T., and Blein, J.-P. (2002). The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells. Plant J. 31, 137-147.
62. Smith, H.H. (1979). The Nicotiana genus as a genetic resource. US Dep. Agric. Tech. Bull. 1586, 1-16.
63. Tavernier, E., Wendehenne, D., Blein, J.-P., and Pugin, A. (1995). Involvement of free calcium in action of cryptogein, a proteinaceous elicitor of hypersensitive reaction in tobacco cells. Plant Physiol. 109, 1025-1031.
64. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994). CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
65. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11, 1187-1194.
66. phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl. Acad. Sci. USA 99, 517-522.
67. phox). Plant J. 14, 365-370.
68. Tronchet, M., Ranty, B., Marco, Y., and Roby, D. (2001). HSR203 antisense suppression in tobacco accelerates development of hypersensitive cell death. Plant J. 27, 115-127.
69. Yang, K.-Y., Liu, Y., and Zhang, S. (2001). Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc. Natl. Acad. Sci. USA 98, 741-746.
70. Yoshioka, H., Miyabe, M., Hayakawa, Y., and Doke, N. (1996). Expression of genes for phenylalanine ammonia-lyase and 3-hydroxy-3-methylglutaryl CoA reductase in aged potato tubers infected with Phytophthora infestans. Plant Cell Physiol. 37, 81-90.
71. Yoshioka, H., Sugie, K., Park, H.-J., Maeda, H., Tsuda, N., Kawakita, K., and Doke, N. (2001). Induction of plant gp91 phox homolog by fungal cell wall, arachidonic acid, and salicylic acid in potato. Mol. Plant-Microbe Interact. 14, 725-736.
72. Yoshioka, H., Yamada, N., and Doke, N. (1999). cDNA cloning of sesquiterpene cyclase and squalene synthase, and expression of the genes in potato tuber infected with Phytophthora infestans. Plant Cell Physiol. 40, 993-998.
73. phox is the heme binding subunit of the superoxide-generating NADPH oxidase. Proc. Natl. Acad. Sci. USA 95, 7993-7998.
74. Zhang, S., Du, H., and Klessig, D.F. (1998). Activation of the tobacco SIP kinase by both a cell wall-derived carbohydrate elicitor and purified proteinaceous elicitins from Phytophthora spp. Plant Cell 10, 435-449.
75. Zhou, F., Zhang, Z., Gregersen, P.L., Mikkelsen, J.D., de Neergaard, E., Collinge, D.B., and Thordal-Christensen, H. (1998). Molecular characterization of the oxalate oxidase involved in the response of barley to the powdery mildew fungus. Plant Physiol. 117, 33-41.