Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana

Plant Journal

Volumn 39, Issue 1, 2004, Pages 45-58

  Vandenabeele, Steven ^a,c   Vanderauwera, Sandy ^a   Vuylsteke, Marnik ^a   Rombauts, Stephane ^a   Langebartels, Christian ^b   Seidlitz, Harald K ^b   Zabeau, Marc ^a   Van Montagu, Marc ^a   Inzé, Dirk ^a   Van Breusegem, Frank ^a  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Arabidopsis thaliana; Catalase deficiency; High light irradiation; Hydrogen peroxide; Microarray

Indexed keywords

CATALYST ACTIVITY; CELL CULTURE; GENES; HYDROGEN PEROXIDE; IRRADIATION; OZONE;

CATALASE-DEFICIENT PLANTS; GENE EXPRESSION;

PLANTS (BOTANY);

ARABIDOPSIS PROTEIN; CAT2 PROTEIN, ARABIDOPSIS; HYDROGEN PEROXIDE; OZONE; PROTEIN;

ARABIDOPSIS; ARTICLE; CELL DEATH; CULTURE MEDIUM; DNA MICROARRAY; ENZYMOLOGY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; LIGHT; METABOLISM; PEROXISOME; PLANT LEAF; RADIATION EXPOSURE; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL DEATH; CULTURE MEDIA; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; HYDROGEN PEROXIDE; LIGHT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OZONE; PEROXISOMES; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; PROTEINS; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA; EUKARYOTA; LETHRINIDAE;

EID: 3142575281     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2004.02105.x     Document Type: Article

References (71)

1. Allen, J.F. and Pfannschmidt, T. (2000) Balancing the two photosystems: photosynthetic electron transfer governs transcription of reaction centre genes in chloroplasts. Philos. Trans. R. Soc. Lond. B, 355, 1351-1359.
2. Bachmair, A., Novatchkova, M., Potuschak, T. and Eisenhaber, F. (2001) Ubiquitylation in plants: a post-genomic look at a post-translational modification. Trends Plant Sci. 6, 463-470.
3. Beers, R.P. and McDowell, J.M. (2001) Regulation and execution of programmed cell death in response to pathogens, stress and developmental cues. Curr. Opin. Plant Biol. 4, 561-567.
4. van der Biezen, E.A. and Jones, J.D.G. (1998) The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr. Biol. 8, R226-R227.
5. Blume, B., Nürnberger, T., Nass, N. and Scheel, D. (2000) Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley. Plant Cell, 12, 1425-1440.
6. 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.
7. 2 in transgenic plants. Proc. Natl. Acad. Sci. USA, 95, 5818-5823.
8. Clare, D.A., Duong, M.N., Darr, D., Archibald, F. and Fridovich, I. (1984) Effects of molecular oxygen on detection of superoxide radical with nitroblue tetrazolium and on activity stains for catalase. Anal. Biochem. 140, 532-537.
9. Clarke, S.F., Guy, P.L., Burritt, D.J. and Jameson, P.E. (2002) Changes in the activities of antioxidant enzymes in response to virus infection and hormone treatment. Physiol. Plant. 114, 157-164.
10. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
11. Corpas, F.J., Barroso, J.B. and del Río, L.A. (2001) Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends Plant Sci. 6, 145-150.
12. Dat, J., Vandenabeele, S., Vranová, E., Van Montagu, M., Inzé, D. and Van Breusegem, F. (2000) Dual action of the active oxygen species during plant stress responses. Cell. Mol. Life Sci. 57, 779-795.
13. Dat, J.F., Pellinen, R., Beeckman, T., Van De Cotte, B., Langebartels, C., Kangasjärvi, J., Inzé, D. and Van Breusegem, F. (2003) Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco. Plant J. 33, 621-632.
14. Day, I.S., Reddy, V.S., Shad Ali, G. and Reddy, A.S.N. (2002) Analysis of EF-hand-containing proteins in Arabidopsis. Genome Biol. 3, 0056.1-0056.24.
15. De Smet, F., Mathys, J., Marchal, K., Thijs, G., De Moor, B. and Moreau, Y. (2002) Adaptive quality-based clustering of gene expression profiles. Bioinformatics, 18, 735-746.
16. De Veylder, L., Beemster, G.T.S., Beeckman, T. and Inzé, D. (2001) CKS1At overexpression in Arabidopsis thaliana inhibits growth by reducing meristem size and inhibiting cell-cycle progression. Plant J. 25, 617-626.
17. Desagher, S. and Martinou, J.-C. (2000) Mitochondria as the central control point of apoptosis. Trends Cell Biol. 10, 369-377.
18. Desikan, R., Mackerness, S.A.-H., Hancock, J.T. and Neill, S.J. (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol. 127, 159-172.
19. Dutilleul, C., Garmier, M., Noctor, G., Mathieu, C., Chétrit, P., Foyer, C.H. and 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.
20. Eisen, M.B., Spellman, P.T., Brown, P.O. and Botstein, D. (1998) Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA, 95, 14863-14868.
21. van Engelen, F.A., Molthoff, J.W., Conner, A.J., Nap, J.-P., Pereira, A. and Stiekema, W.J. (1995) pBINPLUS: an improved plant transformation vector based on pBIN19. Transgenic Res. 4, 288-290.
22. Estelle, M. (2001) Proteases and cellular regulation in plants. Curr. Opin. Plant Biol. 4, 254-260.
23. Fath, A., Bethke, P.C. and Jones, R.L. (2001) Enzymes that scavenge reactive oxygen species are down-regulated prior to gibberellic acid-induced programmed cell death in barley aleurone. Plant Physiol. 126, 156-166.
24. Frugoli, J.A., Zhong, H.H., Nuccio, M.L., McCourt, P., McPeek, M.A., Thomas, T.L. and McClung, C.R. (1996) Catalase is encoded by a multigene family in Arabidopsis thaliana (L.) Heynh. Plant Physiol. 112, 327-336.
25. Heazlewood, J.L., Millar, A.H., Day, D.A. and Whelan, J. (2003) What makes a mitochondrion? Genome Biol. 4, 218.1-218.4.
26. van Helden, J. (2003) Regulatory sequence analysis tools. Nucleic Acids Res. 31, 3593-3596.
27. Hemerly, A., de Almeida Engler, J., Bergounioux, C., Van Montagu, M., Engler, G., Inzé, D. and Ferreira, P. (1995) Dominant negative mutants of the Cdc2 kinase uncouple cell division from iterative plant development. EMBO J. 14, 3925-3936.
28. Hihara, Y., Kamei, A., Kanehisa, M., Kaplan, A. and Ikeuchi, M. (2001) DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell, 13, 793-806.
29. Hrabak, E.M., Dickmann, L.J., Satterlee, J.S. and Sussman, M.R. (1996) Characterization of eight new members of the calmodulin-like domain protein kinase gene family from Arabidopsis thaliana. Plant Mol. Biol. 31, 405-412.
30. 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.
31. Karpinski, S., Gabrys, H., Mateo, A., Karpinska, B. and Mullineaux, P.M. (2003) Light perception in plant disease defence signalling. Curr. Opin. Plant Biol. 6, 390-396.
32. Kaufmann, S.H. and Hengartner, M.O. (2001) Programmed cell death: alive and well in the new millennium. Trends Cell Biol. 11, 526-534.
33. Kendall, A.C., Keys, A.J., Turner, J.C., Lea, P.J. and Miflin, B.J. (1983) The isolation and characterization of a catalase-deficient mutant of barley (Hordeum vulgare). Planta, 159, 505-511.
34. Kimura, M., Yoshizumi, T., Manabe, K., Yamamoto, Y.Y. and Matsui, M. (2001) Arabidopsis transcriptional regulation by light stress via hydrogen peroxide-dependent and -independent pathways. Genes Cells, 6, 697-617.
35. Király, Z., Barna, B., Kecskés, A. and Fodor, J. (2002) Down-regulation of antioxidative capacity in a transgenic tobacco which fails to develop acquired resistance to necrotization caused by TMV. Free Rad. Res. 36, 981-991.
36. Kruft, V., Eubel, H., Jänsch, L., Werhahn, W. and Braun, H.-P. (2001) Proteomic approach to identify novel mitochondrial proteins in Arabidopsis. Plant Physiol. 127, 1694-1710.
37. Leister, D. (2003) Chloroplast research in the genomic age. Trends Genet. 19, 47-56.
38. Lescot, M., Déhais, P., Thijs, G., Marchal, K., Moreau, Y., Van de Peer, Y., Rouzé, P. and Rombauts, S. (2002) PlantCare: a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 30, 325-327.
39. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell, 79, 583-593.
40. Michael, T.P. and McClung, C.R. (2002) Phase-specific circadian clock regulatory elements in Arabidopsis. Plant Physiol. 130, 627-638.
41. Mullen, R.T., Lee, M.S. and Trelease, R.N. (1997) Identification of the peroxisomal targeting signal for cottonseed catalase. Plant J. 12, 313-322.
42. 3 plants: a predominant role for photorespiration? Ann. Bot. 89, 841-850.
43. Novoa, I., Zhang, Y., Zeng, H., Jungreis, R., Harding, H.P. and Ron, D. (2003) Stress-induced gene expression requires programmed recovery from translational repression. EMBO J. 22, 1180-1187.
44. Pastori, G.M. and Foyer, C.H. (2002) Common components, networks, and pathways of cross-tolerance to stress. The central role of 'redox' and abscisic acid-mediated controls. Plant Physiol. 129, 460-468.
45. Pfannschmidt, T. (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci. 8, 33-41.
46. Pfannschmidt, T., Nilsson, A. and Allen, J.F. (1999) Photosynthetic control of chloroplast gene expression. Nature, 397, 625-628.
47. Pignocchi, C., Fletcher, J.M., Wilkinson, J.E., Barnes, J.D. and Foyer, C.H. (2003) The function of ascorbate oxidase in tobacco. Plant Physiol. 132, 1631-1641.
48. Pnueli, 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.
49. Prasad, T.K., Anderson, M.D. and Stewart, C.R. (1994) Acclimation, hydrogen peroxide, and abscisic acid protect mitochondria against irreversible chilling injury in maize seedlings. Plant Physiol. 105, 619-627.
50. Puskás, L.G., Zvara, Á., Hackler, L., Jr and Van Hummelen, P. (2002) RNA amplification results in reproducible microarray data with slight ratio bias. Biotechniques, 32, 1330-1340.
51. Rausell, A., Kanhonou, R., Yenush, L., Serrano, R. and Ros, R. (2003) The translation initiation factor elF1A is an important determinant in the tolerance to NaCl stress in yeast and plants. Plant J. 34, 257-267.
52. Richly, E., Dietzmann, A., Biehl, A., Kurth, J., Laloi, C., Apel, K., Salamini, F. and Leister, D. (2003) Covariations in the nuclear Chloroplast transcriptome reveal a regulatory master-switch. EMBO Rep. 4, 491-498.
53. Riechmann, J.L., Heard, J., Martin, G. et al. (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science, 290, 2105-2110.
54. Rizhsky, L., Liang, H. and Mittler, R. (2002) The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol. 130, 1143-1151.
55. Rojas, E., Llinas, P., Rodríguez-Romero, A., Hernández, C., Linares, M., Zenteno, E. and Lascurain, R. (2001) Hevein, an allergenic lectin from rubber latex, activates human neutrophil's oxidative burst. Glycoconj. J. 18, 339-345.
56. Rombauts, S., Florquin, K., Lescot, M., Marchal, K., Rouzé, P. and Van de Peer, Y. (2003) Computational approaches to identify promoters and cis-regulatory elements in plant genomes. Plant Physiol. 132, 1162-1176.
57. Rossel, J.B., Wilson, I.W. and Pogson, B.J. (2002) Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol. 130, 1109-1120.
58. Schoof, H., Zaccaria, P., Gundlach, H., Lemcke, K., Rudd, S., Kolesov, G., Arnold, R., Mewes, H.W. and Mayer, K.F.X. (2002) MIPS Arabidopsis thaliana database (MAtDB): an integrated biological knowledge resource based on the first complete plant genome. Nucleic Acids Res. 30, 91-93.
59. Sinha, S. and Tompa, M. (2000) A statistical method for finding transcription factor binding sites. In Proceedings of the Eight Intelligent Systems for Molecular Biology (Bourne, P., Gribskov, M., Altman, R., Jensen, N., Hope, D., Lengauer, T., Mitchell, J., Scheeff, E., Smith, C., Strande, S. and Weissig, H., eds). Menlo Park: AAAI Press, pp. 344-354.
60. Smith, I.K., Kendall, A.C., Keys, A.J., Turner, J.C. and Lea, P.J. (1984) Increased levels of glutathione in a catalase-deficient mutant of barley (Hordeum vulgare L.). Plant Sci. Lett. 37, 29-33.
61. Thiel, S., Döhring, T., Köfferlein, M., Kosak, A., Martin, R. and Seidlitz, H.K. (1996) A phytotron for plant stress research: how far can artificial lightning compare with natural sunlight? J. Plant Physiol. 148, 456-463.
62. Thijs, G., Marchal, K., Lescot, M., Rombauts, S., De Moor, B., Rouzé, P. and Moreau, Y. (2002) A Gibbs sampling method to detect overrepresented motifs in the upstream regions of coexpressed genes. J. Comput. Biol. 9, 447-464.
63. Tiwari, B.S., Belenghi, B. and Levine, A. (2002) Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiol. 128, 1271-1281.
64. phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl. Acad. Sci. USA, 99, 517-522.
65. Van Breusegem, F. and Inzé, D. (2002) Transgenic plants expressing tolerance towards oxidative stress. In Plant Biotechnology and Transgenic Plants, Books in Soils, Plants, and the Environment Series, Vol. 92 (Oksman-Caldentey, S. and Barz, W., eds). New York: Marcel Dekker, pp. 497-516.
66. Vandenabeele, S., Van Der Kelen, K., Dat, J. et al. (2003) A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. Proc. Natl. Acad. Sci. USA, 100, 16113-16118.
67. Vranová, E., Atichartpongkul, S., Villarroel, R., Van Montagu, M., Inzé, D. and Van Camp, W. (2002) Comprehensive analysis of gene expression in Nicotiana tabacum leaves acclimated to oxidative stress. Proc. Natl. Acad. Sci. USA, 99, 10870-10875.
68. 3 plants. EMBO J. 16, 4806-4816.
69. Wohlgemuth, H., Mittelstrass, K., Kschieschan, S., Bender, J., Weigel, H.-J., Overmyer, K., Kangasjärvi, J., Sandermann, H. and Langebartels, C. (2002) Activation of an oxidative burst in a general feature of sensitive plants exposed to the air pollutant ozone. Plant Cell Environ. 25, 717-726.
70. Wolfinger, R.D., Gibson, G., Wolfinger, E.D., Bennett, L., Hamadeh, H., Bushel, P., Afshari, C. and Paules, R.S. (2001) Assessing gene significance from cDNA microarray expression data via mixed models. J. Comput. Biol. 8, 625-637.
71. Zhong, H.H. and McClung, C.R. (1996) The circadian clock gates expression of two Arabidopsis catalase genes to distinct and opposite circadian phases. Mol. Gen. Genet. 251, 196-203.