Induction of Ascorbate Peroxidase 2 expression in wounded Arabidopsis leaves does not involve known wound-signalling pathways but is associated with changes in photosynthesis

Plant Journal

Volumn 38, Issue 3, 2004, Pages 499-511

  Chang, Christine Chi Chen ^a   Ball, Louise ^b   Fryer, Michael J ^c   Baker, Neil R ^c   Karpinski, Stanislaw ^a   Mullineaux, Philip M ^b,c  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b JOHN INNES CENTRE   (United Kingdom)

^c UNIVERSITY OF ESSEX   (United Kingdom)

Author keywords

Ascorbate Peroxidase2; Chitosan; Jasmonic acid; Photosynthesis; Reactive oxygen species; Wounding

Indexed keywords

ANTIOXIDANTS; ELECTRON TRANSPORT PROPERTIES; GENES; GENETIC ENGINEERING; HYDROGEN PEROXIDE; PHOTOSYNTHESIS; SIGNALING; STRESS ANALYSIS;

PLANT LEAVES; WOUNDED LEAVES;

PLANTS (BOTANY);

ARABIDOPSIS PROTEIN; ASCORBATE PEROXIDASE, ARABIDOPSIS; HYDROGEN PEROXIDE; ISOENZYME; PEROXIDASE;

ARABIDOPSIS; ARTICLE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; LIGHT; MECHANICAL STRESS; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT EPIDERMIS; PLANT LEAF; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; HYDROGEN PEROXIDE; ISOENZYMES; LIGHT; PEROXIDASES; PHOTOSYNTHESIS; PLANT EPIDERMIS; PLANT LEAVES; SIGNAL TRANSDUCTION; STRESS, MECHANICAL;

ARABIDOPSIS; EMBRYOPHYTA; EUKARYOTA;

EID: 2342584757     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2004.02066.x     Document Type: Article

References (61)

1. Allan, A.C. and Fluhr, R. (1997) Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. Plant Cell, 9, 1559-1572.
2. Alvarez, M.E., Pennell, R.I., Meijer, P.-J., Ishikawa, A., Dixon, R.A. and Lamb, C. (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell, 92, 773-784.
3. 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, 601-639.
4. Baker, N.R., Oxborough, K., Lawson, T. and Morison, J.I.L. (2001) High resolution imaging of photosynthetic activities of tissues, cells and chloroplasts in leaves. J. Exp. Bot. 52, 615-621.
5. Barbagallo, R.P., Oxborough, K., Pallett, K.E. and Baker, N.R. (2003) Rapid, noninvasive screening for perturbations of metabolism and plant growth using chlorophyll fluorescence imaging. Plant Physiol. 132, 485-493.
6. Bleecker, A.B., Estelle, M.A. and Somerville, C. (1988) Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science, 241, 1086-1089.
7. Bolwell, G.P., Blee, K.A., Butt, V.S., Davies, D.R., Gardner, S.L., Gerrish, C., Minibayeva, F., Rowntree, E.G. and Wojtaszek, P. (1999) Recent advances in understanding the origin of the apoplastic oxidative burst in plant cells. Free Radic. Res. 31, S137-S145.
8. Bolwell, G.P., Bindschedler, L.V., Blee, K.A., Butt, V.S., Davies, D.R., Gardner, S.L., Gerrish, C. and Minibayeva, F. (2002) The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. J. Exp. Bot. 53, 1367-1376.
9. Bowler, C. and Fluhr, R. (2000) The role of calcium and activated oxygen as signals for controlling cross-tolerance. Trends Plant Sci. 5, 241-246.
10. Bowles, D. (1998) Signal transduction in the wound response of tomato plants. Philos. Trans. R. Soc. Lond. B, 353, 1495-1510.
11. Cross, A.R. and Jones, O.T.G. (1986) The effect of the inhibitor diphenylene iodonium on the superoxide-generating system of neutrophils. Biochem. J. 237, 111-116.
12. 2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol. 116, 1351-1357.
13. Delledonne, M., Xia, Y., Dixon, R.A. and Lamb, C. (1998) Nitric oxide functions as a signal in plant disease resistance. Nature, 394, 585-588.
14. Ellis, C. and Turner, J.G. (2002) A conditionally fertile coi1 allele indicates cross-talk between plant hormone signalling pathways in Arabidopsis thaliana seeds and young seedlings. Planta, 215, 549-556.
15. Ellis, J.A., Cross, A.R. and Jones, O.T.G. (1989) Studies on the electron-transfer mechanism of the human neutrophil NADPH oxidase. Biochem. J. 262, 575-579.
16. Feys, B., Benedetti, C.E., Penfold, C.N. and Turner, J.G. (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell, 6, 751-759.
17. Fryer, M.J., Oxborough, K., Mullineaux, P.M. and Baker, N.R. (2002) Imaging photo-oxidative stress responses in leaves. J. Exp. Bot. 53, 1249-1254.
18. Fryer, M.J., Ball, L., Oxborough, K., Karpinski, S., Mullineaux, P.M. and Baker, N.R. (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.
19. Guzman, P. and Ecker, J.R. (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell, 2, 513-523.
20. Hadwiger, L.A. and Beckman, J.M. (1980) Chitosan as a component of pea-Fusarium solani interactions. Plant Physiol. 66, 205-211.
21. Innis, M.A., Gelfand, D.H., Sninsky, J.J. and White, T.J. (1990) PCR Protocols: a Guide to Methods and Applications. San Diego, USA: Academic Press.
22. Karpinski, S., Escobar, C., Karpinska, B., Creissen, G. and Mullineaux, P. (1997) Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell, 9, 627-640.
23. Karpinski, S., Reynolds, H., Karpinska, B., Wingsle, G., Creissen, G. and Mullineaux, P. (1999) Systemic signalling and acclimation in response to excess excitation energy in Arabidopsis. Science, 284, 654-657.
24. 2+ binding motifs. Plant Cell, 10, 255-266.
25. Koornneef, M., Reuling, G. and Karssen, C.M. (1984) The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiol. Plant. 61, 377-383.
26. Kovtun, Y., Chiu, W.-L., Tena, G. and Sheen, J. (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc. Natl. Acad. Sci. USA, 97, 2940-2945.
27. Leon, J., Rojo, E. and Sanchez-Serrano, J.J. (2001) Wound signalling in plants. J. Exp. Bot. 52, 1-9.
28. Leung, J., Bouvier-Durand, M., Morris, P.-C., Guerrier, D., Chefdor, F. and Giraudat, J. (1994) Arabidopsis ABA. response gene ABI1: features of a calcium-modulated protein phosphatase. Science, 264, 1448-1452.
29. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell, 79, 583-593.
30. Long, S.P., Humphries, S. and Falkowski, P.G. (1994) Photoinhibition of photosynthesis in nature. Annu. Rev. Plant Physiol. Plant. Mol. Biol. 45, 633-661.
31. Malone, M. (1992) Kinetics of wound-induced hydraulic signals and variation potentials in wheat seedlings. Planta, 187, 505-510.
32. Malone, M. and Alarcon, J.J. (1995) Only xylem-borne factors can account for systemic wound signalling in the tomato plant. Planta, 196, 740-746.
33. McConn, M., Creelman, R.A., Bell, E., Mullet, J.E. and Browse, J. (1997) Jasmonate is essential for insect defense in Arabidopsis. Proc. Natl. Acad. Sci. USA, 94, 5473-5477.
34. Meyer, K., Leube, M.P. and Grill, E. (1994) A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science, 264, 1452-1455.
35. Moulton, P., Martin, H., Ainger, A., Cross, A., Hoare, C., Doel, J., Harrison, R., Eisenthal, R. and Hancock, J. (2000) The inhibition of flavoproteins by phenoxaiodonium, a new iodonium analogue. Eur. J. Pharmacol. 401, 115-120.
36. Mullineaux, P. and Karpinski, S. (2002) Signal transduction in response to excess light: getting out of the chloroplast. Curr. Opin. Plant Biol. 5, 43-48.
37. Mullineaux, P., Ball, L., Escobar, C., Karpinska, B., Creissen, G. and Karpinski, S. (2000) Are diverse signalling pathways integrated in the regulation of Arabidopsis antioxidant defence gene expression in response to excess excitation energy? Philos. Trans. R. Soc. Lond. B, 355, 1531-1540.
38. 2+ channels in guard cells requires cytosolic NAD(p)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell, 13, 2513-2523.
39. Nishiuchi, T., Hamada, T., Kodama, H. and Iba, K. (1997) Wounding changes the spatial expression pattern of the Arabidopsis plastid ω-3 fatty acid desaturase gene (FAD7) through different signal transduction signal transduction pathways. Plant Cell, 9, 1701-1712.
40. O'Donnell, V.B., Tew, D.G., Jones, O.T.G. and England, P.J. (1993) Studies on the inhibitory mechanism of iodonium compounds with special reference to neutrophil NADPH oxidase. Biochem. J. 290, 41-49.
41. Orozco-Cárdenas, M.L. and Ryan, C. (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc. Natl. Acad. Sci. USA, 96, 6553-6557.
42. Orozco-Cárdenas, M.L. and Ryan, C. (2002) Nitric oxide negatively modulates wound signaling in tomato plants. Plant Physiol. 130, 487-493.
43. Orozoco-Cárdenas, M., Narvaez-Vȧsquez, J. and Ryan, C.A. (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.
44. 2 as an alternative electron sink in photosynthesis. Curr. Opin. Plant Biol. 5, 193-198.
45. Panchuk, I.I., Volkov, R.A. and Schöffl, F. (2002) Heat stress- and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol. 129, 838-853.
46. Pei, Z.M., Murata, Y., Benning, G., Thomine, S., Klüsener, B., Allen, G.J., Grill, E. and Schroeder, J. (2000) Ion channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature, 406, 731-734.
47. Pellinen, R., Palva, T. and Kangasjärvi, J. (1999) Subcellular localization of ozone-induced hydrogen peroxide production in birch (Betula pendula) leaf cells. Plant J. 20, 349-356.
48. Peña-Cortės, H., Liu, X., Sanchez-Serrano, J., Schmid, R. and Willmitzer, L. (1992) Factors affecting gene expression of patatin and proteinase-inhibitor-II gene families in detached potato leaves. Planta, 186, 495-502.
49. Peña-Cortės, H., Fisahn, J. and Willmitzer, L. (1995) Signals involved in wound-induced proteinase inhibitor II gene expression in tomato and potato plants. Proc. Natl. Acad. Sci. USA, 92, 4106-4113.
50. Rojo, E., Titarenko, E., Leon, J., Berger, S., Vancanneyt, G. and Sȧnchez-Serrano, J.J. (1998) Reversible protein phosphorylation regulates jasmonic acid-dependent and -independent wound signal transduction pathways in Arabidopsis thaliana. Plant J. 13, 153-165.
51. Rojo, E., León, J. and Sánchez-Serrano, J.J. (1999) Cross-talk between wound-signalling pathways determines local versus systemic gene expression in Arabidopsis thaliana. Plant J. 20, 135-142.
52. Sadka, A., DeWald, D.B., May, G.D., Park, W.D. and Mullet, J.E. (1994) Phosphate modulates transcription of soybean VspB and other sugar-inducible genes. Plant Cell, 6, 737-749.
53. Santos, M., Gousseau, H., Lister, C., Foyer, C., Creissen, G. and Mullineaux, P.M. (1996) Cytosolic ascorbate peroxidase from Arabidopsis thaliana L. is encoded by a small multigene family. Planta, 198, 64-69.
54. Staswick, P.E., Su, W. and Howell, S.H. (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc. Natl. Acad. Sci. USA, 89, 6837-6840.
55. Tenhaken, R., Levine, A., Brisson, L.F., Dixon, R.A. and Lamb, C. (1995) Function of the oxidative burst in hypersensitive disease resistance. Proc. Natl. Acad. Sci. USA, 92, 4158-4163.
56. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11, 1187-1194.
57. Titarenko, E., Rojo, E., Leȯn, J. and Sȧnchez-Serrano, J.J. (1997) Jasmonic acid-dependent and -independent signaling pathways control wound-induced gene activation in Arabidopsis thaliana. Plant Physiol. 115, 817-826.
58. phox). Plant J. 14, 365-370.
59. Watanabe, T. and Sakai, S. (1998) Effects of active oxygen species and methyl jasmonate on expression of the gene for a wound-inducible 1-aminocyclopropane-1-carboxylate synthase in winter squash (Cucurbita maxima). Planta, 206, 570-576.
60. 3 plants. EMBO J. 16, 4806-4816.
61. Zhang, X., Zhang, L., Dong, F., Gao, J., Galbraith, D.W. and Song, C.-P. (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol. 126, 1438-1448.