Generation of hydrogen peroxide in chloroplasts of arabidopsis overexpressing glycolate oxidase as an inducible system to study oxidative stress

Plant Physiology

Volumn 148, Issue 2, 2008, Pages 719-729

  Fahnenstich, Holger ^a   Scarpeci, Telma E ^b   Valle, Estela M ^b   Flügge, Ulf Ingo ^a   Maurino, Verónica G ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 57749111568     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.108.126789     Document Type: Article

References (58)

1. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55: 373-399
2. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50: 601-659
3. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their function. Plant Physiol 141: 391-396
4. Baxter CJ, Redestig H, Schauer N, Repsilber D, Patil KR, Nielsen J, Selbig J, Liu J, Fernie AR, Sweetlove LJ (2007) The metabolic response of heterotrophic Arabidopsis cells to oxidative stress. Plant Physiol 143: 312-325
5. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44: 276-287
6. Bechtold N, Ellis J, Pelletier G (1993) In planta Agrobacterium-mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C R Acad Sci Paris Life Sci 316: 1194-1199
7. Bechtold U, Richard O, Zamboni A, Gapper C, Geisler M, Pogson B, Karpinski S, Mullineaux P (2008) Impact of chloroplastic- and extracellular-sourced ROS on high light-responsive gene expression in Arabidopsis. J Exp Bot 59: 121-133
8. Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56: 187-220
9. Caspar T, Huber SC, Somerville C (1986) Alterations in growth, photosynthesis and respiration in a starchless mutant of Arabidopsis thaliana (L.) Heynh deficient in chloroplast phosphoglucomutase activity. Plant Physiol 79: 1-7
10. Chang CC, Ball L, Fryer MJ, Baker NR, Karpinski S, Mullineaux PM (2004) Induction of ASCORBATE PEROXIDASE 2 expression in wounded Arabidopsis leaves does not involve known wound-signaling pathways but is associated with changes in photosynthesis. Plant J 38: 499-511
11. Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57: 779-795
12. Dat JF, Pellinen R, Beeckman T, Kangasjärvi J, Langebartels C, Inzé D, Van Breusegem F (2003) Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco. Plant J 33: 621-632
13. Desikan R, Mackerness S, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127: 159-172
14. 4-NADP-malic enzyme causes accelerated senescence during extended darkness. Plant Physiol 145: 640-652
15. Fryer MJ, Bill L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR (2003) Control of Ascorbate Peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. Plant J 33: 691-705
16. Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN, Shulaev V, Apel K, Inzé D, Mittler R, Van Breusegem F (2006) Transcriptomic footprinting discloses specificity of reactive oxygen species signalling in Arabidopsis. Plant Physiol 141: 436-445
17. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990: 87-92
18. Gupta AS, Webb RP, Holaday AS, Allen RD (1993) Overexpression of superoxide dismutase protects plants from oxidative stress (induction of ascorbate peroxidase in superoxide dismutase-overexpressing plants). Plant Physiol 103: 1067-1073
19. Halliwell B (2006) Reactive species and antioxidants: redox biology is a fundamental theme of aerobic life. Plant Physiol 141: 312-322
20. Häusler RE, Bailey KJ, Lea PJ, Leegood RC (1996) Control of photosynthesis in barley mutants with reduced activities of glutamine synthetase and glutamate synthase. Planta 200: 388-396
21. Hellens RP, Edwards EA, Leyland NR, Bean S, Mullineaux PM (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol Biol 42: 819-832
22. Hideg É, Barta C, Kalai T, Hideg K, Asada K (2002) Detection of singlet oxygen and superoxide with fluorescent sensors in leaves under stress by photoinhibition or UV radiation. Plant Cell Physiol 43: 1154-1164
23. Hoch WA, Zeldin EL, McCown BH (2001) Physiological significance of anthocyanins during autumnal leaf senescence. Tree Physiol 21: 1-8
24. Horng JT, Behari R, Burke LECA, Baker A (1995) Investigation of the energy requirement and targeting signal for the import of glycolate oxidase into glyoxysomes. Eur J Biochem 230: 157-163
25. Iqbal A, Yabuta Y, Takeda T, Nakano Y, Shigeoka S (2006) Hydroxyperoxide reduction by thioredoxin-specific glutathione peroxidase isozymes of Arabidopsis thaliana. FEBS J 27: 5589-5597
26. Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen J, Mullineaux PC (1999) Systemic signaling and acclimatation in response to excess excitation energy in Arabidopsis. Science 284: 654-657
27. Kliebenstein D, Monde RA, Last RL (1998) Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol 118: 637-650
28. Kunst L, Browse J, Somerville C (1988) Altered regulation of lipid biosynthesis in a mutant of Arabidopsis deficient in chloroplast glycerol-3-phosphate acyltransferase activity. Proc Natl Acad Sci USA 85: 4143-4147
29. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685
30. Lange H, Shropshire W, Mohr H (1971) An analysis of phytochrome-mediated anthocyanin synthesis. Plant Physiol 47: 649-655
31. -ΔΔCt method. Methods 25: 402-408
32. Miyake C, Asada K (1996) Inactivation mechanism of ascorbate peroxidase at low concentrations of ascorbate: hydrogen peroxide decomposes compound I of ascorbate peroxidase. Plant Cell Physiol 37: 423-430
33. Mullineaux PM, Karpinski S (2002) Signal transduction in response to excess light: getting out of the chloroplast. Curr Opin Plant Biol 5: 43-48
34. Mullineaux PM, Karpinski S, Baker NR (2006) Spatial dependence of hydrogen peroxide-directed signalling in light-stressed plants. Plant Physiol 141: 346-350
35. Nagata T, Todoriki S, Masumizu T, Suda I, Furuta S, Du ZJ, Kikuchi S (2003) Levels of active oxygen species are controlled by ascorbic acid and anthocyanin in Arabidopsis. J Agric Food Chem 51: 2992-2999
36. Nishimura M, Akhmedov YD, Strzalka K, Akazawa T (1983) Purification and characterization of glycolate oxidase from pumpkin cotyledons. Arch Biochem Biophys 222: 397-402
37. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49: 249-279
38. Orozco-Cárdenas ML, Narváez-Vàsquez J, Ryan CA (2001) Hydrogen peroxide acts as second messenger for the induction of defense genes in tomato plants in response to wounding, systemin and methyl jasmonate. Plant Cell 13: 179-191
39. Palatnik JF, Carrillo N, Valle EM (1999) The role of photosynthetic electron transport in the oxidative degradation of chloroplastic glutamine synthetase. Plant Physiol 121: 471-478
40. Pnueli L, Liang H, Rozenberg M, Mittler R (2003) Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants. Plant J 34: 187-203
41. 2-induced cell death. Plant J 52: 640-657
42. Rizhsky L, Liang H, Mittler R (2003) The water-water cycle is essential for chloroplast protection in the absence of stress. J Biol Chem 278: 38921-38925
43. Scarpeci TE, Marro ML, Bortolotti S, Boggio SB, Valle EM (2007) Plant nutritional status modulates glutamine synthetase levels in ripe tomatoes (Solanum lycopersicum cv. Micro-Tom). J Plant Physiol 164: 137-145
44. Scarpeci TE, Valle EM (2008) Rearrangement of carbon metabolism in Arabidopsis thaliana subjected to oxidative stress condition: an emergency survival strategy. Plant Growth Regul 54: 133-142
45. Scarpeci TE, Zanor MI, Carrillo N, Mueller-Roeber B, Valle EM (2008) Generation of superoxide anion in chloroplasts of Arabidopsis thaliana during active photosynthesis: a focus on rapidly induced genes. Plant Mol Biol 66: 361-378
46. Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10: 51-62
47. Smirnoff N (2000) Ascorbate biosynthesis and function in photorespiration. Philos Trans R Soc Lond B Biol Sci 355: 1455-1464
48. Smith CV, Huang CC, Miczak A, Russell DG, Sacchettini JC, Höner zu Bentrup K (2003) Biochemical and structural studies of malate synthase from Mycobacterium tuberculosis. J Biol Chem 278: 1735-1743
49. Steyn WJ, Wand SJE, Holcroft DM, Jacobs G (2002) Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. New Phytol 155: 349-361
50. Tarantino D, Vannini C, Bracale M, Campa M, Soave C, Murgia I (2005) Antisense reduction of thylakoidal ascorbate peroxidase in Arabidopsis enhances paraquat-induced photooxidative stress and nitric oxide-induced cell death. Planta 221: 757-765
51. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11: 1187-1194
52. 2 oxidative photosynthetic carbon cycle. Annu Rev Plant Physiol Plant Mol Biol 48: 1-25
53. Vandenabeele S, Vanderauwera S, Vuylsteke M, Rombauts S, Langebartels C, Seidlitz HK, Zabeau M, Van Montagu M, Inzé D, Van Breusegem F (2004) Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana. Plant J 39: 45-58
54. Vandenabeele S, Van der Kelen K, Dat J, Gadjev I, Boonefaes T, Morsa S, Rottiers P, Slooten L, Van Montagu M, Zabeau M, et al (2003) A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. Proc Natl Acad Sci USA 100: 16113-16118
55. Vanderauwera S, Zimmermann P, Rombauts S, Vandenabeele S, Langebartels C, Gruissem W, Inze D, Van Breusegem F (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
56. Verniquet F, Gaillard J, Neuburger M, Douce R (1991) Rapid inactivation of plant aconitase by hydrogen peroxide. Biochem J 276: 643-648
57. Wingler A, Lea PJ, Quick WP, Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Philos Trans R Soc Lond B Biol Sci 255: 1517-1529
58. Yamaguchi K, Nishimura M (2000) Reduction to below threshold levels of glycolate oxidase activities in transgenic tobacco enhances photoinhibition during irradiation. Plant Cell Physiol 41: 1397-1406