Reactive oxygen species as signals that modulate plant stress responses and programmed cell death

BioEssays

Volumn 28, Issue 11, 2006, Pages 1091-1101

  Gechev, Tsanko S ^a,b   Van Breusegem, Frank ^c   Stone, Julie M ^d   Denev, Iliya ^b   Laloi, Christophe ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF PLOVDIV   (Bulgaria)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE TRANSFERASE; HYDROGEN PEROXIDE; HYDROPEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; OXYGEN; PHYTOHORMONE; POLYUNSATURATED FATTY ACID; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; SUPEROXIDE; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR; ZINC FINGER PROTEIN;

ARABIDOPSIS; CATABOLISM; CELL DEATH; CHLOROPLAST; DETOXIFICATION; HOMEOSTASIS; NONHUMAN; PLANT DEVELOPMENT; PLANT GROWTH; REVIEW; STRESS;

APOPTOSIS; HOMEOSTASIS; OXIDATION-REDUCTION; PLANTS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 33750819157     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.20493     Document Type: Review

References (100)

1. Halliwell B. 2006. Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312-322.
2. Van Breusegem F, Vranová E, Dat JF, Inzé D. 2001. The role of active oxygen species in plant signal transduction. Plant Sci 161:405-414.
3. Gapper C, Dolan L. 2006. Control of plant development by reactive oxygen species. Plant Physiol 141:341-345.
4. Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D et al. 2000. Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779-795.
5. Gechev TS and Hille J. 2005. Hydrogen peroxide as a signal controlling plant programmed cell death. J Cell Biol 168:17-20.
6. 2 across water channels. J Exp Bot 51:2053-2066.
7. Bienert GP, Schjoerring JK, Jahn TP. 2006. Membrane transport of hydrogen peroxide. Biochim Biophys Acta 1758:994-1003.
8. Kehrer JP. 2000, The Haber-Weiss reaction and mechanisms of toxicity. Toxicology 149:43-50.
9. Hintze KJ, Theil EC. 2006. Cellular regulation and molecular interactions of the ferritins. Cell Mol Life Sci 63:591-600.
10. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. 2004. Reactive oxygen gene network of plants. Trends Plant Sci 9:490-498.
11. Laloi C, Przybyla D, Apel K. 2006. A genetic approach towards elucidating the biological activity of different reactive oxygen species in Arabidopsis thaliana. J Exp Bot 57:1719-1724.
12. Asada K. 2006. Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391-396.
13. del Rio LA, Sandalio LM, Corpas FJ, Barroso JB. 2006. Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol 141:330-335.
14. Moller IM. 2001. Plant mitochondria and oxidative stress: Electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52:561-591.
15. Robson CA and Vanlerberghe GC. 2002. Transgenic plant cells lacking mitochondrial alternative oxidase have increased susceptibility to mitochondria-dependent and -independent pathways of programmed cell death. Plant Physiol 129:1908-1920.
16. Foyer CH and Noctor G. 2003. Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355-364.
17. Sagi M and Fluhr R. 2006. Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 141:336-340.
18. Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H et al. 2003. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442-446.
19. Torres MA, Dangl JL, Jones JDG. 2002. Arabidopsis gp91(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.
20. Dellapenna D, Pogson BJ. 2006. Vitamin synthesis in plants: tocopherols and carotenoids. Annu Rev Plant Biol 57:711-738.
21. Passardi F, Penel C, Dunand C. 2004. Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci 9:534-540.
22. Meyer Y, Reichheld JP, Vignols F. 2005. Thioredoxins in Arabidopsis and other plants. Photosynth Res 86:419-433.
23. Rouhier N, Gelhaye E, Jacquot JP. 2004. Plant glutaredoxins: still mysterious reducing systems. Cell Mol Life Sci 61:1266-1277.
24. Prasad TK, Anderson MD, Stewart CR. 1995. Localization and characterization of peroxidases in the mitochondria of chilling-acclimated maize seedlings. Plant Physiol 108:1597-1605.
25. Moons A. 2005. Regulatory and functional interactions of plant growth regulators and plant glutathione S-transferases (GSTs). Plant Hormones 72:155-202.
26. 2 in red and green leaves after mechanical injury. Plant Cell Environ 25:1261-1269.
27. Tsuda T, Kato Y, Osawa T. 2000. Mechanism for the peroxynitrite scavenging activity by anthocyanins. FEBS Lett 484:207-210.
28. Carol RJ, Takeda S, Linstead P, Durrant MC, Kakesova H et al. 2005. A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells Nature 438:1013-1016.
29. Torres MA, Jones JDG, Dangl JL. 2005. Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nature Genet 37:1130-1134.
30. Apel K, Hirt H. 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373-399.
31. Zaninotto F, Camera SL, Polverari A, Delledonne M. 2006. Cross talk between reactive nitrogen and oxygen species during the hypersensitive disease resistance response. Plant Physiol 141:379-383.
32. Kwak JM, Nguyen V, Schroeder JI. 2006. The role of reactive oxygen species in hormonal responses. Plant Physiol 141:323-329.
33. Gechev TS, Minkov IN, Hille J. 2005. Hydrogen peroxide-induced cell death in Arabidopsis: Transcriptional and mutant analysis reveals a role of an oxoglutarate-dependent dioxygenase gene in the cell death process. IUBMB Life 57:181-188.
34. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583-593.
35. Desikan R, Mackerness SAH, Hancock JT, Neill SJ. 2001. Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127:159-172.
36. Vandenabeele S, Van Der Kelen K, Dat J, Gadjev I, Boonefaes T et al. 2003. A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. Proc Natl Acad Sci USA 100:16113-16118.
37. Vandenabeele S, Vanderauwera S, Vuylsteke M, Rombauts S, Langebartels C et al. 2004. Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana. Plant J 39:45-58.
38. Vanderauwera S, Zimmermann P, Rombauts S, Vandenabeele S, Langebartels C et al. 2005. Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiol 139:806-821.
39. Vranová E, Atichartpongkul S, Villarroel R, Van Montagu M, Inzé D et al. 2002. Comprehensive analysis of gene expression in Nicotiana tabacum leaves acclimated to oxidative stress. Proc Natl Acad Sci USA 99:10870-10875.
40. op den Camp RGL, Przybyla D, Ochsenbein C, Laloi C, Kim CH et al. 2003. Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15:2320-2332.
41. +-permeable channels in plant root cells. J Cell Sci 116:81-88.
42. Gadjev I, Vanderauwera S, Gechev T, Laloi C, Minkov I et al. 2006. Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol 141:434-445.
43. Gechev T, Gadjev I, Van Breusegem F, Inzé D, Dukiandjiev S et al. 2002. Hydrogen peroxide protects tobacco from oxidative stress by inducing a set of antioxidant enzymes. Cel Mol Life Sci 59:708-714.
44. 2 in the execution of hypersensitive cell death in tobacco leaves. Plant Physiology 138:1516-1526.
45. Van Breusegem F and Dat J. 2006. Reactive oxygen species in plant cell death. Plant Physiology 141:384-390.
46. Quinn J, Findlay VJ, Dawson K, Millar JBA, Jones N et al. 2002. Distinct regulatory proteins control the graded transcriptional response to increasing H2O2 levels in fission yeast Schizosaccharomyces pombe. Molecular Biology of the Cell 13:805-816.
47. Mullineaux P, Karpinski S, Baker N. 2006. Spatial dependence for hydrogen peroxide-directed signaling in light-stressed plants. Plant Physiol 141:346-350.
48. Nakanomyo I, Kost B, Chua NH, Fukuda H. 2002. Preferential and asymmetrical accumulation of a Rac small GTPase mRNA in differentiating xylem cells of Zinnia elegans. Plant and Cell Physiol 43:1484-1492.
49. Davletova S, Rizhsky L, Liang HJ, Zhong SQ, Oliver DJ et al. 2005. Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17:268-281.
50. 2 and is indispensable for stress defence in C-3 plants. EMBO J 16:4806-4816.
51. 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.
52. Murgia I, Tarantino D, Vannini C, Bracale M, Carravieri S et al. 2004. Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to paraquat-induced photooxidative stress and to nitric oxide-induced cell death. Plant J 38:940-953.
53. Zago E, Morsa S, Dat J, Alard P, Ferranni A et al. 2006. Nitric oxide- and hydrogen peroxide-responsive gene regulation during cell death induction in tobacco. Plant Physiol 141:401-411.
54. Mueller MJ. 2004. Archetype signals in plants: the phytoprostanes. Curr Opin Plant Biol 7:441-448.
55. Loeffler C, Berger S, Guy A, Durand T, Bringmann G et al. 2005. B-1-phytoprostanes trigger plant defense and detoxification responses. Plant Physiol 137:328-340.
56. Liang H, Yao N, Song LT, Luo S, Lu H et al. 2003. Ceramides modulate programmed cell death in plants. Genes Dev 17:2636-2641.
57. Gechev TS, Gadjev IZ, Hille J. 2004. An extensive microarray analysis of AAL-toxin-induced cell death in Arabidopsis thaliana brings new insights into the complexity of programmed cell death in plants. Cell Mol Life Sci 61:1185-1197.
58. Meijer HJG and Munnik T. 2003. Phospholipid-based signaling in plants. Annu Rev Plant Biol 54:265-306.
59. Zhang WH, Wang CX, Qin CB, Wood T, Olafsdottir G et al. 2003. The oleate-stimulated phospholipase D, PLD delta, and phosphatidic acid decrease H2O2-induced cell death in Arabidopsis. Plant Cell 15:2285-2295.
60. Wang KLC, Li H, Ecker JR. 2002. Ethylene biosynthesis and signaling networks. Plant Cell 14:8131-5151.
61. Desikan R, Hancock JT, Bright J, Harrison J, Weir L et al. 2005. A role for ETR1 in hydrogen peroxide signaling in stomatal guard cells. Plant Physiology 137:831-834.
62. Orozco-Cardenas ML, Narvaez-Vasquez J, Ryan CA. 2001. Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13:179-191.
63. Huffaker A, Pearce G, Ryan CA. 2006. An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc Natl Acad Sci USA 103:10098-10103.
64. Meskauskiene R, Nater M, Goslings D, Kessler F, den Camp RO et al. 2001. FLU: A negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 98:12826-12831.
65. Wagner D, Przybyla D, Camp ROD, Kim C, Landgraf F et al. 2004. The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306:1183-1185.
66. Dietrich RA, Richberg MH, Schmidt R, Dean C, Dangl JL. 1997. 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.
67. Epple P, Mack AA, Morris VRF, Dangl JL. 2003. Antagonistic control of oxidative stress-induced cell death in Arabidopsis by two related, plant-specific zinc finger proteins. Proc Natl Acad Sci USA 100:6831-6836.
68. Jabs T, Dietrich RA, Dangl JL. 1996. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273:1853-1856.
69. Talarczyk A, Krzymowska M, Borucki W, Hennig J. 2002. Effect of yeast CTA1 gene expression on response of tobacco plants to tobacco mosaic virus infection. Plant Physiol 129:1032-1044.
70. Kovtun Y, Chiu WL, Tena G, Sheen J. 2000. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 97:2940-2945.
71. Rentel MC, Lecourieux D, Quaked F, Usher SL, Petersen L et al. 2004. OXU kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427:858-861.
72. Nakagami H, Kiegerl S, Hirt H. 2004. OMTK1, a novel MAPKKK, channels oxidative stress signaling through direct MAPK interaction. J Biol Chem 279:26959-26966.
73. Moon H, Lee B, Choi G, Shin S, Prasad DT et al. 2003. NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proc Natl Acad Sci USA 100:358-363.
74. Fukamatsu Y, Yabe N, Hasunuma K. 2003. Arabidopsis NDK1 is a component of ROS signaling by interacting with three catalases. Plant Cell Physiol 44:982-989.
75. Schweighofer A, Hirt H, Meskiene I. 2004. Plant PP2C phosphatases: emerging functions in stress signaling. Trends Plant Sci 9:236-243.
76. 2+ signals through plant protein kinases. Annu Rev Plant Biol 55:263-288.
77. Yang TB and Poovaiah BW. 2002. Hydrogen peroxide homeostasis: activation of plant catalase by calcium/calmodulin. Proc Natl Acad Sci USA 99:4097-4102.
78. Pei ZM, Murata Y, Benning G, Thomine S, Klusener B et al. 2000. Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731-734.
79. Miller G and Mittler R. 2006. Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann Bot 98:279-288.
80. Rizhsky L, Davletova S, Liang HJ, Mittler R. 2004. The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J Biol Chem 279:11736-11743.
81. Davletova S, Schlauch K, Coutu J, Mittler R. 2005. The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 139:847-856.
82. Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA et al. 2003. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623-2633.
83. Swidzinski JA, Sweetlove LJ, Leaver CJ. 2002. A custom microarray analysis of gene expression during programmed cell death in Arabidopsis thaliana. Plant J 30:431-446.
84. Koukalova B, Kovarik A, Fajkus J, Siroky J. 1997. Chromatin fragmentation associated with apoptotic changes in tobacco cells exposed to cold stress. FEBS Letters 414:289-292.
85. Fath A, Bethke PC, Jones RL. 2001. Enzymes that scavenge reactive oxygen species are down-regulation prior to gibberellic acid-induced programmed cell death in barley aleurone. Plant Physiol 126:156-166.
86. Bais HP, Vepachedu R, Gilroy S, Callaway RM, Vivanco JM. 2003. Allelopathy and exotic plant invasion: from molecules and genes to species interactions. Science 301:1377-1380.
87. Dat JF, Pellinen R, Beeckman T, van de Cotte B, Langebartels C et al. 2003. Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco. Plant J 33:621-632.
88. del Rio LA, Corpas FJ, Sandalio LM, Palma JM, Barroso JB. 2003. Plant peroxisomes, reactive oxygen metabolism and nitric oxide. IUBMB Life 55:71-81.
89. Zapata JM, Guera A, Esteban-Carrasco A, Martin M, Sabater B. 2006. Chloroplasts regulate leaf senescence: delayed senescence in transgenic ndhF-defective tobacco. Cell Death Differ 12:1277-1284.
90. Palma K and Kermode AR. 2003. Metabolism of hydrogen peroxide during reserve mobilization and programmed cell death of barley (Hordeum vulgare L.) aleurone layer cells. Free Rad Biol Med 35:1261-1270.
91. Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA et al. 1998. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773-784.
92. Stone JM, Heard JE, Asai T, Ausubel FM. 2000. Simulation of fungal-mediated cell death by fumonisin B1 and selection of fumonisin B1-resistant (fbr) Arabidopsis mutants. Plant Cell 12:1811-1822.
93. Prasad TK, Anderson MD, Martin BA, Stewart CR. 1994. Evidence for chilling-induced oxidative stress in maize seedlings and a regulatoryrole for hydrogen peroxide. Plant Cell 6:65-74.
94. Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G et al. 1999. Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284:654-657.
95. 2. J Exp Bot 49:713-720.
96. 2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol 116:1351-1357.
97. 2 in transgenic tobacco. Proc Natl Acad Sci USA 95:5818-5823.
98. Oono Y, Seki M, Satou M, Iida K, Akiyama K et al. 2006. Monitoring expression profiles of Arabidopsis genes during cold acclimation and deacclimation using DNA microarrays. Funct Integr Genomics 4:1-23.
99. Charng YY, Liu HC, Liu NY, Hsu FC, Ko SS. 2006. Arabidopsis Hsa32, a novel heat shock protein, is essential for acquired thermotolerance during long recovery after acclimation. Plant Physiol 140:1297-1305.
100. Mittler R. 2006. Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15-19.