Regulatory mechanisms of nitric oxide and reactive oxygen species generation and their role in plant immunity

Nitric Oxide - Biology and Chemistry

Volumn 25, Issue 2, 2011, Pages 216-221

  Yoshioka, Hirofumi ^a   Mase, Keisuke ^a   Yoshioka, Miki ^a   Kobayashi, Michie ^b   Asai, Shuta ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

Author keywords

CDPK; MAPK; NADPH oxidase; NO; Riboflavin

Indexed keywords

FLAVINE ADENINE NUCLEOTIDE; FLAVINE MONONUCLEOTIDE; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; PROTEIN KINASE C; QUERCETIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RIBOFLAVIN; RIBOFLAVIN DERIVATIVE;

CALCIUM TRANSPORT; CONFERENCE PAPER; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME STRUCTURE; PLANT IMMUNITY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SYNTHESIS;

ENZYME ACTIVATION; GENE SILENCING; GENES, PLANT; MITOGEN-ACTIVATED PROTEIN KINASES; NADPH OXIDASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXIDATION-REDUCTION; PHOSPHORYLATION; PLANT IMMUNITY; PLANT PROTEINS; PLANTS; REACTIVE OXYGEN SPECIES; RIBOFLAVIN; SIGNAL TRANSDUCTION;

EID: 80051546279     PISSN: 10898603     EISSN: 10898611     Source Type: Journal    
DOI: 10.1016/j.niox.2010.12.008     Document Type: Conference Paper

References (98)

1. J.D.G. Jones, and J.L. Dangl The plant immune system Nature 444 2006 323 329 (Pubitemid 44764102)
2. C. Zipfel, S. Robatzek, L. Navarro, E.J. Oakeley, J.D.G. Jones, G. Felix, and T. Boller Bacterial disease resistance in Arabidopsis through flagellin perception Nature 248 2004 764 767 (Pubitemid 38508287)
3. D. Zeidler, U. Zähringer, I. Gerber, I. Dubery, T. Hartung, W. Bors, P. Hutzler, and J. Durner Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes Proc. Natl. Acad. Sci. USA 101 2004 15811 15816 (Pubitemid 39473570)
4. N. Doke 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 1983 345 357
5. D. Wendehenne, J. Durner, and D.F. Klessig Nitric oxide: a new player in plant signalling and defence responses Curr. Opin. Plant Biol. 7 2004 449 455 (Pubitemid 38871620)
6. M.A. Torres, J.D.G. Jones, and J.L. Dangl Reactive oxygen species signaling in response to pathogens Plant Physiol. 141 2006 373 378 (Pubitemid 43974530)
7. J.K. Hong, B.-W. Yun, J.-G. Kang, M.U. Raja, E. Kwon, K. Sorhagen, C. Chu, Y. Wang, and G.J. Loake Nitric oxide function and signalling in plant disease resistance J. Exp. Bot. 59 2008 147 154 (Pubitemid 351651353)
8. D. Kumar, and D.F. Klessig Differential induction of tobacco MAP kinases by the defense signals nitric oxide, salicylic acid, ethylene, and jasmonic acid Mol. Plant-Microbe Interact. 13 2000 347 351 (Pubitemid 30118881)
9. J. Durner, D. Wendehenne, and D.F. Klessig Defense gene induction in tobacco by nitric oxide, cyclic GMP and cyclic ADP-ribose Proc. Natl. Acad. Sci. USA 95 1998 10328 10333 (Pubitemid 28415341)
10. Y.K.-C. Butt, J.H.-K. Lum, and S.C.-L. Lo Proteomic identification of plant proteins probed by mammalian nitric oxide synthase antibodies Planta 216 2003 762 771 (Pubitemid 36761720)
11. C. Garcia-Mata, and L. Lamattina Abscisic acid, nitric oxide and stomatal closure - is nitrate reductase one of the missing links? Trends Plant Sci. 8 2003 20 26 (Pubitemid 36725963)
12. F.-Q. Guo, M. Okamoto, and N.M. Crawford Identification of a plant nitric oxide synthase gene involved in hormonal signaling Science 302 2003 100 103 (Pubitemid 37210696)
13. T. Zemojtel, A. Frohlich, M.C. Palmieri, M. Kolanczyk, I. Mikula, L.S. Wyrwicz, E.E. Wanker, S. Mundlos, M. Vingron, P. Martasek, and J. Durner Plant nitric oxide synthase: a never-ending story? Trends Plant Sci. 11 2006 524 525 (Pubitemid 44636300)
14. N.M. Crawford, M. Galli, R. Tischner, Y.M. Heimer, M. Okamoto, A. Mack, and Zemojtel Plant nitric oxide synthase: back to square one Trends Plant Sci. 11 2006 526 527
15. M. Moreau, G.I. Lee, Y. Wang, B.R. Crane, and D.F. Klessig AtNOS/A1 is a functional Arabidopsis thaliana cGTPase and not a nitric oxide synthase J. Biol. Chem. 283 2008 32957 32967
16. Y. He, R.-H. Tang, Y. Hao, R.D. Stevens, C.W. Cook, S.M. Ahn, L. Jing, Z. Yang, L. Chen, F. Guo, F. Fiorani, R.B. Jackson, N.M. Crawford, and Z.-M. Pei Nitric oxide represses the Arabidopsis floral transition Science 305 2004 1968 1971 (Pubitemid 39287998)
17. M.-G. Zhao, Q.-Y. Tian, and W.-H. Zhang Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis Plant Physiol. 144 2007 206 217 (Pubitemid 46941625)
18. H. Kato, S. Asai, A. Yamamoto-Katou, H. Yoshioka, N. Doke, and K. Kawakita Involvement of NbNOA1 in NO production and defense responses in INF1-treated Nicotiana benthamiana J. Gen. Plant Pathol. 74 2008 15 23 (Pubitemid 351170153)
19. E. Gas, U. Flores-Pérez, S. Sauret-Güeto, and M. Rodríguez-Concepción Hunting for plant nitric oxide synthase provides new evidence of a central role for plastids in nitric oxide metabolism Plant Cell 21 2009 18 23
20. H. Sumimoto Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species FEBS J. 275 2008 3249 3277 (Pubitemid 351813551)
21. phox participate in activation of superoxide-producing NADPH oxidases J. Biol. Chem. 278 2003 25234 25246 (Pubitemid 37548688)
22. Q.J. Groom, M.A. Torres, A.P. Fordham-Skelton, K.E. Hammond-Kosack, N.J. Robinson, and J.D.G. Jones rbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene Plant J. 10 1996 515 522 (Pubitemid 27108404)
23. 2+ binding motifs Plant Cell 10 1998 255 266
24. phox) Plant J. 14 1998 365 370 (Pubitemid 28236000)
25. E. Amicucci, K. Gaschler, and J.M. Ward NADPH oxidase genes from tomato (Lycopersicon esculentum) and curly-leaf pondweed (Potamogeton crispus) Plant Biol. 1 1999 524 528 (Pubitemid 29514360)
26. H. Yoshioka, K. Sugie, H.-J. Park, H. Maeda, N. Tsuda, K. Kawakita, and N. Doke Induction of plant gp91 phox homolog by fungal cell wall, arachidonic acid, and salicylic acid in potato Mol. Plant-Microbe Interact. 14 2001 725 736 (Pubitemid 32464112)
27. phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans Plant Cell 15 2003 706 718 (Pubitemid 36339583)
28. F. Simon-Plas, T. Elmayan, and J.-P. Blein The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells Plant J. 31 2002 137 147 (Pubitemid 34829627)
29. phox homologs OsrbohA and OsrbohE genes in ROS-dependent plant immune responses Plant Biotech. 22 2005 127 135 (Pubitemid 41735079)
30. phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response Proc. Natl. Acad. Sci. USA 99 2002 517 522 (Pubitemid 34060393)
31. J.M. Kwak, I.C. Mori, Z-.M. Pei, N. Leonhardt, M.A. Torres, J.L. Dangl, R.E. Bloom, S. Bodde, J.D.G. Jones, and J.I. Schroeder NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis EMBO J. 22 2003 2623 2633 (Pubitemid 36712360)
32. S. Asai, K. Ohta, and H. Yoshioka MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana Plant Cell 20 2008 1390 1406 (Pubitemid 352844190)
33. M. Sagi, O. Davydov, S. Orazova, Z. Yesbergenova, R. Ophir, J.W. Stratmann, and R. Fluhr Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentum Plant Cell 16 2004 616 628 (Pubitemid 38335274)
34. J. Foreman, V. Demidchik, J.H.F. Bothwell, P. Mylona, H. Miedema, M.A. Torres, P. Linstead, S. Costa, C. Brownlee, J.D.G. Jones, J.M. Davies, and L. Dolan Reactive oxygen species produced by NADPH oxidase regulate plant cell growth Nature 422 2003 442 446 (Pubitemid 36411398)
35. Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana Nature 408 2000 796 815
36. --generating activity in potato tuber tissues J. Exp. Bot. 57 2006 1373 1379
37. phox NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection Plant Physiol. 126 2001 1281 1290 (Pubitemid 32656816)
38. H.L. Wong, R. Pinontoan, K. Hayashi, R. Tabata, T. Yaeno, K. Hasegawa, C. Kojima, H. Yoshioka, K. Iba, T. Kawasaki, and K. Shimamoto Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension Plant Cell 19 2007 4022 4034 (Pubitemid 351253117)
39. M. Kobayashi, I. Ohura, K. Kawakita, N. Yokota, M. Fujiwara, K. Shimamoto, N. Doke, and H. Yoshioka Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase Plant Cell 19 2007 1065 1080 (Pubitemid 46953247)
40. A. Nakashima, L. Chen, N.P. Thao, M. Fujiwara, H.L. Wong, M. Kuwano, K. Umemura, K. Shirasu, T. Kawasaki, and K. Shimamoto RACK1 functions in rice innate immunity by interacting with the Rac1 immune complex Plant Cell 20 2008 2265 2279 (Pubitemid 352844524)
41. T. Elmayan, J. Fromentin, C. Riondet, G. Alcaraz, J.-P. Blein, and F. Simon-Plas Regulation of reactive oxygen species production by a 14-3-3 protein in elicited tobacco cells Plant Cell Environ. 30 2007 722 732 (Pubitemid 46674419)
42. Y. Zhang, H. Zhu, Q. Zhang, M. Li, M. Yan, R. Wang, L. Wang, R. Welti, W. Zhang, and X. Wang Phospholipase Dα1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis Plant Cell 21 2009 2357 2377
43. M. Delledonne, Y. Xia, R.A. Dixon, and C. Lamb Nitric oxide functions as a signal in plant disease resistance Nature 394 1998 585 588 (Pubitemid 28366834)
44. M. Delledonne, J. Zeier, A. Marocco, and C. Lamb Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response Proc. Natl. Acad. Sci. USA 98 2001 13454 13459 (Pubitemid 33051384)
45. B. Blume, T. Nürnberger, N. Nass, and D. Scheel Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley Plant Cell 12 2000 1425 1440
46. M. Grant, I. Brown, M. Knight, A. Ainslie, and J. Mansfield The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death Plant J. 23 2000 441 450 (Pubitemid 30661272)
47. D. Lecourieux, R. Raneva, and A. Pugin Calcium in plant defence-signalling pathways New Phytol. 171 2006 249 269
48. A.C. Harmon, B.-C. Yoo, and C. McCaffery Pseudosubstrate inhibition of CDPK, a protein kinase with a calmodulin-like domain Biochemistry 33 1994 7278 7287 (Pubitemid 24208766)
49. G. Freymark, T. Diehl, M. Miklis, T. Romeis, and R. Panstruga Antagonistic control of powdery mildew host cell entry by barley calcium-dependent protein kinases (CDPKs) Mol. Plant-Microbe Interact. 20 2007 1213 1221 (Pubitemid 47417391)
50. M. Bachmann, N. Shiraishi, W.H. Campbell, B.C. Yoo, A.C. Harmon, and S.C. Huber Identification of a Ser-543 as the major regulatory phosphorylation site in spinach leaf nitrate reductase Plant Cell 8 1996 505 517 (Pubitemid 126635923)
51. G.M. Yoon, P.E. Dowd, S. Gilroy, and A.G. McCubbina Calcium-dependent protein kinase isoforms in Petunia have distinct functions in pollen tube growth, including regulating polarity Plant Cell 18 2006 867 878 (Pubitemid 43956141)
52. A.G. McCubbin, S.M. Ritchie, S.J. Swanson, and S. Gilroy The calcium-dependent protein kinase HvCDPK1 mediates the gibberellic acid response of the barley aleurone through regulation of vacuolar function Plant J. 39 2004 206 218 (Pubitemid 38940811)
53. 2+-permeable channels and stomatal closure PLoS Biol. 4 2006 1749 1761
54. P.R. Gargantini, V. Giammaria, C. Grandellis, S.E. Feingold, S. Maldonado, and R.M. Ulloa Genomic and functional characterization of StCDPK1 Plant Mol. Biol. 70 2009 153 172
55. 2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants Plant J. 23 2000 319 327 (Pubitemid 30620839)
56. T. Romeis, A.A. Ludwig, R. Martin, and J.D.G. Jones Calcium-dependent protein kinases play an essential role in a plant defence response EMBO J. 20 2001 5556 5567 (Pubitemid 33010033)
57. J.M. Chico, M. Raíces, M.T. Téllez-Iñón, and R.M. Ulloa A calcium-dependent protein kinase is systemically induced upon wounding in tomato plants Plant Physiol. 128 2002 256 270 (Pubitemid 34115327)
58. S. Ivashuta, J. Liu, J. Liu, D.P. Lohar, S. Haridas, B. Bucciarelli, K.A. VandenBosch, C.P. Vance, M.J. Harrison, and J.S. Gantt RNA interference identifies a calcium-dependent protein kinase involved in Medicago truncatula root development Plant Cell 17 2005 2911 2921
59. A.A. Ludwig, H. Saitoh, G. Felix, G. Freymark, O. Miersch, C. Wasternack, T. Boller, J.D.G. Jones, and T. Romeis Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants Proc. Natl. Acad. Sci. USA 102 2005 10736 10741 (Pubitemid 41061623)
60. G.M. Yoon, H.S. Ha, H.J. Cho, J.R. Liu, and H.S.P. Lee Characterization of NtCDPK1, a calcium-dependent protein kinase gene in Nicotiana tabacum, and the activity of its encoded protein Plant Mol. Biol. 39 1999 991 1001
61. I. Murillo, E. Jaeck, M.J. Cordero, and B. San Segundo Transcriptional activation of a maize calcium-dependent protein kinase gene in response to fungal elicitors and infection Plant Mol. Biol. 45 2001 145 158 (Pubitemid 32228600)
62. A.A. Ludwig, T. Romeis, and J.D.G. Jones CDPK-mediated signalling pathways: specificity and cross-talk J. Exp. Bot. 55 2004 181 188 (Pubitemid 38119160)
63. T. Xing, X.J. Wang, K. Malik, and B.L. Miki Ectopic expression of an Arabidopsis calmodulin-like domain protein kinase-enhanced NADPH oxidase activity and oxidative burst in tomato protoplasts Mol. Plant-Microbe Interact. 14 2001 1261 1264 (Pubitemid 32965036)
64. 2+ signals through plant protein kinases Annu. Rev. Plant Physiol. Plant Mol. Biol. 55 2004 263 288 (Pubitemid 38940933)
65. J.F. Harper, J.-F. Huang, and S.J. Lloyd Genetic identification of an autoinhibitor in CDPK, a protein kinase with a calmodulin-like domain Biochemistry 33 1994 7267 7277 (Pubitemid 24208765)
66. H.B. Chai, and N. Doke Activation of the potential of potato leaf tissue to react hypersensitively to Phytophthora infestans by cytospore germination fluid and the enhancement of this potential by calcium ions Physiol. Mol. Plant Pathol. 30 1987 27 37
67. C. Yamamizo, K. Kuchimura, A. Kobayashi, S. Katou, K. Kawakita, J.D.G. Jones, N. Doke, and H. Yoshioka Rewiring mitogen-activated protein kinase cascade by positive feedback confers potato blight resistance Plant Physiol. 140 2006 681 692 (Pubitemid 43956287)
68. Y. Miura, H. Yoshioka, and N. Doke An autophotographic determination of the active oxygen generation in potato tuber discs during hypersensitive response to fungal infection or elicitor Plant Sci. 105 1995 45 52
69. J.J. Benschop, S. Mohammed, M. O'Flaherty, A.J. Heck, M. Slijper, and F.L. Menke Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis Mol. Cell. Proteomics 6 2007 1192 1214
70. T.S. Nühse, A.R. Bottrill, A.M. Jones, and S.C. Peck Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses Plant J. 51 2007 931 940 (Pubitemid 47301663)
71. 2+ and phosphorylation J. Biol. Chem. 283 2008 8885 8892
72. S. Takeda, C. Gapper, H. Kaya, E. Bell, K. Kuchitsu, and L. Dolan Local positive feedback regulation determines cell shape in root hair cells Science 319 2008 1241 1244 (Pubitemid 351323019)
73. C. Sirichandra, D. Gu, H.C. Hu, M. Davanture, S. Lee, M. Djaoui, B. Valot, M. Zivy, J. Leung, S. Merlot, and J.M. Kwak Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase FEBS Lett. 583 2009 2982 2986
74. L. Serrander, V. Jaquet, K. Bedard, O. Plastre, O. Hartley, S. Arnaudeau, N. Demaurex, W. Schlegel, and K.H. Krause NOX5 is expressed at the plasma membrane and generates superoxide in response to protein kinase C activation Biochimie 89 2007 1159 1167 (Pubitemid 47248008)
75. D. Jagnandan, J.E. Church, B. Bánfi, D.J. Stuehr, M.B. Marrero, and D.J. Fulton Novel mechanism of activation of NADPH oxidase 5 calcium sensitization via phosphorylation J. Biol. Chem. 282 2007 6494 6507 (Pubitemid 47100887)
76. S. Tanaka, N. Ishihama, H. Yoshioka, A. Huser, R. O'Connell, G. Tsuji, S. Tsuge, and Y. Kubo The Colletotrichum orbiculare ssd1 mutant enhances Nicotiana benthamiana basal resistance by activating a mitogen-activated protein kinase pathway Plant Cell 21 2009 2517 2526
77. K.-Y. Yang, Y. Liu, and S. Zhang Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco Proc. Natl. Acad. Sci. USA 98 2001 741 746 (Pubitemid 32105113)
78. H. Jin, M.J. Axtell, D. Dahlbeck, O. Ekwenna, S. Zhang, B. Staskawicz, and B. Baker NPK1, an MEKK1-like mitogen-activated protein kinase, regulates innate immunity and development in plants Dev. Cell 3 2002 291 297
79. S. Katou, A. Yamamoto, H. Yoshioka, K. Kawakita, and N. Doke Functional analysis of potato mitogen-activated protein kinase kinase, StMEK1 J. Gen. Plant Pathol. 69 2003 161 168
80. S. Katou, H. Yoshioka, K. Kawakita, O. Rowland, J.D.G. Jones, H. Mori, and N. Doke Involvement of PPS3 phosphorylated by elicitor-responsive mitogen-activated protein kinases in the regulation of plant cell death Plant Physiol. 139 2005 1914 1926 (Pubitemid 43899827)
81. S. Asai, and H. Yoshioka The role of radical burst via MAPK signaling in plant immunity Plant Signal. Behav. 3 2008 920 922
82. S. Asai, and H. Yoshioka Nitric oxide as a partner of reactive oxygen species participates in disease resistance to necrotrophic pathogen Botrytis cinerea in Nicotiana benthamiana Mol. Plant-Microbe Interact. 22 2009 619 629
83. H. Yoshioka, S. Asai, M. Yoshioka, and M. Kobayashi Molecular mechanisms of generation for nitric oxide and reactive oxygen species, and role of the radical burst in plant immunity Mol. Cells 28 2009 321 329
84. P. Wang, Y. Du, Y. Li, D. Ren, and C.-P. Song Hydrogen Peroxide-mediated activation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis Plant Cell 22 2010 2981 2998
85. M. Delledonne NO news is good news for plants Curr. Opin. Plant Biol. 8 2005 390 396 (Pubitemid 40817381)
86. F. Zaninotto, S. La Camera, A. Polverari, and M. Delledonne Cross talk between reactive nitrogen and oxygen species during the hypersensitive disease resistance response Plant Physiol. 141 2006 379 383 (Pubitemid 43974531)
87. M.C. Romero-Puertas, M. Perazzolli, E.D. Zago, and M. Delledonne Nitric oxide signalling functions in plant-pathogen interactions Cell. Microbiol. 9 2004 795 803 (Pubitemid 39162622)
88. + channels indicates direct control by protein nitrosylation in guard cells Plant Physiol. 136 2004 4275 4284
89. A. Feechan, E. Kwon, B.W. Yun, Y. Wang, J.A. Pallas, and G.J. Loake A central role for S-nitrosothiols in plant disease resistance Proc. Natl. Acad. Sci. USA 22 2005 8054 8059 (Pubitemid 40781061)
90. C. Lindermayr, G. Saalbach, and J. Durner Proteomic identification of S-nitrosylated proteins in Arabidopsis Plant Physiol. 137 2005 921 930 (Pubitemid 43138164)
91. R. Gupta, and S. Luan Redox control of protein tyrosine phosphatases and mitogen-activated protein kinases in plants Plant Physiol. 132 2003 1149 1152 (Pubitemid 36872865)
92. Y. Tada, S.H. Spoel, K. Pajerowska-Mukhtar, Z. Mou, J. Song, C. Wang, J. Zuo, and X. Dong Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins Science 321 2008 952 956
93. J.T. Greenberg, and N. Yao The role and regulation of programmed cell death in plant-pathogen interactions Cell. Microbiol. 6 2004 201 211 (Pubitemid 38248004)
94. S. Saito, A. Yamamoto-Katou, H. Yoshioka, N. Doke, and K. Kawakita Peroxynitrite generation and tyrosine nitration in defense responses in tobacco BY-2 cells Plant Cell Physiol. 47 2006 689 697 (Pubitemid 43946297)
95. E. Bonfoco, D. Krainc, M. Ankarcrona, P. Nicotera, and S.A. Lipton Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N -methyl-d-aspartate or nitric oxide/superoxide in cortical cell cultures Proc. Natl. Acad. Sci. USA 92 1995 7162 7166
96. J.M. Alamillo, and F. García-Olmedo Effects of urate, a natural scavenger of peroxynitrite-mediated toxicity, in the response of Arabidopsis thaliana to the bacterial pathogen Pseudomonas syringae Plant J. 25 2001 529 540 (Pubitemid 32442252)
97. L. Zago, S. Morsa, J.F. Dat, P. Alard, A. Ferrarini, D. Inzé, M. Delledonne, and F. Van Breusegem Nitric oxide- and hydrogen peroxide-responsive gene regulation during cell death induction in tobacco Plant Physiol. 141 2006 404 411 (Pubitemid 43974535)
98. S. Asai, K. Mase, and H. Yoshioka A key enzyme for flavin synthesis is required for nitric oxide and reactive oxygen species production in disease resistance Plant J. 62 2010 911 924