Post-transcriptional mechanisms control catalase synthesis during its light-induced turnover in rye leaves through the availability of the hemin cofactor and reversible changes of the translation efficiency of mRNA

Plant Journal

Volumn 31, Issue 5, 2002, Pages 601-613

  Schmidt, Matthias ^a   Dehne, Silvia ^a   Feierabend, Jürgen ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

Catalase turnover; Heme; Methylation; mRNA association; Photoinactivation; Polysomes; Translational regulation

Indexed keywords

CLONING; DEGRADATION; DNA; ENZYMES; EXTRACTION; POLYPEPTIDES; RNA; SYNTHESIS (CHEMICAL);

PHOTOINACTIVATION;

PLANTS (BOTANY);

CATALASE; DARKNESS; DEOXYADENOSINES; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; HEMIN; LIGHT; METHYLATION; PEROXIDASE; PLANT LEAVES; POLYRIBOSOMES; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; SECALE CEREALE; SIGNAL TRANSDUCTION;

EMBRYOPHYTA; FELIS CATUS; SECALE CEREALE;

EID: 0036733158     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2002.01382.x     Document Type: Article

References (69)

1. Acevedo, A., Williamson, J.D. and Scandalios, J.G. (1991) Photoregulation of the Cat2 and Cat3 catalase genes in pigmented and pigment-deficient maize: The circadian regulation of Cat3 is superimposed on its quasi-constitutive expression in maize leaves. Genetics, 127, 601-607.
2. Acevedo, A., Skadsen, R.W. and Scandalios, J.G. (1996) Two barley catalase genes respond differentially to light. Physiol. Plant. 96, 369-374.
3. Aro, E.M., Virgin, I. and Andersson, B. (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim. Biophys. Acta, 1143, 113-134.
4. Bailey-Serres, J. (1999) Selective translation of cytoplasmic mRNAs in plants. Trends Plant Sci. 4, 142-148.
5. Barak, S., Nejidat, A., Heimer, Y. and Volokita, M. (2001) Transcriptional and posttranscriptional regulation of the glycolate oxidase gene in tobacco seedlings. Plant Mol. Biol. 45, 399-407.
6. Berberich, T., Sugawara, K., Harada, M. and Kusano, T. (1995) Molecular cloning, characterization and expression of an elongation factor 1α gene in maize. Plant Mol. Biol. 29, 611-615.
7. Berry, J.O., Nikolau, B.J., Carr, J.P. and Klessig, D.F. (1986) Translational regulation of light-induced ribulose 1,5-bisphosphate carboxylase gene expression in amaranth. Mol. Cell. Biol. 6, 2347-2353.
8. Berry, J.O., Carr, J.P. and Klessig, D.F. (1988) mRNAs encoding ribulose-1,5-bisphosphate carboxylase remain bound to polysomes but are not translated in amaranth seedlings transferred to darkness. Proc. Natl Acad. Sci. USA, 85, 4190-4194.
9. Biekmann, S. and Feierabend, J. (1982) Subcellular distribution, multiple forms and development of glutamate--pyruvate (glyoxylate) aminotransferase in plant tissues. Biochim. Biophys. Acta, 721, 268-279.
10. Chamberlain, J.P. (1979) Fluorographic detection of radioactivity in polyacrylamide gels with the water-soluble fluor, sodium salicylate. Anal Biochem. 98, 132-135.
11. Cohen, A. and Mayfield, S.P. (1997) Translational regulation of gene expression in plants. Curr. Opin. Biotechnol. 8, 189-194.
12. Davies, E., Larkins, B.A. and Knight, R.H. (1972) Polyribosomes from peas. An improved method for their isolation in the absence of ribonuclease inhibitors. Plant Physiol. 50, 581-584.
13. De Boer, J. and Feierabend, J. (1978) Comparative analysis of the action of cytokinin and light on the growth of rye leaves. Planta, 142, 67-73.
14. Drumm, H. and Schopfer, P. (1974) Effect of phytochrome on development of catalase activity and isoenzyme pattern in mustard (Sinapis alba L.) seedlings. A reinvestigation. Planta, 120, 13-30.
15. Eichacker, L.A., Soll, J., Lauterbach, P., Rüdiger, W., Klein, R.R. and Mullet, J.E. (1990) In vitro synthesis of chlorophyll A in the dark triggers accumulation of chlorophyll A apoproteins in barley etioplasts. J. Biol. Chem. 265, 13566-13571.
16. Feierabend, J. (1975) Developmental studies on microbodies in wheat leaves. III. On the photocontrol of microbody development. Planta, 123, 63-77.
17. Feierabend, J. and Beevers, H. (1972) Developmental studies on microbodies in wheat leaves. I. Conditions influencing enzyme development. Plant Physiol. 49, 28-32.
18. Feierabend, J. and Dehne, S. (1996) Fate of the porphyrin cofactors during the light-dependent turnover of catalase and of the photosystem II reaction-center protein D1 in mature rye leaves. Planta, 198, 413-422.
19. Feierabend, J., Meschede, D. and Vogel, K.-D. (1980) Comparison of the polypeptide compositions of the internal membranes of chloroplasts, etioplasts and ribosome-deficient heat-bleached plastids from rye leaves. Z. Pflanzenphysiol. 98, 61-78.
20. Feierabend, J., Schaan, C. and Hertwig, B. (1992) Photoinactivation of catalase occurs under both high- and low-temperature stress conditions and accompanies photoinhibition of photosystem II. Plant Physiol. 100, 1554-1561.
21. Feierabend, J. and Wildner, G. (1978) Formation of the small subunit in the absence of the large subunit of ribulose 1,5-bisphosphate carboxylase in 70s ribosome-deficient rye leaves. Arch. Biochem. Biophys. 186, 283-291.
22. Feinberg, A.P. and Vogelstein, B. (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132, 6-13.
23. Ferreira, R.B. and Davies, D.D. (1987) Protein degradation in Lemna with particular reference to ribulose bisphosphate carboxylase. I. The effect of light and dark. Plant Physiol. 83, 869-877.
24. Flynn, C.R., Mullen, R.T. and Trelease, R.N. (1998) Mutational analyses of a type 2 peroxisomal targeting signal that is capable of directing oligomeric protein import into tobacco BY-2 glyoxysomes. Plant J. 16, 709-720.
25. Fromm, H., Devic, M., Fluhr, R. and Edelman, M. (1985) Control of psbA gene expression: in mature Spirodela chloroplasts light regulation of 32-kd protein synthesis is independent of transcript level. EMBO J. 4, 291-295.
26. Frugoli, J.A., McPeek, M.A., Thomas, T.L. and McClung, C.R. (1998) Intron loss and gain during evolution of the catalase gene family in angiosperms. Genetics, 149, 355-365.
27. Gallie, D. (1993) Posttranslational regulation of gene expression in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44, 77-105.
28. Ganal, M. and Hemleben, V. (1986) Comparison of the ribosomal RNA genes in four closely related Cucurbitaceae. Plant Syst. Evol. 154, 63-77.
29. Gillian-Daniel, D.L., Gray, N.K., Åström, J., Barkoff, A. and Wickens, M. (1998) Modifications of the 5′-cap of mRNAs during Xenopus oocyte maturation: independence from changes in poly (A) length and impact on translation. Mol. Cell Biol. 18, 6152-6163.
30. Guan, L. and Scandalios, J.G. (1996) Molecular evolution of maize catalases and their relationship to other eukaryotic and prokaryotic catalases. J. Mol. Evol. 42, 570-579.
31. Hamilton, B., Hofbauer, R. and Ruis, H. (1982) Translational control of catalase synthesis by hemin in the yeast Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA, 79, 7609-7613.
32. Hansen, E.R., Petracek, M.E., Dickey, L.F. and Thompson, W.F. (2001) The 5′ end of the pea ferredoxin-1 mRNA mediates rapid and reversible light-directed changes in translation in tobacco. Plant Physiol. 125, 770-778.
33. Hanson, A.D. and Roje, S. (2001) One-carbon metabolism in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 119-137.
34. Hertwig, B., Streb, P. and Feierabend, J. (1992) Light dependence of catalase synthesis and degradation in leaves and the influence of interfering stress conditions. Plant Physiol. 100, 1547-1553.
35. Huang, A.H.C., Trelease, R.N. and Moore, T.S. (1983) Plant Peroxisomes, Academic Press, New York.
36. Jackson, A.O. and Larkins, B.A. (1976) Influence of ionic strength, pH, and chelation of divalent metals on isolation of polyribosomes from tobacco leaves. Plant Physiol. 57, 5-10.
37. Kim, J. and Mayfield, S.P. (1997) Protein disulfide isomerase as a regulator of chloroplast: translational activation. Science, 278, 1954-1957.
38. Kim, J., Klein, P.G. and Mullet, J.E. (1994) Synthesis and turnover of photosystem II reaction center protein D1. J. Biol. Chem. 269, 17918-17923.
39. Klausner, R.D., Rouault, T.A. and Harford, J.B. (1993) Regulating the fate of mRNA: The control of cellular iron metabolism. Cell, 72, 19-28.
40. Klein, R.R., Mason, H.S. and Mullet, J.E. (1988) Light-regulated translation of chloroplast proteins. I. Transcripts of PsaA-PsaB, PsbA, and RbcL are associated with polysomes in dark-grown and illuminated barley seedlings. J. Cell Biol. 106, 289-301.
41. Komar, A.A., Kommer, A., Krasheninnikov, I.A. and Spirin, A.S. (1993) Cotranslational heme binding to nascent globin chains. FEBS Lett. 326, 261-263.
42. Kuge, H., Brownlee, G.G., Gershon, P.D. and Richter, J.D. (1998) Cap ribose methylation of c-mos mRNA stimulates translation and oocyte maturation in Xenopus laevis. Nucl. Acids Res. 26, 3208-3214.
43. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
44. Logemann, J., Schell, J. and Willmitzer, L. (1987) Improved method for the isolation of RNA from plant tissues. Anal. Biochem. 163, 16-20.
45. McClung, C.R. (1997) Regulation of catalases in Arabidopsis. Free Rad. Biol. Med. 23, 489-496.
46. McNew, J.A. and Goodman, J.M. (1996) The targeting and assembly of peroxisomal proteins: some old rules do not apply. Trends Biol. Sci. 21, 54-58.
47. Mishra, N.P., Mishra, R.K. and Singhal, G.S. (1993) Changes in the activities of anti-oxidant enzymes during exposure of intact wheat leaves to strong visible light at different temperatures in the presence of protein synthesis inhibitors. Plant Physiol. 102, 903-910.
48. Mittler, R., Feng, X. and Cohen, M. (1998) Posttranscriptional suppression of cytosolic ascorbate peroxidase expression during pathogen-induced programmed cell death in tobacco. Plant Cell, 10, 461-473.
49. Mullet, J.E., Klein, P.G. and Klein, R.R. (1990) Chlorophyll regulates accumulation of the plastid-encoded chlorophyll apoproteins CP43 and D1 by increasing apoprotein stability. Proc. Natl Acad. Sci. USA, 87, 4038-4042.
50. Nagy, F., Kay, S.A. and Chua, N.-H. (1988) Analysis of gene expression in transgenic plants. In Plant Molecular Biology Manual (Gelvin, R.A. and Schilperpoort, R.A., eds). Dordrecht, the Netherlands: Kluwer Academic, pp. 1-29.
51. Navarro, R.E. and Aguirre, J. (1998) Posttranscriptional control mediates cell type-specific expression of catalase A during Aspergillus nidulans development. J. Bacteriol. 180, 5733-5738.
52. Ni, W. and Trelease, R.N. (1991) Posttranscriptional regulation of catalase isozyme expression in cotton seeds. Plant Cell, 3, 737-744.
53. Peterson, L.W., Kleinkopf, G.E. and Huffacker, R.C. (1973) Evidence for tack of turnover of ribulose 1,5-bisphosphate carboxylase in barley leaves. Plant Physiol. 51, 1042-1045.
54. Polidoros, A.N. and Scandalios, J.G. (1997) Response of the maize catalases to light. Free Rad. Biol. Med. 23, 497-504.
55. Preiss, T. and Hentze, M.W. (1999) From factors to mechanisms: translation and translational control in eukaryotes. Curr. Opin. Genet. Dev. 9, 515-521.
56. Ruis, H. and Koller, F. (1997) Biochemistry, molecular biology, and cell biology of yeast and fungal catalases. In Oxidative Stress and the Molecular Biology of Antioxidant Defenses (Scandalios, J.G., ed.). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, pp. 309-342.
57. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
58. Scandalios, J.G. (1994) Regulation and properties of plant catalases. In Causes of Photooxidative Stress and Amelioration of Defence Systems in Plants (Foyer, Ch.H. and Mullineaux, Ph.M., eds). Boca Raton, FL: CRC Press, pp. 275-315.
59. Schmidt, M. and Feierabend, J. (2000) Characterization of cDNA nucleotide sequences encoding two differentially expressed catalase isozyme polypeptides from winter rye (Secale cereale L.). (Accession nos. Z54113, Z99634and AJ251894) (PGR 00-032). Plant Physiol. 122, 1457.
60. Schmitz, G., Schmidt, M. and Feierabend, J. (1996) Characterization of a plastid-specific HSP90 homologue: identification of a cDNA sequence, phylogenetic descendence and analysis of its mRNA and protein expression. Plant Mol. Biol. 30, 479-492.
61. Shang, W. and Feierabend, J. (1999) Dependence of catalase photoinactivation in rye leaves on light intensity and quality and characterization of a chloroplast-mediated inactivation in red light. Photosynth. Res. 59, 201-213.
62. Skadsen, R.W. and Scandalios, J.G. (1987) Translational control of photo-induced expression of the Cat2 catalase gene during leaf development in maize. Proc. Natl Acad. Sci. USA, 84, 2785-2789.
63. Streb, P. and Feierabend, J. (1999) Significance of antioxidants and electron sinks for the cold-hardening-induced resistance of winter rye leaves to photo-oxidative stress. Plant Cell Environ. 22, 1225-1237.
64. Streb, P., Michael-Knauf, A. and Feierabend, J. (1993) Preferential photoinactivation of catalase and photoinhibition of photosystem II are common early symptoms under various osmotic and chemical stress conditions. Physiol. Plant. 88, 590-598.
65. Trebitsh, T., Levitan, A., Sofer, A. and Danon, A. (2000) Translation of chloroplast psbA is modulated in the light by counteracting and reducing activities. Mol. Cell Biol. 20, 1116-1123.
66. Tuck, M.T., Wiehl, P.E. and Pan, T. (1999) Inhibition of 6-methyladenine formation decreases the translation efficiency of dihydrofolate reductase transcripts. Int. J. Biochem. Cell Biol. 31, 837-851.
67. Volk, S. and Feierabend, J. (1989) Photoinactivation of catalase at low temperature and its relevance to photosynthetic and peroxide metabolism in leaves. Plant Cell Environ. 12, 701-712.
68. Willekens, H., Inzé, D., Van Montagu, M. and van Camp, W. (1995) Catalases in plants. Mol. Breed, 1, 207-228.
69. Willekens, H., Langebartels, Ch, Tiré, Ch, Van Montagu, M., Inzé, D. and van Camp, W. (1994) Differential expression of catalase genes in Nicotiana plumbaginifolia (L.). Proc. Natl Acad. Sci. USA, 91, 10450-10454.