Involvement of nitric oxide generation in hypersensitive cell death induced by elicitin in tobacco cell suspension culture

Journal of General Plant Pathology

Volumn 70, Issue 2, 2004, Pages 85-92

  Yamamoto, Ayako ^a   Katou, Shinpei ^a,b   Yoshioka, Hirofumi ^a   Doke, Noriyuki ^a   Kawakita, Kazuhito ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

Author keywords

Defense response; Hypersensitive cell death INF1 elicitin; Nitric oxide; Signal transduction; Tobacco BY 2

Indexed keywords

ESCHERICHIA COLI; MAMMALIA; NICOTIANA TABACUM; PHYTOPHTHORA; PHYTOPHTHORA INFESTANS;

EID: 3042704494     PISSN: 13452630     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10327-003-0094-3     Document Type: Article

References (49)

1. Ausubel FM, Brent R, Kingston RE. Moore DD, Seidman JG, Smith JA, Strul K (1987) Current protocols in molecular biology. Wiley, New York, pp 4.3.1-4.3.4
2. Barchowsky A, Klei LR, Dudek EJ, Swartz HM, James PE (1999) Stimulation of reactive oxygen, but not reactive nitrogen species in vascular endothelial cells exposed to low levels of arsenite. Free Radic Biol Med 27:1405-1412
3. Bradford MM (1976) A rapid and sensitive method for the quantiation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
4. Chandok MR, Ytterberg AJ, van Wijk KJ, Klessig DF (2003) The pathogen-inducible nitric oxide synthase (iNOS) in plants is a variant of the P protein of the glycine decarboxylase complex. Cell 113:469-482
5. Chandra S, Low PS (1995) Role of phosphorylation in elicitation of the oxidative burst in cultured soybean cells. Proc Natl Acad Sci USA 92:4120-4123
6. Clarke A, Desikan R, Hurst RD, Hancock JT, Neill SJ (2000) NO way back: nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. Plant J 24:667-677
7. Cueto M, Hernández-Perea O, Martín R, Bentura ML, Rodrigo J, Lamas S, Golvano MP (1996) Presence of nitric oxide synthase activity in roots and nodules of Lupinus albus. FEBS Lett 398:159-164
8. Czernic P, Huang HC, Marco Y (1996) Characterization of hsr201 and hsr515, two tobacco genes preferentially expressed during the hypersensitive reaction provoked by phytopathogenic bacteria. Plant Mol Biol 31:255-265
9. De León IP, Sanz A, Hamberg M, Castresana C (2002) Involvement of the Arabidopsis α-DOX fatty acid dioxygenase in protection against oxidative stress and cell death. Plant J 29:61-72
10. Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394:585-588
11. Delledonne M, Zeier J, Marocco A, 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
12. Delledonne M, Polverari A, Murgia I (2003) The functions of nitric oxide-mediated signaling and changes in gene expression during the hypersensitive response. Antioxid Redox Signal 5:33-41
13. De Pinto MC, Tommasi F, De Gara L (2002) Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco Bright-Yellow 2 cells Plant Physiol 130:698-708
14. Desikan R, Griffiths R, Hancock J, Neill S (2002) A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc Natl Acad Sci USA 99:16314-16318
15. Dick JMC, Lefebvre RA (1997) Influence of different classes of NO synthase inhibitors in the pig gastric fundus. Naunyn-Schmiedebergs Arch Pharmacol 356:488-494
16. Durner J, Klessig DF (1999) Nitric oxide as a signal in plants. Curr Opin Plant Biol 2:369-374
17. Durner J, Wendehenne D, Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc Natl Acad Sci USA 95:10328-10333
18. Goodman RN, Novacky AJ (1994) The hypersensitive reaction in plants to pathogens: a resistance phenomenon. American Phytopathological Society, St. Paul, MN
19. Hoyos ME, Zhang S (2000) Calcium-independent activation of salicylic acid-induced protein kinase and a 40-kilodalton protein kinase by hyperosmotic stress. Plant Physiol 122:1355-1363
20. Kamoun S, van West P, de Jong AJ, de Groot KE, Vleeshouwers VGAA, 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
21. Katou S, Senda K, Yoshioka H, Doke N, Kawakita K (1999) A 51 kDa protein kinase of potato activated with hyphal wall components from Phytophthora infestans. Plant Cell Physiol 40:825-831
22. Klessig DF, Durner J, Noad R, Navarre DA, Wendehenne D, Kumar D, Zhou JM, Shah J, Zhang S, Kachroo P, Trifa Y, Pontier D, Lam E, Silva H (2000) Nitric oxide and salicylic acid signaling in plant defense. Proc Natl Acad Sci USA 97:8849-8855
23. Kojima H, Nakatsubo N, Kikuchi K, Kawahara S, Kirino Y, Nagoshi H, Hirata Y, Nagano T (1998) Detection and imaging of nitric oxide with novel fluorescent indicators: diaminofluoresceins. Anal Chem 70:2446-2453
24. Kumar D, Klessig DF (2000) Differential induction of tobacco MAP kinases by the defense signals nitric oxide, salicylic acid, ethylene, and jasmonic acid. Mol Plant Microbe Interact 3:347-351
25. Lam E, Pontier D, del Pozo O (1999) Die and let live-programmed cell death in plants. Curr Opin Plant Biol 2:502-507
26. Lam E, Kato N, Lawton M (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411:848-853
27. Lipton SA, Choi Y-B, Pan Z-H, Lei SZ, Chen H-SV, Sucher NJ, Loscalzo J, Singel DJ, Stamler JS (1993) A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364:626-632
28. Marco Y, Raguesh F, Godiard L, Froissard D (1990) Transcriptional activation of 2 classes of genes during hypersensitive reaction of tobacco leaves infiltrated with an incompatible isolate of the phytopathogenic bacterium Pseudomonas solanacearum. Plant Mol Biol 15:145-154
29. Mayer B, Hemmens B (1997) Biosynthesis and action of nitric oxide in mammalian cells. Trends Biochem Sci 20:477-481
30. Millar AH, Day DA (1997) Alternative solutions to radical problems. Trends Plant Sci 2:289-290
31. Miura Y, Yoshioka H, Park H-J, Kawakita K, Doke N (1999) Plasma membrane perturbation in association with calcium ion movement followed by fungal elicitor-stimulated oxidative burst and defense gene activation in potato tuber. Ann Phytopathol Soc Jpn 65:447-453
32. Nakatsubo N, Kojima H, Kikuchi K, Nagoshi H, Hirata Y, Maeda D, Imai Y, Irimura T, Nagano T (1998) Direct evidence of nitric oxide production from bovine aortic endothelial cells using new fluorescence indicators: diaminofluoresceins. FEBS Lett 427:263-266
33. Nathan C (1995) Natural resistance and nitric oxide. Cell 82:873-876
34. Ninnemann H, Maier J (1996) Indications for the occurrence of nitric oxide synthase in fungi and plants and the involvement in photoconidiation of Neurospora crassa. Photochem Photobiol 64:393-398
35. Noritake T, Kawakita K, Doke N (1996) Nitric oxide induces phytoalexin accumulation in potato tuber tissues. Plant Cell Physiol 37:113-116
36. Pontier D, Tronchet M, Rogowsky P, Lam E, Roby D (1998) Activation of hsr203, a plant gene expressed during incompatible plant-pathogen interactions, is correlated with programmed cell death. MoI Plant Microbe Interact 11:544-554
37. Ren D, Yang H, Zhang S (2002) Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J Biol Chem 277:559-565
38. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
39. Sasabe M, Takeuchi K, Kamoun S, Ichinose Y, Govers F, Toyoda K, Shiraishi T, 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
40. Sen S, Cheema IR (1995) Nitric oxide synthase and calmodulin immunoreactivity in plant embryonic tissue. Biochem Arch 11:221-227
41. Stamler JS (1994) Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell 78:931-936
42. Tronchet M, Ranty B, Marco Y, Roby D (2001) HSR203 antisense suppression in tobacco accelerates development of hypersensitive cell death. Plant J 27:115-127
43. Wendehenne D, Lamotte O, Frachisse J-M, Barbier-Brygoo H, Pugin A (2002) Nitrate efflux is an essential component of the cryptogein signaling pathway leading to defense responses and hypersensitive cell death in tobacco. Plant Cell 14:1937-1951
44. Xiang C, Miao Z-H, Lam E (1996) Coordinated activation of as-1-lype elements and a tobacco glutathione S-transferase gene by auxins, salicylic acid, methyl-jasmonate and hydrogen peroxide. Plant Mol Biol 32:415-426
45. Yamamoto A, Katou S, Yoshioka H, Doke N, Kawakita K (2003) Nitrate reductase, a nitric oxide-producing enzyme: induction by pathogen signals. J Gen Plant Pathol 69:218-229
46. Yamasaki H, Sakihama Y (2000) Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Lett 468:89-92
47. Yano A, Suzuki K, Uchimiya H, Shinshi H (1998) Induction of hypersensitive cell death by a fungal protein in cultures of tobacco cells. Mol Plant Microbe Interact 11:115-123
48. Zhang S, Klessig DF (2001) MAPK cascades in plant defense signaling. Trends Plant Sci 6:520-527
49. Zhang S, Du H, Klessig DF (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