Skip to main content
SpringerLink
Log in

Mode of translational activation of the catalase (cat1) mRNA of rye leaves (Secale cereale L.) and its control through blue light and reactive oxygen

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The enzyme catalase (EC 1.11.1.6) is inactivated by light and must be continuously replaced by new synthesis in order to maintain a constant enzyme activity in leaves. In winter rye leaves (Secale cereale L.) posttranscriptional mechanisms determine the rate of new catalase synthesis, including a light-controlled reversible modification of the catalase cat1 mRNA by methylation which greatly enhanced its translation efficiency. The specificity and regulation of this mRNA activation were further investigated. The translation efficiency of the rye cat1 mRNA was much more enhanced by N-7 methylation of the cap than that of an lhcb transcript. Investigations with truncated rye cat1 mRNAs indicated that the translational enhancement resulting from N-7 cap methylation did not require the presence of specific sequences of cat1 5′- and 3′-untranslated regions. Translational activation of the cat1 mRNA in rye leaves was independent of photosynthesis and most effectively induced by blue light. Peroxides (H2O2, tertiary butyl hydroperoxide) and conditions enforcing an H2O2 accumulation in the leaves (aminotriazole, paraquat) also caused an activation of the cat1 mRNA. A search for further signalling systems controlling the replenishment of inactivated catalase in light suggested that an inositol-1,4,5-triphosphate-mediated liberation of Ca2+ from internal stores and a protein phosphatase played some role. However, these signalling systems did not affect the activation of the cat1 mRNA. After removal of Ca2+ by EGTA the cat1 mRNA was rapidly degraded.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

DCMU:

3-(3,4-dichlorophenyl)-1,1-dimethylurea

PAR:

Photosynthetically active radiation

ROS:

Reactive oxygen species

UTR:

Untranslated region

References

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–393

    Article  PubMed  CAS  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  PubMed  CAS  Google Scholar 

  • Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134

    Article  PubMed  CAS  Google Scholar 

  • Bailey-Serres J (1999) Selective translation of cytoplasmic mRNAs in plants. Trends Plant Sci 4:141–148

    Article  Google Scholar 

  • Bailey-Serres J, Dawe RK (1996) Both 5′ and 3′ sequences of maize adh1 mRNA are required for enhanced translation under low-oxygen conditions. Plant Physiol 112:685–695

    Article  PubMed  CAS  Google Scholar 

  • Ball L, Accotto G-P, Bechtold U, Creissen G, Funck D, Jimenez A, Kular B, Leyland N, Mejia-Carranza J, Reynolds H, Karpinski S, Mullineaux PM (2004) Evidence for a link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. Plant Cell 16:2448–2462

    Article  PubMed  CAS  Google Scholar 

  • Bradbeer JW (1969) The activities of photosynthetic carbon cycle enzymes of greening bean leaves. New Phytol 68:233–245

    Article  Google Scholar 

  • Browning KS (1996) The plant translational apparatus. Plant Mol Biol 32:107–144

    Article  PubMed  CAS  Google Scholar 

  • Bruick RK, Mayfield SP (1999) Light-activated translation of chloroplast mRNAs. Trends Plant Sci 4:190–195

    Article  PubMed  Google Scholar 

  • Carberry SE, Darzynkiewicz E, Goss DJ (1991) A comparison of the binding of methylated cap analogues to wheat germ protein synthesis initiation factors 4F and (Iso)4F. Biochemistry 30:1624–1627

    Article  PubMed  CAS  Google Scholar 

  • Chandok MR, Sopory SK, Oelmüller R (2001) Cytoplasmic kinase and phosphatase activities can induce PsaF gene expression in the absence of functional plastids: evidence that phosphorylation/dephosphorylation events are involved in interorganellar crosstalk. Mol Gen Genet 264:819–826

    Article  PubMed  CAS  Google Scholar 

  • Cheng L, Kellogg III EW, Packer L (1981) Photoinactivation of catalase. Photochem Photobiol 34:125–129

    PubMed  CAS  Google Scholar 

  • Feierabend J (2005) Catalases in plants: molecular and functional properties and role in stress defence. In: Smirnoff N (ed) Antioxidants and reactive oxygen species in plants. Blackwell, Oxford, pp 101–140

    Chapter  Google Scholar 

  • Feierabend J, 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

    CAS  Google Scholar 

  • Feierabend J, Schaan C, 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

    PubMed  CAS  Google Scholar 

  • Gabev E, Kasianowicz J, Abbott T, McLaughlin S (1989) Binding of neomycin to phosphatidylinositol 4,5-bisphosphate (PIP)2. Biochem Biophys Acta 979:105–112

    Article  PubMed  CAS  Google Scholar 

  • Gallie DR (1993) Posttranscriptional regulation of gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 44:77–105

    Article  CAS  Google Scholar 

  • Gallie DR, Browning KS (2001) eIF4G functionally differs from eIF4iso4G in promoting internal initiation, cap-independent translation, and translation of structured mRNAs. J Biol Chem 276:36951–36960

    Article  PubMed  CAS  Google Scholar 

  • Gillian-Daniel DL, Gray NK, Å ström J, Barkoff A, 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

    PubMed  CAS  Google Scholar 

  • Haake V, Geiger M, Walch-Liu P, Engels C, Zrenner R, Stitt M (1999) Changes in aldolase activity in wild-type potato plants are important for acclimation to growth irradiance and carbon dioxide concentration, because plastid aldolase exerts control over the ambient rate of photosynthesis across a range of growth conditions. Plant J 17:479–489

    Article  CAS  Google Scholar 

  • Hansen ER, Petracek ME, Dickey LF, Thompson WF (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

    Article  PubMed  CAS  Google Scholar 

  • Hertwig B, Streb P, Feierabend J (1992) Light dependence of catalase synthesis and degradation in leaves and the influence of interfering stress conditions. Plant Physiol 100:1547–1553

    PubMed  CAS  Google Scholar 

  • Kawaguchi R, Bailey-Serres J (2002) Regulation of translational initiation in plants. Curr Opin Plant Biol 5:460–465

    Article  PubMed  CAS  Google Scholar 

  • Levine A, Tenhaken R, Dixon RA, Lamb CJ (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593

    Article  PubMed  CAS  Google Scholar 

  • Lück H (1965) Catalase. In: HU Bergmeyer (ed) Methods of enzymatic analysis. Academic, New York, pp 885–894

    Google Scholar 

  • Manjunath S, Williams AJ, Bailey-Serres J (1999) Oxygen deprivation stimulates Ca2+-mediated phosphorylation of mRNA cap-binding protein eIF4E in maize roots. Plant J 19:21–30

    Article  PubMed  CAS  Google Scholar 

  • Mazumder B, Seshandri V, Fox PL (2003) Translational control by the 3′-UTR: the ends specify the means. Trends Biochem Sci 28:91–98

    Article  PubMed  CAS  Google Scholar 

  • Mishra NP, Mishra RK, Singhal GS (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

    PubMed  CAS  Google Scholar 

  • Muir SR, Sanders D (1997) Inositol 1,4,5-trisphosphate-sensitive Ca2+ release across non-vacuolar membranes in cauliflower. Plant Physiol 114:1511–1521

    Article  PubMed  CAS  Google Scholar 

  • Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5:388–395

    Article  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  PubMed  CAS  Google Scholar 

  • Pfannschmidt T, Allen JF, Oelmüller R (2001) Principles of redox control in photosynthesis gene expression. Physiol Plant 112:1–9

    Article  CAS  Google Scholar 

  • Polidoros AN, Scandalios JG (1999) Role of hydrogen peroxide and different classes of antioxidants in the regulation of catalase and glutathione S-transferase gene expression in maize (Zea mays L.). Physiol Plant 106:112–120

    Article  CAS  Google Scholar 

  • Schäfer L, Feierabend J (2000) Photoinactivation and protection of glycolate oxidase in vitro and in leaves. Z Naturforsch 55c:361–372

    Google Scholar 

  • Schmidt M, Feierabend J (2000) Characterization of cDNA nucleotide sequences encoding two differentially expressed catalase isozyme polypeptides from winter rye (Secale cereale L.) (Accession nos. Z54143, Z99634 and AJ251894) (PGR 00-032). Plant Physiol 122:1457

    Article  Google Scholar 

  • Schmidt M, Dehne S, Feierabend J (2002) 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 J 31:601–613

    Article  PubMed  CAS  Google Scholar 

  • Shang W, 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

    Article  CAS  Google Scholar 

  • Skadsen RW, Scandalios JG (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

    Article  PubMed  CAS  Google Scholar 

  • Streb P, 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

    Article  CAS  Google Scholar 

  • Tang L, Bhat S, Petracek E (2003) Light control of nuclear gene mRNA abundance and translation in tobacco. Plant Physiol 133:1979–1990

    Article  PubMed  CAS  Google Scholar 

  • Trebitsch T, Levitan A, Sofer A, Danon A (2000) Translation of chloroplast psbA mRNA is modulated in the light by counteracting oxidizing and reducing activities. Mol Cell Biol 20:1116–1123

    Article  Google Scholar 

  • Vandenabeele S, van der Kelen K, Dat J, Gadjev I, Boonefaes T, Morsa S, Rottiers P, Slooten L, van Montagu M, Zabeau M, Inzé D, van Breusegem F (2003) A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. Proc Natl Acad Sci USA 100:16113–16118

    Article  PubMed  CAS  Google Scholar 

  • Wilkie GS, Dickson KS, Gray NK (2003) Regulation of mRNA translation by 5′- and 3′-UTR-binding factors. Trends Biochem Sci 28:182–188

    Article  PubMed  CAS  Google Scholar 

  • Willekens H, Inzé D, van Montagu M, van Camp W (1995) Catalases in plants. Mol Breed 1:207–228

    Article  CAS  Google Scholar 

  • Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M, Inzé D, Van Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J 16:4806–4816

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Zhu J-K (2001) Abiotic stress signal transduction in plants: molecular and genetic perspectives. Physiol Plant 112:152–166

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Financial support by the Deutsche Forschungsgemeinschaft (DFG), Bonn, is greatly appreciated. We thank Kerstin Pieper and Christel van Oijen for excellent technical assistance.

Author information

Authors and Affiliations

  1. Fachbereich Biowissenschaften, Goethe-Universität, Fach 213, 60054, Frankfurt am Main, Germany

    Matthias Schmidt, Jürgen Grief & Jürgen Feierabend

Authors
  1. Matthias Schmidt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jürgen Grief
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jürgen Feierabend
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jürgen Feierabend.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schmidt, M., Grief, J. & Feierabend, J. Mode of translational activation of the catalase (cat1) mRNA of rye leaves (Secale cereale L.) and its control through blue light and reactive oxygen. Planta 223, 835–846 (2006). https://doi.org/10.1007/s00425-005-0125-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-005-0125-8

Keywords

Search

Navigation