Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in arabidopsis W inside a box sign

Plant Cell

Volumn 16, Issue 9, 2004, Pages 2448-2462

  Ball, Louise ^a   Accotto, Gian Paolo ^b   Bechtold, Ulrike ^c   Creissen, Gary ^a   Funck, Dietmar ^d   Jimenez, Ana ^e   Kular, Baldeep ^a   Leyland, Nicola ^a   Mejia Carranza, Jaime ^a   Reynolds, Helen ^a   Karpinski, Stanislaw ^d   Mullineaux, Philip M ^c  

^a JOHN INNES CENTRE   (United Kingdom)

^b INSTITUTE FOR SUSTAINABLE PLANT PROTECTION   (Italy)

^c UNIVERSITY OF ESSEX   (United Kingdom)

^d STOCKHOLM UNIVERSITY   (Sweden)

^e RESEARCH GROUP ON QUALITY   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; GENES; METABOLISM; MUTAGENESIS; PHOTOOXIDATION; PHYSIOLOGY;

GLUTATHIONE; MUTANTS; SIGNALING PATHWAYS;

PLANTS (BOTANY);

BIOSYNTHESIS; GENES; METABOLISM; PHYSIOLOGY; PLANTS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA; EUKARYOTA;

EID: 4544224632     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.104.022608     Document Type: Article

References (83)

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. Asada, K. (1999). The water-water cycle in chloroplasts: Scavenging of active oxygen species and dissipation of excess photons. Annu. Rev. Plant Physiol. Mol. Biol. 50, 601-639.
3. Ball, L. (2001). Identification of Arabidopsis Mutants with Altered ASCORBATE PEROXIDASE II Gene Expression. PhD dissertation (Norwich, UK: University of East Anglia).
4. Bechtold, U., Murphy, D.J., and Mullineaux, P.M. (2004). Arabidopsis peptide methionine sulfoxide reductase2 prevents cellular oxidative damage in long nights. Plant Cell 16, 908-919.
5. Berger, S., Mitchell-Olds, T., and Stotz, H.U. (2002). Local and differential control of vegetative storage protein expression in response to herbivore damage in Arabidopsis thaliana. Physiol. Plant 114, 85-91.
6. Brüggemann, W., Beyel, V., Brodka, M., Poth, H., Weil, M., and Stockhaus, J. (1999). Antioxidants and antioxidative enzymes in wildtype and transgenic Lycopersicon genotypes of different chilling tolerance. J. Plant Physiol. 140, 145-154.
7. Cameron, R.K., Paiva, N.L., Lamb, C.J., and Dixon, R.A. (1999). Accumulation of salicylic acid and PR-1 gene transcripts in relation to the systemic acquired resistance (SAR) response induced by Pseudomonas syringae pv. tomato in Arabidopsis. Physiol. Mol. Plant Pathol. 55, 121-130.
8. Chang, C.C.-C., Ball, L., Fryer, M.J., Baker, N.R., Karpinski, S., and Mullineaux, P.M. (2004). 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 J. 38, 499-511.
9. 1 protein, ascorbate, glutathione and xanthophyll contents and the electron transport rate in vine leaves. Plant Cell Environ. 18, 1358-1366.
10. Chen, M.-H., Sheng, J., Hind, G., Handa, A.K., and Citovsky, V. (2000). Interaction between tobacco mosaic virus movement protein and host cell pectin methylesterases is required for viral cell-to-cell movement. EMBO J. 19, 913-920.
11. Cobbett, C.S., May, M.J., Howden, R., and Rolls, B. (1998). The glutathione deficient, cadmium-sensitive mutant, cad2-1 of Arabidopsis thaliana is deficient in γ-glutamylcysteine synthetase. Plant J. 16, 73-78.
12. Collinge, M., and Boller, T. (2001). Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytopthora infestans and to wounding. Plant Mol. Biol. 46, 521-529.
13. Conklin, P.L., Williams, E.H., and Last, R.L. (1996). Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant. Proc. Natl. Acad. Sci. USA 93, 9970-9974.
14. Cooper, C.E., Patel, R.P., Brookes, P.S., and Darley-Usmar, V.M. (2002). Nanotransducers in cellular redox signaling: Modification of thiols by reactive oxygen and nitrogen species. Trends Biochem. Sci. 27, 489-492.
15. Creissen, G., Firmin, J., Fryer, M., Kular, B., Leyland, N., Reynolds, H., Pastori, G., Wellburn, F., Baker, N., Wellburn, A., and Mullineaux, P. (1999). Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco plants paradoxically causes increased oxidative stress. Plant Cell 11, 1277-1292.
16. 2 receptor and a redox-transducer in gene activation. Cell 111, 471-481.
17. De Vos, R.H.C., Vonk, M.J., Vooijs, R., and Schat, H. (1992). Glutathione depletion due to copper-induced phytochelatin synthesis causes oxidative stress in Silene cucubalus. Plant Physiol. 98, 853-858.
18. Duval, M., Hsieh, T.-F., Kim, S.Y., and Thomas, T.L. (2002). Molecular characterization of AtNAM: A member of the Arabidopsis NAC domain superfamily. Plant Mol. Biol. 50, 237-248.
19. Frohman, M.A., Dush, M.K., and Martin, G.R. (1988). Rapid production of full-length cDNAs from rare transcripts: Amplification using a single gene specific oligonucleotide primer. Proc. Natl. Acad. Sci. USA 85, 8998-9002.
20. 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.
21. 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.
22. Gallouzi, I.-E., Brennan, C.M., and Steitz, U.A. (2001). Protein ligands mediate the CRM1-dependent export of HuR in response to heat shock. RNA 7, 1348-1361.
23. de A Gerhardt, L.B., Sachetto-Martins, G., Contarini, M.G., Sandroni, M., de P Ferreira, R., de Lima, V.M., Cordeiro, M.C., de Oliveira, D.E., and Margis-Pinheiro, M. (1997). Arabidopsis thaliana class IV chitinase is early induced during the interaction with Xanthomonas campestris. FEBS Lett. 419, 69-75.
24. Grant, J.J., and Loake, G.J. (2000). Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiol. 124, 21-29.
25. Gruber, F., Falkner, F.G., Dorner, F., and Hämmerlee, T. (2001). Quantitation of viral DNA by real-time PCR applying duplex amplification, internal standardization, and two-color fluorescence detection. Appl. Environ. Microbiol. 67, 2837-2839.
26. Han, J., Modha, D., and White, E. (1998). Interaction of E1B 19K with Bax is required to block Bax-induced loss of mitochondrial membrane potential and apoptosis. Oncogene 17, 2993-3005.
27. Hernandez, J.A., Jimenez, A., Mullineaux, P., and Seville, F. (2000). Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defenses. Plant Cell Environ. 23, 853-862.
28. Hirschi, K.D. (1999). Expression of Arabidopsis CAX1 in tobacco: Altered calcium homeostasis and increased stress sensitivity. Plant Cell 11, 2113-2122.
29. Hoeberichts, F.A., and Woltering, E.J. (2003). Multiple mediators of plant programmed cell death: Interplay of conserved cell death mechanisms and plant-specific regulators. Bioessays 25, 47-57.
30. Iliev, E.A., Xu, W., Polisensky, D.H., Oh, M.-H., Torisky, R.S., Clouse, S.D., and Braam, J. (2002). Transcriptional and postranscriptional regulation of Arabidopsis TCH4 expression by diverse stimuli. Roles of cis regions and brassinosteroids. Plant Physiol. 130, 770-783.
31. Irihimovitch, V., and Shapira, M. (2000). Glutathione redox potential modulated by reactive oxygen species regulates translation of Rubisco large subunit in the chloroplast. J. Biol. Chem. 275, 16289-16295.
32. Iturbe-Ormataexe, I., Escuredo, P.R., Arresse-Igor, C., and Becana, M. (1998). Oxidative damage in pea plants exposed to water deficit or paraquat. Plant Physiol. 116, 173-181.
33. Jander, G., Norris, S.R., Rounsley, S.D., Bush, D.F., Levin, I.M., and Last, R.L. (2002). Arabidopsis map-based cloning in the postgenomic era. Plant Physiol. 129, 440-450.
34. Jang, I.-C., Oh, S.-J., Seo, J.-S., Choi, W.-B., Chong, S.-I., Kim, C.-H., Kim, Y.S., Seo, H.-S., Choi, Y.D., Nahm, B.H., and Kim, J.-K. (2003). Expression of a bifunctional fusion of the Escherichia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in transgenic rice plants increases trehalose accumulation and abiotic stress tolerance with stunting growth. Plant Physiol. 131, 516-524.
35. Jimenez, A., Hernandez, J.A., del Rio, J.A., and Seville, F. (1997). Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol. 114, 275-284.
36. Kampfenkel, K., Van Montagu, M., and Inzé, D. (1995). Effects of iron excess on Nicotiana plumbaginifolia plants. Plant Physiol. 107, 725-735.
37. Karpinska, B., Wingsle, G., and Karpinski, S. (2000). Antagonistic effects of hydrogen peroxide and glutathione on acclimation to excess excitation energy in Arabidopsis. IUBMB Life 50, 21-26.
38. Karpinski, S., Escobar, C., Karpinska, B., Creissen, G., and Mullineaux, P.M. (1997). Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9, 627-640.
39. Karpinski, S., Reynolds, H., Karpinska, B., Wingsle, G., Creissen, G., and Mullineaux, P. (1999). Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284, 654-657.
40. Klatt, P., and Lamas, S. (2000). Regulation of protein function by S-glutathiolation in response to oxidative and nitrosative stress. Eur. J. Biochem. 267, 4928-4944.
41. Koumoto, Y., Tsugeki, R., Shimada, T., Mori, H., Kondo, M., HaraNishimura, I., and Nishimura, M. (1996). Isolation and characterization of a cDNA encoding mitochondrial chaperonin 10 from Arabidopsis thaliana by functional complementation of an Escherichia coli groES mutant. Plant J. 10, 1119-1125.
42. Leuder, D.V., and Phillips, M.A. (1996). Characterization of Trypanosoma brucei γ-glutamylcysteine synthetase, an essential enzyme in the biosynthesis of trypanothione (diglutathionylspermidine). J. Biol. Chem. 271, 17485-17490.
43. Lopukhina, A., Dettenberg, M., Weiler, E.W., and Holländer-Czytko, H. (2001). Cloning and characterization of a coronatine-regulated tyrosine aminotransferase from Arabidopsis. Plant Physiol. 126, 1678-1687.
44. Loyall, L., Uchida, K., Braun, S., Furuya, M., and Frohnmeyer, H. (2000). Glutathione and a UV light-induced glutathione-S-transferase are involved in signaling to chalcone synthase in cell cultures. Plant Cell 12, 1939-1950.
45. May, M.J., Hammond-Kosack, K.E., and Jones, J.D.G. (1996). Involvement of reactive oxygen species, glutathione metabolism, and lipid peroxidation in the Cf-gene-dependent defense response of tomato cotyledons induced by race-specific elicitors of Cladosporium fulvum. Plant Physiol. 110, 1367-1379.
46. Meinhard, M., Rodriguez, P.L., and Grill, E. (2002). The sensitivity of ABI2 to hydrogen peroxide links the abscisic acid-response regulator to redox signalling. Planta 214, 775-782.
47. Meyer, A.J., and Fricker, M.D. (2002). Control of demand-driven biosynthesis of glutathione in green Arabidopsis suspension culture cells. Plant Physiol. 130, 1927-1937.
48. Mira, H., Martinez, N., and Peñarrubia, L. (2002). Expression of a vegetative-storage-protein gene from Arabidopsis is regulated by copper, senescence and ozone. Planta 214, 939-946.
49. Mou, Z., Fan, W., and Dong, X. (2003). Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113, 935-944.
50. Murgia, I., Briat, J.F., Tarantino, D., and Soave, C. (2001). Plant ferritin acumulates in response to photoinhibition but its ectopic overexpression does not protect against photoinhibition. Plant Physiol. Biochem. 39, 797-805.
51. Murgia, I., Delledonne, M., and Soave, C. (2002). Nitric oxide mediates iron-induced ferritin accumulation in Arabidopsis. Plant J. 30, 521-528.
52. Muskett, P.R., Kahn, K., Austin, M.J., Moisan, L.J., Sadandom, A., Shirasu, K., Jones, J.D.G., and Parker, J.E. (2002). Arabidopsis RAR1 exerts rate-limiting control of R gene-mediated defenses against multiple pathogens. Plant Cell 14, 979-992.
53. Nikiforova, V., Freitag, J., Kempa, S., Adamik, M., Hesse, H., and Hoefgen, R. (2003). Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: Interlacing of biosynthetic pathways provides response specificity. Plant J. 33, 633-650.
54. Niyogi, K.K., Grossman, A.R., and Björkman, O. (1998). Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10, 1121-1134.
55. Noctor, G., Gornez, L., Vanacker, H., and Foyer, C.H. (2002). Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signaling. J. Exp. Bot. 53, 1283-1304.
56. op den Camp, R.G.L., Przbyla, D., Ochsenbein, C., Laloi, C., Kim, C., Danon, A., Wagner, D., Hideg, E., Göbel, C., Feussner, I., Nater, M., and Apel, K. (2003). Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15, 2320-2332.
57. 2 as an alternative electron sink in photosynthesis. Curr. Opin. Plant Biol. 5, 193-198.
58. Paget, M.S.B., and Buttner, M.J. (2003). Thiol-based regulatory switches. Annu. Rev. Genet. 37, 91-121.
59. Park, Y.-S., Min, H.-J., Ryang, S.-H., Oh, K.-J., Cha, J.-S., Kim, H.Y., and Cho, T.-J. (2003). Characterization of salicylic acid-induced genes in Chinese cabbage. Plant Cell Rep. 21, 1027-1034.
60. Pfannschmidt, T. (2003). Chloroplast redox signals: How photosynthesis controls its own genes. Trends Plant Sci. 8, 33-41.
61. Pneuli, L., Liang, H., Rozenberg, M., and 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.
62. Rauser, W.E., Schupp, R., and Rennenberg, H. (1991). Cysteine, γ-glutamylcysteine, and glutathione levels in maize seedlings: Distribution and translocation in normal and cadmium-exposed plants. Plant Physiol. 97, 128-138.
63. Rawlins, M.R., Leaver, C.J., and May, M.J. (1995). Characterisation of a cDNA encoding Arabidopsis glutathione synthetase. FEBS Lett. 376, 81-86.
64. Rezzonico, E., Flury, N., Meins, F., and Beffa, R. (1998). Transcriptional down-regulation by abscisic acid of pathogenesis-related B-1,3-glucanase genes in tobacco cell cultures. Plant Physiol. 117, 585-592.
65. Rogers, E.E., and Ausubel, F.M. (1997). Arabidopsis enhanced disease susceptibility mutants exhibit enhanced susceptibility to several bacterial pathogens and alterations in PR-1 gene expression. Plant Cell 9, 305-316.
66. Rossel, J.B., Wilson, I.M., and Pogson, B.J. (2002). Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol. 130, 1109-1120.
67. Sandorf, I., and Holländer-Czytko, H. (2002). Jasmonate is involved in the induction of tyrosine aminotransferase and tocopherol biosynthesis in Arabidopsis thaliana. Planta 216, 173-179.
68. Schafer, F.Q., and Buettner, G.R. (2001). Redox environment of the cell as viewed through the redox state of the glutathione disulfide/ glutathione couple. Free Rad. Biol. Med. 30, 1191-1212.
69. Schaller, F. (2001). Enzymes of the biosynthesis of octadecanoid-derived signalling molecules. J. Exp. Bot. 52, 11-23.
70. Söderman, E., Mattsson, J., and Engström, P. (1996). The Arabidopsis homeobox gene ATHB-7 is induced by water deficit and abscisic acid. Plant J. 10, 375-381.
71. Storozhenko, S., Belles-Boix, E., Babiychuk, E., Hérouart, D., Davey, M.W., Slooten, L., Van Montagu, M., Inzé, D., and Kushnir, S. (2002). γ-Glutamyl transpeptidase in transgenic tobacco plants. Cellular localization, processing and biochemical properties. Plant Physiol. 128, 1109-1119.
72. Utsugi, S., Sakamoto, W., Murata, M., and Motoyoshi, F. (1998). Arabidopsis thaliana vegetative storage protein (VSP) genes: Gene organization and tissue-specific expression. Plant Mol. Biol. 38, 565-576.
73. Vernoux, T., Wilson, R.C., Seeley, K.A., Reicheid, J.P., Muroy, S., Brown, S., Maughan, S.C., Cobbett, C.S., Van Montagu, M., Inzé, D., May, M.J., and Sung, Z.R. (2000). The ROOT MERISTEMLESS/ CADMIUM SENSITIVE 2 gene defines a glutathione dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12, 97-110.
74. Walker, M.A., and McKersie, B.D. (1993). Role of the ascorbate- glutathione antioxidant system in chilling resistance in tomato. J. Plant Physiol. 141, 234-239.
75. Welin, B.V., Olson, A., Nylander, M., and Palva, E.T. (1994). Characterization and differential expression of DHN/LEA/RAB-like genes during cold-acclimation and drought stress in Arabidopsis thaliana. Plant Mol. Biol. 26, 131-144.
76. 2 and is indispensable for stress defence in C3 plants. EMBO J. 16, 4806-4816.
77. Wingate, V.M.P., Lawton, M.A., and Lamb, C.J. (1988). Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol. 87, 206-210.
78. Wingler, A. (2002). The function of trehalose biosynthesis in plants. Phytochemistry 60, 437-440.
79. Wingsle, G., and Karpinski, S. (1996). Differential redox regulation of glutathione reductase and Cu/Zn superoxide dismutase gene expression in Pinus sylvestris L. needles. Planta 198, 151-157.
80. Xiang, C., and Oliver, D.J. (1998). Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10, 1539-1550.
81. Xiang, C., Werner, B.L., Christensen, E.M., and Oliver, D.J. (2001). The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiol. 126, 564-574.
82. Zhang, B., Ramonell, K., Somerville, S., and Stacey, G. (2002). Characterization of early, chitin-induced gene expression in Arabidopsis. Mol. Plant-Microbe Interact. 15, 963-970.
83. Zhu, T., and Wang, X. (2000). Large-scale profiling of the Arabidopsis transcriptome. Plant Physiol. 124, 1472-1476.