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Peroxiredoxin antioxidants in seed physiology

Published online by Cambridge University Press:  22 February 2007

R. B. Aalen
R. B. Aalen
Affiliation:
Division of General Genetics, University of Oslo, PO Box 1031 Blindern, N-0315 Oslo, Norway
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Abstract

Peroxiredoxins are thiol–requiring antioxidants found in organisms ranging from bacteria to humans. They can be divided into two subgroups with either one or two conserved cysteine residues. In plants, 1–Cys peroxiredoxins have been identified in a number of grasses and cereals, and in the dicotyledonous species Arabidopsis thaliana. In contrast to other antioxidants, the 1–Cys peroxiredoxin genes are expressed solely in seeds, and only in the parts of the seeds surviving desiccation, i.e. the embryo and the aleurone layer. The expression pattern is characteristic of late embryogenesis–abundant genes. The PER1 protein of barley is present in high concentrations in the nucleus at the onset of desiccation. 1–Cys genes are expressed in a dormancy–related manner in mature seeds, in that transcript levels are high in imbibed dormant seeds, but disappear upon germination of their non–dormant counterparts. 1–Cys transcript levels can be up–regulated by ABA and osmotic stresses and suppressed by gibberellic acid. Two hypotheses have been put forward on the function of 1–Cys peroxiredoxins in seed physiology. First, these proteins might protect macromolecules of embryo and aleurone cells against damaging reactive oxygen species during seed desiccation and early imbibition. And second, seed peroxiredoxins might play a role in the maintenance of dormancy. These hypotheses are discussed, taking into account present knowledge of the biochemistry and molecular biology of peroxiredoxins.

Keywords

AtPer1desiccation toleranceperoxidoxinthiol-specific antioxidant (TSA)thioredoxin peroxidase (TPx)subcellular localization
Type
Research Article
Information
Seed Science Research , Volume 9 , Issue 4 , April 1999 , pp. 285 - 295
Copyright
Copyright © Cambridge University Press 1999

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References

Aalen, R.B., Opsahl-Ferstad, H.-G., Linnestad, C. and Olsen, O.-A. (1994) Transcripts encoding an oleosin and a dormancy-related protein are present in both the aleurone layer and the embryo of developing barley (Hordeum vulgare L.) seeds. Plant Journal 5, 385–396.CrossRefGoogle Scholar
Baier, M. and Dietz, K.-J. (1997) The plant 2-cys peroxiredoxin BAS1 is a nuclear encoded chloroplast protein: Its expressional regulation, phylogenetic origin, and implications for its specific function in plants. Plant Journal 12, 179–190.CrossRefGoogle ScholarPubMed
Baker, J., Steele, C. and Dure, L. III. (1988) Sequence and characterization of 6 Lea proteins and their genes from cotton. Plant Molecular Biology 11, 277–291.CrossRefGoogle ScholarPubMed
Bewley, J.D. (1997) Seed germination and dormancy. Plant Cell 9, 1055–1066.CrossRefGoogle ScholarPubMed
Bewley, J.D. and Black, M. (1994) Seeds. Physiology of development and germination. New York, Plenum Press.CrossRefGoogle Scholar
Cadle, M.M., Rayfuse, L.M., Walker-Simmons, M.K. and Jones, S.S. (1994) Mapping of abscisic acid responsive genes and VP1 to chromosomes in wheat and Lophopyrum elongatum. Genome 37, 129–132.CrossRefGoogle ScholarPubMed
Chae, H.Z., Kim, I.-H., Kim, K. and Rhee, S.G. (1993) Cloning, sequencing, and mutation of thiol-specific antioxidant gene of Saccharomyces cerevisiae. Journal of Biological Chemistry 268, 16815–16821.CrossRefGoogle ScholarPubMed
Chae, H.Z., Robison, K., Poole, L.B., Church, G., Storz, G. and Rhee, S.G. (1994a) Cloning and sequencing of thiolspecific antioxidant from mammalian brain: Alkyl hydroperoxide reductase and thiol-specific antioxidant define a large family of antioxidant enzymes. Proceedings of the National Academy of Sciences, USA 91, 7017–7021.CrossRefGoogle ScholarPubMed
Chae, H.Z., Chung, S.J. and Rhee, S.G. (1994b) Thioredoxin-dependent peroxide reductase from yeast. Journal of Biological Chemistry 269, 27670–27678.CrossRefGoogle ScholarPubMed
Chae, H.Z., Uhm, T.B. and Rhee, S.G. (1994c) Dimerization of thiol-specific antioxidant and the essential role of cysteine 47. Proceedings of the National Academy of Sciences, USA 91, 7022–7026.CrossRefGoogle ScholarPubMed
Chen, Z.-L.,Schuler, M.A. and Beachy, R.N. (1986) Functional analysis of regulatory elements in a plant embryo-specific gene. Proceedings of the National Academy of Sciences, USA 83, 8560–8564.CrossRefGoogle Scholar
Close, T.J. (1996) Dehydrins: Emergence of a biochemical role of a family of plant dehydration proteins. Physiologia Plantarum 97, 795–803.CrossRefGoogle Scholar
Dure, L. III. (1993a) A repeating 11-mer amino acid motif and plant desiccation. Plant Journal 3, 363–369.CrossRefGoogle ScholarPubMed
Dure, L. III. (1993b) Structural motifs in Lea proteins. pp 91–103in Close, T.J.; Bray, E.A. (Eds) Current topics in plant physiology, Volume 10. Rockville, USA, American Society of Plant Physiologists.Google Scholar
Espelund, M., Sæbøe-Larssen, S., Hughes, D.W., Galau, G.A., Larsen, F. and Jakobsen, K.S. (1992) Late embryogenesis-abundant genes encoding proteins with different numbers of hydrophilic repeats are regulated differentially by abscisic acid and osmotic stress. Plant Journal 2, 241–252.CrossRefGoogle ScholarPubMed
Espelund, M., De Bedout, J.A., Outlaw, W.H. Jr. and Jakobsen, K.S. (1995) Environmental and hormonal regulation of barley late-embryogenesis-abundant (Lea) mRNAs is via different signal transduction pathways. Plant, Cell and Environment 18, 943–949.CrossRefGoogle Scholar
Evans, M., Black, M. and Chapman, J. (1975) Induction of hormone sensitivity by dehydration is one positive role for drying in cereal seed. Nature 258, 144–145.CrossRefGoogle Scholar
Foyer, C.H., Descourvieres, P. and Kunert, K.J. (1994) Protection against oxygen radicals: an important defence mechanism studied in transgenic plants. Plant, Cell and Environment 17, 507–523.CrossRefGoogle Scholar
Frank, S., Munz, B. and Werner, S. (1997) The human homologue of a bovine non-selenium glutathione peroxidase is a novel keratinocyte growth factorregulated gene. Oncogene 14, 915–921.CrossRefGoogle ScholarPubMed
Galau, G.A., Wang, H.Y.-C. and Hughes, D.W. (1993) Cotton Lea5 and Lea14 encode atypical late embryogenesis-abundant proteins. Plant Physiology 101, 695–696.CrossRefGoogle ScholarPubMed
Goldmark, P.J., Curry, J., Morris, C.F. and Walker- Simmons, M.K. (1992) Cloning and expression of an embryo-specific mRNA up-regulated in hydrated dormant seeds. Plant Molecular Biology 19, 433–441.CrossRefGoogle ScholarPubMed
Guiltinan, M.J., Marcotte, W.R. and Quatrano, R.S. (1990) A plant leucine zipper protein that recognizes an abscisic acid responsive element. Science 250, 267–271.CrossRefGoogle Scholar
Haslekås, C., Stacy, R.A.P., Nygaard, V., Culiáñez-Macià, F.A. and Aalen, R.B. (1998) The expression of a peroxiredoxin antioxidant gene, AtPer1, in Arabidopsis thaliana is seed specific and related to dormancy. Plant Molecular Biology 36, 833–845.CrossRefGoogle ScholarPubMed
Hiroi, T., Watabe, S., Takimoto, K., Yago, N., Yamamoto, Y. and Takahashi, S.Y. (1996). The cDNA sequence encoding bovine SP-22, a new defence system against reactive oxygen species in mitochondria. DNA Sequence 6, 239–242.CrossRefGoogle ScholarPubMed
Holbrook, L.A., van Rooijen, G.J.H., Wilen, R.W. and Moloney, M.M. (1991) Oilbody proteins in microsporederived embryos of Brassica napus. Plant Physiology 97, 1051–1058.CrossRefGoogle ScholarPubMed
Jacobson, F.S., Morgan, R.W., Christman, M.F. and Ames, B.N. (1989) An alkyl hydroperoxide reductase from Salmonella typhimurium involved in the defence of DNA against oxidative damage. Journal of Biological Chemistry 264, 1488–1496.CrossRefGoogle ScholarPubMed
Jakobsen, K.S., Klemsdal, S.S., Aalen, R.B., Bosnes, M., Alexander, D. and Olsen, O.-A. (1989) Barley aleurone cell development: molecular cloning of aleurone-specific cDNAs from immature grains. Plant Molecular Biology 12, 285–293.CrossRefGoogle ScholarPubMed
Kalla, R., Shimamoto, K., Potter, R., Nielsen, P.S., Linnestad, C. and Olsen, O.-A. (1994) The promoter of the barley aleurone-specific gene encoding a putative 7 kDa lipid transfer protein confer aleurone cell-specific expression in transgenic rice. Plant Journal 6, 849–860.CrossRefGoogle ScholarPubMed
Kang, S.W., Baines, I.C. and Rhee, S.G. (1998) Characterization of a mammalian peroxiredoxin that contains one conserved cysteine. Journal of Biological Chemistry 273, 6303–6311.CrossRefGoogle ScholarPubMed
Karssen, C.M., Brinkhorst-van der Swan, D.L.C., Breekland, A.E. and Koornneef, M. (1983) Induction of dormancy during seed development by endogenous abscisic acid: studies on abscisic acid deficient genotypes of Arabidopsis thaliana (L.) Heynh. Planta 157, 158–165.CrossRefGoogle ScholarPubMed
Kim, K., Kim, I.H., Lee, K.-Y., Rhee, S.G. and Stadtman, E.R. (1988) The isolation and purification of a specific ‘protector’ protein which inhibits enzyme inactivation by a thiol/Fe(III)/O2 mixed-function oxidation system. Journal of Biological Chemistry 263, 4704–4711.CrossRefGoogle ScholarPubMed
Kim, T.-S., Sundaresh, C.S., Feinstein, S.I., Dodia, C., Skach, W.R., Jain, M.K., Nagase, T., Seki, N., Ishikawa, K.-I., Nomura, N. and Fisher, A.B. (1997) Identification of a human cDNA clone for lysosomal type Ca2+- independent phospholipase A2 and properties of the expressed protein. Journal of Biological Chemistry 272, 2542–2550.CrossRefGoogle ScholarPubMed
Koornneef, M., Jorna, M.L., Brinkhorst-van der Swan, D.L.C. and Karssen, C.M. (1982) The isolation of abscisic acid (ABA) deficient mutants by selection of induced revertants in non-germinating gibberellin sensitive lines of Arabidopsis thaliana (L.) Heynh. Theoretical and Applied Genetics 61, 385–393.CrossRefGoogle ScholarPubMed
Koornneef, M., Reuling, G. and Karssen, C.M. (1984) The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiologia Plantarum 61, 377–383.CrossRefGoogle Scholar
Kwon, S.J., Park, J.-W., Choi, W.-K., Kim, I.H. and Kim, K. (1994) Inhibition of metal-catalyzed oxidation systems by a yeast protector protein in the presence of thioredoxin. Biochemical and Biophysical Research Communications 201, 8–15.CrossRefGoogle ScholarPubMed
Leah, R., Skriver, K., Knudsen, S., Ruud-Hansen, J., Raikhel, N.V. and Mundy, J. (1994) Identification of an enhancer/silencer sequence directing the aleuronespecific expression of a barley chitinase gene. Plant Journal 6, 579–589.CrossRefGoogle ScholarPubMed
Leon-Kloosterziel, K.M., van de Bunt, G.A., Zeevart, J.A.D. and Koornneef, M. (1996) Arabidopsis mutants with a reduced seed dormancy. Plant Physiology 110, 233–240.CrossRefGoogle ScholarPubMed
Leprince, O., Hendry, G.A.F. and McKersie, B.D. (1993) The mechanisms of desiccation tolerance in developing seeds. Seed Science Research 3, 231–246.CrossRefGoogle Scholar
Leprince, O., Atherton, N.M., Deltour, R. and Hendry, G.A.F. (1994) The involvement of respiration in free radical processes during loss of desiccation tolerance in germinating Zea mays L. Plant Physiology 104, 1333–1339.CrossRefGoogle ScholarPubMed
Li, B. and Foley, M.E. (1997) Genetic and molecular control of seed dormancy. Trends in Plant Science 2, 384–389.CrossRefGoogle Scholar
Lim, Y.S., Cha, M.K., Kim, H.K., Uhm, T.B., Park, J.W., Kim, K. and Kim, I.H. (1993) Removals of hydrogen peroxide and hydroxyl radical by thiol-specific antioxidant protein as a possible role in vivo. Biochemical and Biophysical Research Communications 192, 273–280.CrossRefGoogle ScholarPubMed
Lim, Y.S., Cha, M.-K., Yun, C.-H., Kim, H.-K., Kim, K. and Kim, I.-H. (1994) Purification and characterization of thiol-specific antioxidant protein from human red blood cell: a new type of antioxidant protein. Biochemical and Biophysical Research Communications 199, 199–206.CrossRefGoogle ScholarPubMed
Linnestad, C., Lönneborg, A., Kalla, R. and Olsen, O.-A. (1991) Promoter of a lipid transfer protein gene expressed in barley aleurone cells contains similar myb and myc recognition sites as the maize Bz-McC allele. Plant Physiology 97, 841–843.CrossRefGoogle ScholarPubMed
McGonigle, S., Dalton, J.P. and James, E.R. (1998) Peroxidoxins: A new antioxidant family. Parasitology Today 14, 139–145.CrossRefGoogle ScholarPubMed
Netto, L.E.S., Chae, H.Z., Kang, S.-W., Rhee, S.G. and Stadtman, E.R. (1996) Removal of hydrogen peroxide by thiol-specific antioxidant enzyme (TSA) is involved with its antioxidant properties. Journal of Biological Chemistry 271, 15315–15321.CrossRefGoogle ScholarPubMed
Oliver, M.J. (1996) Desiccation tolerance in vegetative plant cells. Physiologia Plantarum 97, 779–787.CrossRefGoogle Scholar
Parcy, F. and Giraudat, J. (1997) Interactions between the ABI1 and the ectopically expressed ABI3 genes in controlling abscisic acid responses in Arabidopsis vegetative tissues. Plant Journal 11, 693–702.CrossRefGoogle ScholarPubMed
Parcy, F., Valon, C., Raynal, M., Gaubier-Comella, P., Delseny, M. and Giraudat, J. (1994) Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6, 1567–1582.Google ScholarPubMed
Peshenko, I.V., Novoselov, V.I., Evdokimov, V.A., Nikolaev, Yu.V., Shuvaeva, T.M., Lipkin, V.M. and Fesenko, E.E. (1996) Novel 28-kDa secretory protein from rat olfactory epithelium. FEBS Letters 381, 12–14.CrossRefGoogle ScholarPubMed
Reinbothe, C., Tewes, A. and Reinbothe, S. (1992) Altered gene expression during somatic embryogenesis in Nicotiana plumbaginifolia and Digitalis lantana. Plant Science 82, 47–58.CrossRefGoogle Scholar
Rushmore, T.H., Morton, M.R. and Pickett, C.B. (1991) The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. Journal of Biological Chemistry 266, 11632–11639.CrossRefGoogle ScholarPubMed
Scandalios, J.G. (1987) The antioxidant enzyme genes Cat and Sod of maize: regulation, functional significance, and molecular biology. pp 19–44in Rattazzi, M.C.; Scandalios, J.G.; Whitt, G.S. (Eds) Isozymes: Current topics in biological and medical research, volume 16, Molecular and cellular biology. New York, Alan R. Liss.Google Scholar
Shichi, H. and Demar, J.C. (1990) Non-selenium glutathione peroxidase without glutathione S-transferase activity from bovine ciliary body. Experimental Eye Research 50, 513–520.CrossRefGoogle ScholarPubMed
Singh, A.K. and Shichi, H. (1998) A novel glutathione peroxidase in bovine eye. Sequence analysis, mRNA level, and translation. Journal of Biological Chemistry 273, 26171–26178.CrossRefGoogle ScholarPubMed
Stacy, R.A.P., Munthe, E., Steinum, T., Sharma, B. and Aalen, R.B. (1996) A peroxiredoxin antioxidant is encoded by a dormancy-related gene, Per1, expressed during late development in the aleurone and embryo of barley grains. Plant Molecular Biology 31, 1205–1216.CrossRefGoogle ScholarPubMed
Stacy, R.A.P., Nordeng, T.W., Culiáñez-Macià, F.A. and Aalen, R.B. (1999) The dormancy-related peroxiredoxin antioxidant, PER1, is localized to the nucleus of barley embryo and aleurone cells. Plant Journal 19, 1–8.CrossRefGoogle Scholar
Stirn, S., Mordhorst, A.P., Fuchs, S. and Loerz, H. (1995) Molecular and biochemical markers for embryogenic potential and regenerative capacity of barley (Hordeum vulgare L.) cell cultures. Plant Science 106, 195–206.CrossRefGoogle Scholar
Yim, M.B., Chae, H.Z., Rhee, S.G., Chock, P.B. and Stadtman, E.R. (1994). On the protective mechanism of the thiol-specific antioxidant enzyme against the oxidative damage of biomacromolecules. Journal of Biological Chemistry 269, 1621–1626.CrossRefGoogle ScholarPubMed