Ascorbate oxidase-dependent changes in the redox state of the apoplast modulate gene transcript accumulation leading to modified hormone signaling and orchestration of defense processes in tobacco

Plant Physiology

Volumn 141, Issue 2, 2006, Pages 423-435

  Pignocchi, Cristina ^a,c   Kiddle, Guy ^a   Hernández, Iker ^b,d   Foster, Simon J ^a,c   Asensi, Amparo ^b   Taybi, Tahar ^b   Barnes, Jeremy ^b   Foyer, Christine H ^a  

^a ROTHAMSTED RESEARCH   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c JOHN INNES CENTRE   (United Kingdom)

^d UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCOMMUNICATIONS; CELLS; ENZYMES; GENES; GROWTH KINETICS; TOBACCO; VITAMINS;

APOPLAST; ASCORBIC ACID (AA); AUXIN; GLUTATHIONE; SHOOT GROWTH;

GENETIC ENGINEERING;

CELLS; ENZYMES; GENES; GENETIC ENGINEERING; GROWTH; TOBACCO; VITAMINS;

NICOTIANA TABACUM; PSEUDOMONAS SYRINGAE;

EID: 33745652076     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.106.078469     Document Type: Article

References (67)

1. Achard P, Chaeng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phyto hormone signals. Science 322: 91-94
2. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu W-L, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415: 977-983
3. Barbier-Brygoo H, Ephritikhine G, Klämbt D, Ghislain M, Guern J (1989) Functional evidence for an auxin receptor at the plasmalemma of tobacco mesophyll protoplasts. Proc Natl Acad Sci USA 86: 891-895
4. Barnes JD, Zheng Y, Lyons TM (2002) Plant resistance to ozone: the role of ascorbate. In K Omasa, H Saji, S Youssefian, N Kondo, eds, Air Pollution and Plant Biotechnology. Springer-Verlag, Tokyo, pp 235-252
5. Barth C, Moeder W, Klessig DF, Conklin PL (2004) The timing of senescence and response to pathogens is altered in the ascorbate-deficient mutant vitamin C-1. Plant Physiol 134: 178-192
6. Chen Z, Gallie DR (2004) The ascorbic acid redox state controls guard cell signalling and stomatal movement. Plant Cell 16: 1143-1162
7. Chen Z, Silva H, Klessig DF (1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262: 1883-1886
8. Chinoy NJ (1984) Ascorbic acid in plant growth and development. In W Junk, ed, The Role of Ascorbic Acid in Growth, Differentiation and Metabolism of Plants. Martinus Nijhoff, The Hague, The Netherlands, pp 68-195
9. De Long A, Mockaitis K, Christensen S (2002) Protein phosphorylation in the delivery of and response to auxin signals. Plant Mol Biol 49: 285-303
10. Desikan R, Hancock JT, Ichimura K, Shinozaki K, Neill SJ (2001) Harpin induces activation of the Arabidopsis mitogen-activated protein kinases AtMPK4 and AtMPK6. Plant Physiol 126: 1579-1587
11. De Smet I, Signora L, Beeckman T, Inzé D, Foyer CH, Zhang H (2003) An ABA-sensitive lateral root developmental checkpoint in Arabidopsis. Plant J 33: 543-555
12. De Souza IRP, MacAdam JW (2001) Gibberellic acid and dwarfism effects on the growth dynamics of B73 maize (Zea mays L.) leaf blades: a transient increase in apoplastic peroxidase activity precedes cessation of cell elongation. J Exp Bot 52: 1673-16S2
13. Dutilleul C, Garmier M, Mathieu C, Chetrit P, Noctor G, Foyer CH, De Paepe R (2003) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 15: 1212-1226
14. Esaka M, Fujisawa K, Goto M, Kisu Y (1992) Regulation of ascorbate oxidase expression in pumpkin by auxin and copper. Plant Physiol 100: 231-237
15. Fath A, Bethke P, Beligni V, Jones R (2002) Active oxygen and cell death in cereal aleurone cells. J Exp Bot 53: 1273-1282
16. Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG, et al (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422: 442-446
17. Foyer CH, Noctor G (2000) Tansley Review No 112. Oxygen processing in photosynthesis: regulation and signalling. New Phytol 146: 359-388
18. Foyer CH, Noctor G (2005a) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17: 1866-1875
19. 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
20. Green MA, Fry SC (2005) Vitamin C degradation in plant cells via enzymatic hydrolysis of 4-O-oxalyl-L-threonate. Nature 433: 83-87
21. Gupta R, Luan S (2003) Redox control of protein tyrosine phosphatases and mitogen-activated protein kinases in plants. Plant Physiol 132: 1149-1152
22. Horemans N, Foyer CH, Asard H (2000) Transport and action of ascorbate at the plant plasma membrane. Trends Plant Sci 5: 263-267
23. Joo JH, Bae YS, Lee JS (2001) Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol 126: 1055-1060
24. Joo JH, Wang S, Chen JG, Jones AM, Fedoroff NV (2005) Different signaling 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
25. 2+ permeable channels NtTPC1A/B in tobacco BY-2 cells. Biochem Biophys Res Commun 336: 1259-1267
26. Kato N, Esaka M (2000) Expansion of transgenic tobacco protoplasts expressing pumpkin ascorbate oxidase is more rapid that that of wild type protoplasts. Planta 210: 1018-1022
27. Kerk NM, Jiang K, Feldman LJ (2000) Auxin metabolism in the root apical meristem. Plant Physiol 122: 925-932
28. Kisu Y, Harada Y, Goto M, Esaka M (1997) Cloning of the pumpkin ascorbate oxidase gene and analysis of a cis-acting region involved in induction by auxin. Plant Cell Physiol 38: 631-637
29. Knight H, Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6: 262-267
30. 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 14: 2940-2945
31. Kovtun Y, Chiu WL, Zeng W, Sheen J (1998) Suppression of auxin signal transduction by a MAPK cascade in higher plants. Nature 395: 716-720
32. Kyriakis JM, Avruch J (1996) Sounding the alarm: protein kinase cascades activated by stress and inflammation. J Biol Chem 271: 24313-24316
33. Löbler M, Klämbt D (1985) Auxin-binding protein from coleoptile membranes of corn (Zea mays L.). J Biol Chem 260: 9854-9859
34. 2 accumulation, catalase (CAT) activity and CAT gene expression in wheat. J Exp Bot 56: 417-423
35. Menke FL, van Pelt JA, Pieterse CM, Klessing DF (2004) Silencing of the mitogen-activated protein kinase MPK6 compromises disease resistance in Arabidopsis. Plant Cell 16: 897-907
36. Métraux JP (1987) Gibberellins and plant cell elongation. In PJ Davies, ed, Plant Hormones and Their Role in Plant Growth and Development. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 296-317
37. Mockaitis K, Howell SH (2000) Auxin induces mitogenic activated protein kinase (MAPK) activation in roots of Arabidopsis seedlings. Plant J 24: 785-796
38. 2 function by independent pathways in the induction of freezing tolerance in potato. Physiol Plant 125: 430-440
39. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22: 867-880
40. Nanasato Y, Akashi K, Yokota A (2005) Co-expression of cytochrome b561 and ascorbate oxidase in leaves of wild watermelon under drought and high light conditions. Plant Cell Physiol 46: 1515-1524
41. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49: 249-279
42. Noctor G, Veljovic-Jovanovic SD, Driscoll S, Novitskaya L, Foyer CH (2002) Drought and oxidative load in wheat leaves: a predominant role for photorespiration? Ann Bot (Lond) 89: 841-850
43. Östin A, Kowalycz M, Bhalerao RP, Sandberg G (1998) Metabolism of indole-3-acetic acid in Arabidopsis. Plant Physiol 118: 285-296
44. 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 that control development through hormone signaling. Plant Cell 15: 939-951
45. Pavet V, Olmos E, Kiddle G, Mowla S, Kumar S, Antoniw J, Alvarez ME, Foyer CH (2005) Ascorbic acid deficiency activates cell death and disease resistance responses in Arabidopsis thaliana. Plant Physiol 139: 1291-1303
46. Payne RW, Lane PW, Digby PGN, Harding SA, Leech PK, Morgan GW, Todd AD, Thompson R, Tunnicliffe WG, Welham SJ, et al (1993) Genstat 5, Release 3, Reference Manual. Clarendon Press, Oxford
47. Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406: 731-734
48. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: 2002-2007
49. Pignocchi C, Fletcher JM, Wilkinson JE, Barnes JD, Foyer CH (2003) The function of ascorbate oxidase in tobacco. Plant Physiol 132: 1631-1641
50. Pignocchi C, Foyer CH (2003) Apoplastic ascorbate metabolism and its role in the regulation of cell signalling. Curr Opin Plant Biol 6: 379-389
51. Polidoros AN, Scandalios JG (1998) Circadian expression of the maize catalase cat3 gene is highly conserved among diverse maize genotypes with structurally different promoters: Genetics 149: 405-415
52. Preger V, Scagliarini S, Pupillo P, Trost P (2005) Identification of an ascorbate-dependent cytochrome b of the tonoplast membrane sharing biochemical features with members of the cytochrome b561 family. Planta 220: 365-375
53. Rentel MC, Lecourieux D, Quaked F, Usher SL, Petersen L, Okamoto H, Knight H, Peck SC, Grierson CS, Hirt H, et al (2004) OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427: 858-861
54. Sanmartin M, Drogoudi PD, Lyons T, Pateraki I, Barnes J, Kanellis AK (2003) Over-expression of ascorbate oxidase in the apoplast of transgenic tobacco results in altered ascorbate and glutathione redox states and increased sensitivity to ozone. Planta 216: 918-928
55. Schopfer P, Liszkay A, Bechtold M, Frahry G, Wagner A (2002) Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta 214: 821-828
56. 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
57. Signora L, De Smet I, Foyer CH, Zhang H (2001) ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis. Plant J 28: 655-662
58. Smirnoff N (2000) Ascorbic acid: metabolism and functions of a multi-faceted molecule. Curr Opin Plant Biol 3: 229-235
59. Steffens B, Wang J, Sauter B (2005) Interactions between ethylene, gibberellin and abscisic acid regulate emergence and growth rate of adventitious roots in deepwater rice. Planta 14: 1-9
60. Sun TP, Gubler F (2004) Molecular mechanisms of gibberellin signalling in plants. Annu Rev Plant Biol 55: 197-223
61. Takahama U (1994) Changes induced by abscisic acid and light in the redox state of ascorbate in the apoplast of epicotyls of Vigna angularis. Plant Cell Physiol 35: 975-978
62. Takahama U (1998) Ascorbic acid-dependent regulation of redox levels of chlorogenic acid and its isomers in the apoplast of leaves of Nicotiana tabacum L. Plant Cell Physiol 39: 681-689
63. Takahama U, Oniki T (1994) The association of ascorbate and ascorbate oxidase in the apoplast with IAA-enhanced elongation of epicotyls from Vigna angularis. Plant Cell Physiol 35: 257-266
64. Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8: 397-403
65. Yamamizo C, Kuchimura K, Kobayashi A, Katou S, Kawakita K, Jones JDG, Doke N, Yoshioka H (2006) Rewiring mitogen-activated protein kinase cascade by positive feedback confers potato blight resistance. Plant Physiol 140: 681-692
66. Yamamoto A, Bhuiyan NH, Waditee R, Tanaka Y, Esaka M, Oba K, Jagendorf AT, Takabe T (2005) Suppressed expression of the apoplastic ascorbate oxidase gene increases salt tolerance in tobacco and Arabidopsis plants. J Exp Bot 56: 1785-1796
67. Zhong HH, Young JC, Pease EA, Hangarter RP, McClung CR (1994) Interactions between light and the circadian clock in the regulation of CAT2 expression in Arabidopsis. Plant Physiol 104: 889-898