Ascorbic acid deficiency activates cell death and disease resistance responses in Arabidopsis

Plant Physiology

Volumn 139, Issue 3, 2005, Pages 1291-1303

  Pavet, Valeria ^a   Olmos, Enrique ^b,c   Kiddle, Guy ^b   Mowla, Shaheen ^b   Kumar, Sanjay ^b,d   Antoniw, John ^b   Alvarez, María E ^a   Foyer, Christine H ^b  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

^b ROTHAMSTED RESEARCH   (United Kingdom)

^c RESEARCH GROUP ON QUALITY   (Spain)

^d CSIR INSTITUTE OF HIMALAYAN BIORESOURCE TECHNOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYLIC ACIDS; CELLS; DISEASE CONTROL; PLANTS (BOTANY);

COMPLEX GENETIC CONTROLS; PATHOGENESIS-RELATED (PR) PROTEINS; PROGRAMMED CELL DEATH; REDOX REGULATION;

GENETIC ENGINEERING;

CARBOXYLIC ACIDS; CELLS; DISEASES; GENETIC ENGINEERING; PLANTS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; PSEUDOMONAS SYRINGAE;

ANTIOXIDANT; ARABIDOPSIS PROTEIN; ASCORBIC ACID; CYSTEINE PROTEINASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; NPR1 PROTEIN, ARABIDOPSIS; SAG12 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; BACTERIAL GENE; CELL DEATH; CELL NUCLEUS; CELL SIZE; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; METABOLISM; MICROBIOLOGY; MUTATION; OXIDATION REDUCTION REACTION; PHENOTYPE; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PROTEIN TRANSPORT; PSEUDOMONAS SYRINGAE;

ANTIOXIDANTS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ASCORBIC ACID; CELL DEATH; CELL NUCLEUS; CELL SIZE; CYSTEINE ENDOPEPTIDASES; GENE EXPRESSION REGULATION, PLANT; GENES, BACTERIAL; GLUTATHIONE; GLUTATHIONE DISULFIDE; MUTATION; OXIDATION-REDUCTION; PHENOTYPE; PLANT DISEASES; PLANT LEAVES; PROTEIN TRANSPORT; PSEUDOMONAS SYRINGAE;

EID: 33644844932     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.105.067686     Document Type: Article

References (67)

1. Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity Cell 20: 773-784
2. Apel K, Hirt H (2004) Reactive oxygen species; metabolism, oxidative stress, and signal transduction. Annu Rev Plant Physiol Plant Mol Biol 55: 373-399
3. Arrigoni O, de Tullio MC (2000) The role of ascorbic acid in cell metabolism: between gene-directed functions and unpredictable chemical reactions. J Plant Physiol 157: 481-488
4. Balagué C, Lin B, Alcon C, Flottes G, Malmstrom S, Kohler C, Neuhaus G, Pelletier G, Gaymard F, Roby D (2003) HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family. Plant Cell 15: 365-379
5. Barth C, Moeder W, Klessig DF, Conklin PL (2004) The timing of senescence and response to pathogens is altered in ascorbate-deficient mutant vitamin C-1. Plant Physiol 134: 178-192
6. Boccara M, Boue C, Garmier M, De Paepe R, Boccara AC (2001) Infra-red thermography revealed a role for mitochondria in pre-symptomatic cooling during harpin-induced hypersensitive response. Plant J 28: 663-670
7. Cameron R, Dixon RA, Lamb CJ (1994) Biologically induced systemic acquired resistance in Arabidopsis thaliana. Plant J 5: 715-725
8. Cao H, Bowling SA, Gordon S, Dong X (1994) Characterization of an Arabidopsis mutant that is non-responsive to inducers of systemic acquired resistance. Plant Cell 6: 1583-1592
9. Chamnongpol S, Willekens H, Langebartels C, Van Montagu M, Inze D, Van Camp W (1996) Transgenic tobacco with a reduced catalase activity develops necrotic lesions and induces pathogenesis-related expression under high light. Plant J 10: 491-503
10. Chen C, Dickman MB (2004) Bcl-2 family members localize to tobacco chloroplasts and inhibit programmed cell death induced by chloroplast-targeted herbicides. J Exp Bot 55: 2617-2623
11. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
12. Conklin PL, Norris SR, Wheeler GL, Williams EH, Smirnoff N, Last RL (1999) Genetic evidence for the role of GDP-mannose in plant ascorbic acid (vitamin C) biosynthesis. Proc Natl Acad Sci USA 30: 4198-4203
13. Conklin PL, Williams EH, Last RL (1996) Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant. Proc Natl Acad Sci USA 3: 9970-9974
14. Conklin PL, Saracco SA, Norris SR, Last RL (2000) Identification of ascorbic acid deficient Arabidopsis thaliana mutants. Genetics 154: 847-856
15. Delaney TP, Friedrich L, Ryals JA (1995) Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc Natl Acad Sci USA 92: 6602-6606
16. 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
17. de Pinto MC, De Gara L (2004) Changes in the ascorbate metabolism of apoplastic and symplastic spaces are associated with cell differentiation. J Exp Bot 55: 2559-2569
18. Desikan R, A-H-Mackerness S, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127: 159-172
19. Després C, Chubak C, Rochon A, Clark R, Bethune T, Desveaux D, Fobert PR (2003) The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. Plant Cell 15: 2181-2191
20. Devadas SK, Enyedi A, Raina R (2002) The Arabidopsis hrl1 mutation reveals novel overlapping roles for salicylic acid, jasmonic acid and ethylene signalling in cell death and defence against pathogens. Plant J 30: 467-480
21. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, et al (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422: 442-446
22. Foyer CH (2004) The role of ascorbic acid in defence networks and signalling in plants. In H Asard, JM May, N Smirnoff, eds, Vitamin C. Functions and Biochemistry in Animals and Plants. BIOS Scientific Publishers, Oxon, UK, pp 65-82
23. Foyer CH, Noctor G (2005a) Redox homeostasis and antioxidant signalling; a metabolic interface between stress perception and physiological responses. Plant Cell 17: 1866-1875
24. Foyer CH, Noctor G (2005b) Oxidant and antioxidant signalling in plants; a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28: 1056-1071
25. Fry SC (1998) Oxidative scission of plant cell wall polysaccharides by ascorbate-induced hydroxyl radicals. Biochem J 332: 507-515
26. Gomez LD, Noctor G, Knight MR, Foyer CH (2004) Regulation of calcium signalling and gene expression by glutathione. J Exp Bot 55: 1851-1859
27. Green R, Fluhr R (1995) UV-B-induced PR-1 accumulation is mediated by active oxygen species. Plant Cell 7: 203-212
28. Hensel LL, Grbic V, Baumgarten DA, Bleecker AB (1993) Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in Arabidopsis. Plant Cell 5: 553-564
29. Jabs T, Dietrich RA, Dangl JL (1996) Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273: 1853-1856
30. Jambunathan N, Siani JM, McNellis TW (2001) A humidity-sensitive Arabidopsis copine mutant exhibits precocious cell death and increased disease resistance. Plant Cell 13: 2225-2240
31. Jones B, Frasse P, Olmos E, Zegzouti H, Leclerq J, Tournier B, Latché A, Pech JC, Bouzayen M (2002) Down-regulation of DR12, an auxin-response-factor homolog, in the tomato results in pleiotropic phenotype including dark-green and blotchy ripening fruit. Plant J 32: 603-613
32. Joo JH, Bae YS, Lee JS (2001) Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol 126: 1055-1060
33. Joo JH, Wang S, Chen JG, Jones AM, Fedoroff NV (2005) Different signalling and cell death roles of heterotrimeric G protein a and b subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell 17: 957-970
34. Kiddle G, Pastori GM, Bernard B, Pignocchi C, Antoniw J, Verrier PJ, Foyer CH (2003) Effects of leaf ascorbate content on defense and photosynthesis gene expression in Arabidopsis thaliana. Antioxid Redox Signal 5: 23-32
35. Kinkema M, Fan W, Dong X (2000) Nuclear localisation of NPR1 is required for activation of PR gene expression. Plant Cell 12: 2339-2350
36. Laloi C, Apel K, Danon A (2004) Reactive oxygen signalling: the latest news. Curr Opin Plant Biol 7: 323-328
37. Levine A, Pennell RI, Alvarez ME, Palmer R, Lamb C (1996) Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr Biol 6: 427-437
38. Lorrain S, Vailleau F, Balague C, Roby D (2003) Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci 8: 263-271
39. Mateo A, Mühlenbock P, Rustérucci C, Chang CCC, Miszalski Z, Karpinska B, Parker JE, Mullineaus PM, Karpinski S (2004) LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiol 136: 2818-2830
40. Matsumura H, Nirasawa S, Kiba A, Urasaki N, Saitoh H, Ito M, Kawai-Yamada M, Uchimiya H, Terauchi R (2003) Overexpression of Bax inhibitor suppresses the fungal elicitor-induced cell death in rice (Oryza sativa L) cells. Plant J 33: 425-434
41. Maxwell DP, Nickels R, McIntosh L (2002) Evidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescence. Plant J 29: 269-279
42. McCormac AC, Elliott MC, Chen DF (1998) A simple method for the production of highly competent cells of Agrobacterium for transformation via electroporation. Mol Biotechnol 9: 155-159
43. Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 27: 935-944
44. Mulle-Moule P, Conklin PL, Niyogi KK (2002) Ascorbate deficiency can limit violaxanthin de-epoxidase activity in vivo. Plant Physiol 128: 970-977
45. Navabpour S, Morris K, Allen R, Harrison E, A-H-Mackerness S, Buchanan-Wollaston V (2003) Expression of senescence-enhanced genes in response to oxidative stress. J Exp Bot 54: 2285-2292
46. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49: 249-279
47. Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J Exp Bot 53: 1283-1304
48. Olmos E, Hellín E (1998) Ultrastructural differences of hyperhydric and normal leaves from regenerated carnation plants. Sci Hortic (Amsterdam) 75: 91-101
49. Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic-Jovanovic S, Verrier PJ, Noctor G, Foyer CH (2003) Leaf vitamin C contents modulate plant defense transcripts and regulate genes controlling development through hormone signaling. Plant Cell 15: 939-951
50. Potters G, De Gara L, Asard H, Horemans N (2002) Ascorbate and glutathione; guardians of the cell cycle, partners in crime? Plant Physiol Biochem 40: 537-548
51. Potters G, Horemans N, Bellone S, Caubergs RJ, Trost P, Guisez Y, Asard H (2004) Dehydroascorbate influences the plant cell cycle through a glutathione-independent reduction mechanism. Plant Physiol 134: 1479-1487
52. Puntarulo S, Cederbaum AI (1988) Comparison of the ability of ferric complexes to catalyze microsomal chemiluminescence, lipid peroxidation, and hydroxyl radical generation. Arch Biochem Biophys 264: 432-491
53. Radzio A, Lorence A, Chevone BI, Nessler CL (2003) L-Gulono-1,4-lactone oxidase expression rescues vitamin C-deficient Arabidopsis (vtc) mutants. Plant Mol Biol 53: 837-844
54. Rodriguez AA, Grunberg KA, Taleisnik EL (2002) Reactive oxygen species in the elongation zone of maize leaves are necessary for leaf extension. Plant Physiol 129: 1627-1632
55. Schon P, Degefa TH, Asaftei S, Meyer W, Walder L (2005) Charge propagation in "ion channel sensors" based on protein-modified electrodes and redox marker ions. J Am Chem Soc 127: 11436-11496
56. Schopfer P, Liszkay A, Bechtold M, Frahry G, Wagner A (2002) Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta 214: 821-828
57. Schopfer P, Plachy C, Frahry G (2001) Release of reactive oxygen intermediates (superoxide radicals, hydrogen peroxide, and hydroxyl radicals) and peroxidase in germinating radish seeds controlled by light, gibberellin, and abscisic acid. Plant Physiol 125: 1591-1602
58. Thomas H, Ougham HJ, Wagstaff C, Stead AD (2003) Defining senescence and death. J Exp Bot 54: 1127-1132
59. Tokuna T, Miyahara K, Tabata K, Esaka M (2005) Generation and properties of ascorbic acid-over-producing transgenic tobacco cells expressing sense ENA for L-galactono-1,4-lactone dehydrogenase. Planta 220: 854-863
60. Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S, Dincher S, Chandler D, Slusarenko A, Ward E, Ryals J (1992) Acquired resistance in Arabidopsis. Plant Cell 4: 645-656
61. 2 accumulation in mesophyll cells leads to induction of glutathione during the hyper-sensitive response in the barley-powdery mildew interaction. Plant Physiol 123: 1289-1300
62. Veljovic-Jovanovic SD, Pignocchi C, Noctor G, Foyer CH (2001) Low ascorbic acid in the vtc-1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system. Plant Physiol 127: 426-435
63. Vernon LP (1960) Spectrophotometric determination of chlorophylls and pheo-phytins in plant extracts. Anal Chem 32: 1144-1150
64. Wagner D, Przybyla D, Op den Camp R, Kim C, Landgraf F, Lee KP, Würsch M, Laloi C, Nater M, Hideg E, et al (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306: 1183-1185
65. Waspi U, Schweizer P, Dudler R (2001) Syringolin reprograms wheat to undergo hypersensitive cell death in a compatible interaction with powdery mildew. Plant Cell 13: 153-161
66. Whalen MC, Innes RW, Bent AE, Staskawicz BJ (1991) Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell 3: 49-59
67. Yao N, Eisfelder BJ, Marvin J, Greenberg JT (2004) The mitochondrion-an organelle commonly involved in programmed cell death in Arabidopsis thaliana. Plant J 40: 596-610