Proteomic and biochemical analyses show a functional network of proteins involved in antioxidant defense of the arabidopsis anp2anp3 double mutant

Journal of Proteome Research

Volumn 13, Issue 12, 2014, Pages 5347-5361

  Takáč, Tomáš ^a   Šamajová, Olga ^a   Vadovič, Pavol ^a   Pechan, Tibor ^b   Košútová, Petra ^a   Ovečka, Miroslav ^a   Husičková, Alexandra ^a   Komis, George ^a   Šamaj, Jozef ^a  

^a PALACKÝ UNIVERSITY   (Czech Republic)

^b MISSISSIPPI STATE UNIVERSITY   (United States)

Author keywords

ANP2; ANP3; antioxidant defense; Arabidopsis; mitogen activated protein kinase kinase kinase; oxidative stress; proteomics; signaling

Indexed keywords

ARABIDOPSIS PROTEIN; ARABIDOPSIS THALIANA HOMOLOGUE OF NUCLEUS AND PHRAGMOPLASTLOCALIZED KINASE 2; ARABIDOPSIS THALIANA HOMOLOGUE OF NUCLEUS AND PHRAGMOPLASTLOCALIZED KINASE 3; ASCORBIC ACID; BISPHOSPHOGLYCERATE MUTASE; CALMODULIN 4; CARBONATE DEHYDRATASE I; CATALASE; CHAPERONIN 20; CPN20 PROTEIN; FERREDOXIN 2; GLUTATHIONE; LIPOXYGENASE; LIPOXYGENASE 2; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; PORIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REGULATOR PROTEIN; RIBULOSEBISPHOSPHATE CARBOXYLASE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; ANP2 PROTEIN, ARABIDOPSIS; ANP3 PROTEIN, ARABIDOPSIS; ANTIOXIDANT; HERBICIDE; PARAQUAT; PROTEOME;

ARABIDOPSIS THALIANA; ARTICLE; BIOCHEMISTRY; COMPARATIVE STUDY; CONTROLLED STUDY; ENVIRONMENTAL STRESS; ENZYME ACTIVITY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHOTOSYNTHESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS; QUANTITATIVE ANALYSIS; SEEDLING; SIGNAL TRANSDUCTION; UPREGULATION; ARABIDOPSIS; BIOLOGICAL MODEL; DRUG EFFECTS; GENETICS; IMMUNOBLOTTING; LIQUID CHROMATOGRAPHY; METABOLISM; MUTATION; PROCEDURES; TANDEM MASS SPECTROMETRY;

ARABIDOPSIS;

ANTIOXIDANTS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMATOGRAPHY, LIQUID; HERBICIDES; IMMUNOBLOTTING; MAP KINASE KINASE KINASES; MODELS, BIOLOGICAL; MUTATION; PARAQUAT; PROTEOME; PROTEOMICS; REACTIVE OXYGEN SPECIES; SEEDLINGS; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE; TANDEM MASS SPECTROMETRY;

EID: 84915751026     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr500588c     Document Type: Article

References (91)

1. Rodriguez, M. C. S.; Petersen, M.; Mundy, J. Mitogen-activated protein kinase signaling in plants Annu. Rev. Plant Biol. 2010, 61, 621-649
2. Šamajová, O.; Plíhal, O.; Al-Yousif, M.; Hirt, H.; Šamaj, J. Improvement of stress tolerance in plants by genetic manipulation of mitogen-activated protein kinases Biotechnol. Adv. 2013, 31, 118-128
3. Andreasson, E.; Ellis, B. Convergence and specificity in the Arabidopsis MAPK nexus Trends Plant Sci. 2010, 15, 106-113
4. Krysan, P. J.; Jester, P. J.; Gottwald, J. R.; Sussman, M. R. An Arabidopsis mitogen-activated protein kinase kinase kinase gene family encodes essential positive regulators of cytokinesis Plant Cell 2002, 14, 1109-1120
5. Sasabe, M.; Soyano, T.; Takahashi, Y.; Sonobe, S.; Igarashi, H.; Itoh, T. J.; Hidaka, M.; Machida, Y. Phosphorylation of NtMAP65-1 by a MAP kinase down-regulates its activity of microtubule bundling and stimulates progression of cytokinesis of tobacco cells Genes Dev. 2006, 20, 1004-1014
6. Takahashi, Y.; Soyano, T.; Kosetsu, K.; Sasabe, M.; Machida, Y. HINKEL kinesin, ANP MAPKKKs and MKK6/ANQ MAPKK, which phosphorylates and activates MPK4 MAPK, constitute a pathway that is required for cytokinesis in Arabidopsis thaliana Plant Cell Physiol. 2010, 51, 1766-1776
7. Beck, M.; Komis, G.; Muller, J.; Menzel, D.; Šamaj, J. Arabidopsis homologs of nucleus- and phragmoplast-localized kinase 2 and 3 and mitogen-activated protein kinase 4 are essential for microtubule organization Plant Cell 2010, 22, 755-771
8. Sasabe, M.; Machida, Y. Regulation of organization and function of microtubules by the mitogen-activated protein kinase cascade during plant cytokinesis Cytoskeleton (Hoboken) 2012, 69, 913-918
9. Kovtun, Y.; Chiu, W. L.; Tena, G.; Sheen, J. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants Proc. Natl. Acad. Sci. U. S. A. 2000, 97, 2940-2945
10. Savatin, D. V.; Bisceglia, N. G.; Marti, L.; Fabbri, C.; Cervone, F.; Lorenzo, G. D. The Arabidopsis Nucleus- And Phragmoplast-Localized Kinase1-Related Protein Kinases Are Required for Elicitor-Induced Oxidative Burst and Immunity Plant Physiol. 2014, 165, 1188-1202
11. Gawroński, P.; Witoń, D.; Vashutina, K.; Bederska, M.; Betliński, B.; Rusaczonek, A.; Karpiński, S. Mitogen-Activated Protein Kinase 4 Is a Salicylic Acid-Independent Regulator of Growth But Not of Photosynthesis in Arabidopsis Mol. Plant 2014, 7, 1151-1166
12. Pitzschke, A.; Djamei, A.; Bitton, F.; Hirt, H. A major role of the MEKK1-MKK1/2-MPK4 pathway in ROS signalling Mol. Plant 2009, 2, 120-137
13. Nakagami, H.; Soukupová, H.; Schikora, A.; Zárský, V.; Hirt, H. A Mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis J. Biol. Chem. 2006, 281, 38697-38704
14. Xing, Y.; Cao, Q.; Zhang, Q.; Qin, L.; Jia, W.; Zhang, J. MKK5 regulates high light-induced gene expression of Cu/Zn superoxide dismutase 1 and 2 in Arabidopsis Plant Cell Physiol. 2013, 54, 1217-1227
15. 2 production in Arabidopsis J. Exp. Bot. 2007, 58, 2969-2981
16. 2 production via AtMPK6-coupled signaling in Arabidopsis Plant J. Cell Mol. Biol. 2008, 54, 440-451
17. Murashige, T.; Skoog, F. A revised medium for rapid growth and bio assays with tobacco tissue cultures Physiol. Plant. 1962, 15, 473-497
18. Takáč, T.; Pechan, T.; Richter, H.; Müller, J.; Eck, C.; Böhm, N.; Obert, B.; Ren, H.; Niehaus, K.; Šamaj, J. Proteomics on brefeldin A-treated Arabidopsis roots reveals profilin 2 as a new protein involved in the cross-talk between vesicular trafficking and the actin cytoskeleton J. Proteome Res. 2011, 10, 488-501
19. Hurkman, W. J.; Tanaka, C. K. Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis Plant Physiol. 1986, 81, 802-806
20. Bridges, S. M.; Magee, G. B.; Wang, N.; Williams, W. P.; Burgess, S. C.; Nanduri, B. ProtQuant: a tool for the label-free quantification of MudPIT proteomics data BMC Bioinformatics 2007, 8 (Suppl 7) S24
21. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 1976, 72, 248-254
22. Pan, S. M.; Yau, Y. Y. Characterization of superoxide dismutase in Arabidopsis Plant Cell Physiol. 1998, 37, 58-66
23. Beauchamp, C.; Fridovich, I. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels Anal. Biochem. 1971, 44, 276-87
24. Amako, K.; Chen, G. X.; Asada, K. Separate assays specific for ascorbate peroxidase and guaiacol peroxidase and for the chloroplastic and cytosolic isozymes of ascorbate peroxidase in plants Plant Cell Physiol. 1994, 35, 497-504
25. Nakano, Y.; Asada, K. Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts Plant Cell Physiol. 1981, 22, 867-880
26. Gillespie, K. M.; Ainsworth, E. A. Measurement of reduced, oxidized and total ascorbate content in plants Nat. Protoc. 2007, 2, 871-874
27. Sagi, M.; Fluhr, R. Superoxide production by plant homologues of the gp91(phox) NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection Plant Physiol. 2001, 126, 1281-1290
28. Able, A. J.; Guest, D. I.; Sutherland, M. W. Use of a new tetrazolium-based assay to study the production of superoxide radicals by tobacco cell cultures challenged with avirulent zoospores of Phytophthora parasitica var nicotianae Plant Physiol. 1998, 117, 491-499
29. Cheeseman, J. M. Hydrogen peroxide concentrations in leaves under natural conditions J. Exp. Bot. 2006, 57, 2435-2444
30. Ramel, F.; Sulmon, C.; Bogard, M.; Couée, I.; Gouesbet, G. Differential patterns of reactive oxygen species and antioxidative mechanisms during atrazine injury and sucrose-induced tolerance in Arabidopsis thaliana plantlets BMC Plant Biol. 2009, 9, 28
31. Daudi, A.; Cheng, Z.; O'Brien, J. A.; Mammarella, N.; Khan, S.; Ausubel, F. M.; Bolwell, G. P. The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity Plant Cell 2012, 24, 275-287
32. Oxborough, K.; Baker, N. R. Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components-calculation of qP and Fv′/Fm′ without measuring Fo′ Photosynth. Res. 1997, 54, 135-142
33. Jensen, L. J.; Kuhn, M.; Stark, M.; Chaffron, S.; Creevey, C.; Muller, J.; Doerks, T.; Julien, P.; Roth, A.; Simonovic, M.; Bork, P.; von Mering, C. STRING 8-a global view on proteins and their functional interactions in 630 organisms Nucleic Acids Res. 2009, 37, D412-416
34. McCormack, E.; Tsai, Y.-C.; Braam, J. Handling calcium signaling: Arabidopsis CaMs and CMLs Trends Plant Sci. 2005, 10, 383-389
35. Kuo, W. Y.; Huang, C. H.; Liu, A. C.; Cheng, C. P.; Li, S. H.; Chang, W. C.; Weiss, C.; Azem, A.; Jinn, T. L. CHAPERONIN 20 mediates iron superoxide dismutase (FeSOD) activity independent of its co-chaperonin role in Arabidopsis chloroplasts New Phytol. 2013, 197, 99-110
36. Camacho, L.; Smertenko, A. P.; Perez-Gomez, J.; Hussey, P. J.; Moore, I. Arabidopsis Rab-E GTPases Exhibit a Novel Interaction with a Plasma-membrane Phosphatidylinositol-4-phosphate 5-kinase J. Cell Sci. 2009, 122, 4383-4392
37. Seltmann, M. A.; Stingl, N. E.; Lautenschlaeger, J. K.; Krischke, M.; Mueller, M. J.; Berger, S. Differential impact of lipoxygenase 2 and jasmonates on natural and stress-induced senescence in Arabidopsis Plant Physiol. 2010, 152, 1940-1950
38. Takahashi, F.; Yoshida, R.; Ichimura, K.; Mizoguchi, T.; Seo, S.; Yonezawa, M.; Maruyama, K.; Yamaguchi-Shinozaki, K.; Shinozaki, K. The mitogen-activated protein kinase cascade MKK3-MPK6 is an important part of the jasmonate signal transduction pathway in Arabidopsis Plant Cell 2007, 19, 805-818
39. Pilon, M.; Ravet, K.; Tapken, W. The biogenesis and physiological function of chloroplast superoxide dismutases Biochim. Biophys. Acta BBA-Bioenerg. 2011, 1807, 989-998
40. Gallie, D. R. The Role of L-ascorbic acid recycling in responding to environmental stress and in promoting plant growth J. Exp. Bot. 2013, 64, 433-443
41. Smirnoff, N. Ascorbate biosynthesis and function in photoprotection Philos. Trans. R. Soc. London, B: Biol. Sci. 2000, 355, 1455-1464
42. Wolucka, B. A.; Van Montagu, M. GDP-mannose 3′,5′-epimerase forms GDP-L-gulose, a putative intermediate for the de novo biosynthesis of vitamin C in plants J. Biol. Chem. 2003, 278, 47483-47490
43. Valpuesta, V.; Botella, M. A. Biosynthesis of L-ascorbic acid in plants: new pathways for an old antioxidant Trends Plant Sci. 2004, 9, 573-577
44. Bus, J. S.; Aust, S. D.; Gibson, J. E. Superoxide- and singlet oxygen-catalyzed lipid peroxidation as a possible mechanism for paraquat (methyl viologen) toxicity Biochem. Biophys. Res. Commun. 1974, 58, 749-755
45. Karpiński, S.; Szechyńska-Hebda, M.; Wituszyńska, W.; Burdiak, P. Light acclimation, retrograde signalling, cell death and immune defenses in plants Plant Cell Environ. 2013, 36, 736-744
46. Pesaresi, P.; Scharfenberg, M.; Weigel, M.; Granlund, I.; Schröder, W. P.; Finazzi, G.; Rappaport, F.; Masiero, S.; Furini, A.; Jahns, P.; Leister, D. Mutants, overexpressors, and interactors of Arabidopsis plastocyanin isoforms: revised roles of plastocyanin in photosynthetic electron flow and thylakoid redox state Mol. Plant 2009, 2, 236-248
47. Allahverdiyeva, Y.; Suorsa, M.; Rossi, F.; Pavesi, A.; Kater, M. M.; Antonacci, A.; Tadini, L.; Pribil, M.; Schneider, A.; Wanner, G.; Leister, D.; Aro, E. M.; Barbato, R.; Pesaresi, P. Arabidopsis plants lacking PsbQ and PsbR subunits of the oxygen-evolving complex show altered PSII super-complex organization and short-term adaptive mechanisms Plant J. 2013, 75, 671-684
48. Ihnatowicz, A.; Pesaresi, P.; Varotto, C.; Richly, E.; Schneider, A.; Jahns, P.; Salamini, F.; Leister, D. Mutants for photosystem I subunit D of Arabidopsis thaliana: effects on photosynthesis, photosystem I stability and expression of nuclear genes for chloroplast functions Plant J. 2004, 37, 839-52
49. Sinha, A. K.; Jaggi, M.; Raghuram, B.; Tuteja, N. Mitogen-activated protein kinase signaling in plants under abiotic stress Plant Signal. Behav. 2011, 6, 196-203
50. Li, G.; Peng, X.; Xuan, H.; Wei, L.; Yang, Y.; Guo, T.; Kang, G. Proteomic analysis of leaves and roots of common wheat (Triticum aestivum L.) under copper-stress conditions J. Proteome Res. 2013, 12, 4846-4861
51. Hossain, Z.; Khatoon, A.; Komatsu, S. Soybean proteomics for unraveling abiotic stress response mechanism J. Proteome Res. 2013, 12, 4670-4684
52. Singh, R.; Jwa, N. S. Understanding the responses of rice to environmental stress using proteomics J. Proteome Res. 2013, 12, 4652-4669
53. Amme, S.; Matros, A.; Schlesier, B.; Mock, H. P. Proteome analysis of cold stress response in Arabidopsis thaliana using DIGE-technology J. Exp. Bot. 2006, 57, 1537-1546
54. Wang, H.; Wang, S.; Lu, Y.; Alvarez, S.; Hicks, L. M.; Ge, X.; Xia, Y. Proteomic analysis of early-responsive redox-sensitive proteins in Arabidopsis J. Proteome Res. 2012, 11, 412-424
55. Du, H.; Liang, Y.; Pei, K.; Ma, K. UV radiation-responsive proteins in rice leaves: a proteomic analysis Plant Cell Physiol. 2011, 52, 306-316
56. Jiang, Y.; Yang, B.; Harris, N. S.; Deyholos, M. K. Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots J. Exp. Bot. 2007, 58, 3591-3607
57. Foyer, C. H.; Noctor, G. Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications Antioxidants Redox Signal. 2009, 11, 861-905
58. Suzuki, N.; Koussevitzky, S.; Mittler, R.; Miller, G. ROS and Redox Signalling in the Response of Plants to Abiotic Stress Plant Cell Environ. 2012, 35, 259-270
59. Apel, K.; Hirt, H. REACTIVE OXYGEN SPECIES: Metabolism, oxidative stress, and signal transduction Annu. Rev. Plant Biol. 2004, 55, 373-399
60. Farmer, E. E.; Mueller, M. J. ROS-mediated lipid peroxidation and RES-activated signaling Annu. Rev. Plant Biol. 2013, 64, 429-450
61. Jacques, S.; Ghesquière, B.; Van Breusegem, F.; Gevaert, K. Plant proteins under oxidative attack Proteomics 2013, 13, 932-940
62. 2-induced leaf cell death and the crosstalk of reactive nitric/oxygen species J. Integr. Plant Biol. 2013, 55, 202-208
63. Hideg, E.; Jansen, M. A.; Strid, A. UV-B exposure, ROS, and stress: inseparable companions or loosely linked associates? Trends Plant Sci. 2013, 18, 107-115
64. Jaspers, P.; Kangasjärvi, J. Reactive oxygen species in abiotic stress signaling Physiol. Plant. 2010, 138, 405-413
65. Hossain, Z.; Komatsu, S. Contribution of proteomic studies towards understanding plant heavy metal stress response Front. Plant Sci. 2013, 3, 310
66. González Besteiro, M. A.; Bartels, S.; Albert, A.; Ulm, R. Arabidopsis MAP kinase phosphatase 1 and its target MAP kinases 3 and 6 antagonistically determine UV-B stress tolerance, independent of the UVR8 photoreceptor pathway Plant J. 2011, 68, 727-737
67. Lee, J. S.; Ellis, B. E. Arabidopsis MAPK phosphatase 2 (MKP2) positively regulates oxidative stress tolerance and inactivates the MPK3 and MPK6 MAPKs J. Biol. Chem. 2007, 282, 25020-25029
68. 2 production via AtMPK6-coupled signaling in Arabidopsis Plant J. 2008, 54, 440-451
69. Kliebenstein, D. J.; Monde, R. A.; Last, R. L. Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization Plant Physiol. 1998, 118, 637-650
70. Van Breusegem, F.; Slooten, L.; Stassart, J. M.; Moens, T.; Botterman, J.; Van Montagu, M.; Inzé, D. Overproduction of Arabidopsis thaliana FeSOD confers oxidative stress tolerance to transgenic maize Plant Cell Physiol. 1999, 40, 515-523
71. Morgan, M. J.; Lehmann, M.; Schwarzländer, M.; Baxter, C. J.; Sienkiewicz-Porzucek, A.; Williams, T. C. R.; Schauer, N.; Fernie, A. R.; Fricker, M. D.; Ratcliffe, R. G. Decrease in manganese superoxide dismutase leads to reduced root growth and affects tricarboxylic acid cycle flux and mitochondrial redox homeostasis Plant Physiol. 2008, 147, 101-114
72. Hodgson, R. A.; Raison, J. K. Superoxide production by thylakoids during chilling and its implication in the susceptibility of plants to chilling-induced photoinhibition Planta 1991, 183, 222-228
73. Torres, M. A.; Dangl, J. L.; Jones, J. D. G. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 517-522
74. Jiang, M.; Zhang, J. Involvement of plasma-membrane NADPH oxidase in abscisic acid- and water stress-induced antioxidant defense in leaves of maize seedlings Planta 2002, 215, 1022-1030
75. Hao, F.; Wang, X.; Chen, J. Involvement of plasma-membrane NADPH oxidase in nickel-induced oxidative stress in roots of wheat seedlings Plant Sci. 2006, 170, 151-158
76. Desikan, R.; Cheung, M.-K.; Bright, J.; Henson, D.; Hancock, J. T.; Neill, S. J. ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells J. Exp. Bot. 2004, 55, 205-212
77. Foreman, J.; Demidchik, V.; Bothwell, J. H. F.; Mylona, P.; Miedema, H.; Torres, M. A.; Linstead, P.; Costa, S.; Brownlee, C.; Jones, J. D. G. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth Nature 2003, 422, 442-446
78. Kim, S.-H.; Woo, D.-H.; Kim, J.-M.; Lee, S.-Y.; Chung, W. S.; Moon, Y.-H. Arabidopsis MKK4 mediates osmotic-stress response via its regulation of MPK3 activity Biochem. Biophys. Res. Commun. 2011, 412, 150-154
79. Colcombet, J.; Hirt, H. Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes Biochem. J. 2008, 413, 217-226
80. Takahashi, F.; Mizoguchi, T.; Yoshida, R.; Ichimura, K.; Shinozaki, K. Calmodulin-Dependent Activation of MAP Kinase for ROS Homeostasis in Arabidopsis Mol. Cell 2011, 41, 649-660
81. Yoshida, S.; Tamaoki, M.; Shikano, T.; Nakajima, N.; Ogawa, D.; Ioki, M.; Aono, M.; Kubo, A.; Kamada, H.; Inoue, Y.; Saji, H. Cytosolic dehydroascorbate reductase is important for ozone tolerance in Arabidopsis thaliana Plant Cell Physiol. 2006, 47, 304-308
82. Chen, Z.; Young, T. E.; Ling, J.; Chang, S.-C.; Gallie, D. R. Increasing vitamin C content of plants through enhanced ascorbate recycling Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 3525-3530
83. Chen, Z.; Gallie, D. R. Dehydroascorbate Reductase Affects Leaf Growth, Development, and Function Plant Physiol. 2006, 142, 775-787
84. Foyer, C. H.; Noctor, G. Ascorbate and Glutathione: The Heart of the Redox Hub Plant Physiol. 2011, 155, 2-18
85. Conklin, P. L.; Norris, S. R.; Wheeler, G. L.; Williams, E. H.; Smirnoff, N.; Last, R. L. Genetic evidence for the role of GDP-mannose in plant ascorbic acid (vitamin C) biosynthesis Proc. Natl. Acad. Sci. U. S. A. 1999, 96, 4198-4203
86. Van Breusegem, F.; Vranová, E.; Dat, J. F.; Inzé, D. The role of active oxygen species in plant signal transduction Plant Sci. 2001, 161, 405-414
87. Yao, N.; Tada, Y.; Park, P.; Nakayashiki, H.; Tosa, Y.; Mayama, S. Novel evidence for apoptotic cell response and differential signals in chromatin condensation and DNA cleavage in victorin-treated oats Plant J. 2001, 28, 13-26
88. Gupta, A. S.; Webb, R. P.; Holaday, A. S.; Allen, R. D. Overexpression of Superoxide Dismutase Protects Plants from Oxidative Stress (Induction of Ascorbate Peroxidase in Superoxide Dismutase-Overexpressing Plants) Plant Physiol. 1993, 103, 1067-1073
89. Kwon, S. Y.; Jeong, Y. J.; Lee, H. S.; Kim, J. S.; Cho, K. Y.; Allen, R. D.; Kwak, S. S. Enhanced tolerances of transgenic tobacco plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against methyl viologen-mediated oxidative stress Plant, Cell Environ. 2002, 25, 873-882
90. Camp, W. V.; Capiau, K.; Montagu, M. V.; Inze, D.; Slooten, L. Enhancement of Oxidative Stress Tolerance in Transgenic Tobacco Plants Overproducing Fe-Superoxide Dismutase in Chloroplasts Plant Physiol. 1996, 112, 1703-1714
91. Eng, J.; McCormack, A.; Yates, J. R. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database J. Am. Soc. Mass. Spectrom. 1994, 5, 976-989