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A peroxiredoxin antioxidant is encoded by a dormancy-related gene,Per1, expressed during late development in the aleurone and embryo of barley grains

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Abstract

Antioxidants can remove damaging reactive oxygen species produced as by-products of desiccation and respiration during late embryogenesis, imbibition of dormant seeds and germination. We have expressed a protein, PER1, encoded by theBalem (barleyaleurone andembryo) transcript previously called B15C, and show it to reduce oxidative damagein vitro. PER1 shares high similarity to a novel group of thiol-requiring antioxidants, named peroxiredoxins, and represents a subgroup with only one conserved cysteine residue (1-Cys). PER1 is the first antioxidant belonging to the 1-Cys subgroup shown to be functionally active, and the first peroxiredoxin of any kind to be functionally described in plants. The steady state level of the transcript,Per1, homologous to a dormancy-related transcript (pBS128) from bromegrass (Bromus secalinus), increases considerably in imbibed embryos from dormant barley (Hordeum vulgare L.) grains. Our investigations also indicate thatPer1 transcript levels are dormancy-related in the aleurone layer of whole grains. In contrast to most seed-expressed antioxidantsPer1 disappears in germinating embryos, and in the mature aleurone the transcript is down-regulated by the germinating embryo or by gibberellic acid (GA). Our data show that the barley seed peroxiredoxin is encoded by a singlePer1 gene. Possible roles of the PER1 peroxiredoxin in barley grains during desiccation, dormancy and imbibition are discussed.

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References

  1. Aalen RB, Opsahl-Ferstad H-G, Linnestad C, Olsen O-A: 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 J 5: 385–396 (1994).

    Google Scholar 

  2. Aalen RB: The transcripts encoding two oleosin isoforms are both present in the aleurone and in the embryo of barley (Hordeum vulgare L.) seeds. Plant Mol Biol 28: 583–588 (1995).

    Google Scholar 

  3. Bewley JD, Black M: Seeds: Physiology of Development and Germination, Plenum Press, New York (1994).

    Google Scholar 

  4. Buraas T, Skinnes H: Development and seed dormancy in barley, wheat and triticale under controlled conditions. Acta Agric Scand 35: 233–244 (1985).

    Google Scholar 

  5. Cakmak I, Strbac D, Marschner H: Activities of hydrogen peroxide-scavenging enzymes in germinating wheat seeds. J Exp Bot 258: 127–132 (1993).

    Google Scholar 

  6. Chae HZ, Robison K, Poole LB, Church G, Storz G, Rhee SG: Cloning and sequencing of thiol-specific antioxidant from mammalian brain: alkyl hydroperoxide reductase and thiol-specific antioxidant define a large family of antioxidant enzymes. Proc Natl Acad Sci USA 91: 7017–7021 (1994).

    Google Scholar 

  7. Chae HZ, Uhm TB, Rhee SG: Dimerization of thiol-specific antioxidant and the essential role of cysteine 47. Proc Natl Acad Sci USA 91: 7022–7026 (1994).

    Google Scholar 

  8. Chae HZ, Chung SJ, Rhee SG: Thioredoxin-dependent peroxide reductase from yeast. J Biol Chem 269: 27670–27678 (1994).

    Google Scholar 

  9. Dyer WE: Dormancy-associated embryonic mRNAs and proteins in imbibingAvena fatua caryopses. Physiol Plant 88: 201–211 (1993).

    Google Scholar 

  10. Espelund M, Prentice Stacy RA, Jakobsen KS: A simple method for generating single-stranded DNA probes labeled to high activities. Nucl Acids Res 18: 6157–6158 (1990).

    Google Scholar 

  11. Espelund M, DeBedout JA, Outlaw WHJr, Jakobsen KS: Environmental and hormonal regulation of barley late-embryogenesis-abundant (Lea) mRNAs is via different signal transduction pathways. Plant Cell Environ 18: 43–949 (1995).

    Google Scholar 

  12. Evans M, Black M, Chapman J: Induction of hormone sensitivity by dehydration is one positive role for drying in careal seed. Nature 258: 144–145 (1975).

    Google Scholar 

  13. Fincher GB: Molecular and cellular biology associated with endosperm mobilization in germinating cereal grains. Annu Rev Plant Physiol Plant Mol Biol 40: 305–346 (1989).

    Google Scholar 

  14. Fontaine O, Huault C, Pavis N, Billard J-P: Dormancy break-age ofHordeum vulgare seeds: effects of hydrogen peroxide and scarification on glutathione level and glutathione reductase activity. Plant Physiol Biochem 32: 677–683 (1994).

    Google Scholar 

  15. Fuerst EP, Upadhyaya MK, Simpson GM, Naylor JM, Adkins SW: A study of the relationship between seed dormancy and pentose phosphate pathway activity inAvena fatua. Can J Bot 61: 667–670 (1983).

    Google Scholar 

  16. Goldmark PJ, Curry J, Morris CF, Walker-Simmons MK: Cloning and expression of an embryo-specific mRNA up-regulated in hydrated dormant seeds. Plant Mol Biol 19: 433–441 (1992).

    Google Scholar 

  17. Heck GR, Ho T-HD: Gibberellin-repressible gene expression in the barley aleurone layer. Plant Mol Biol, in press.

  18. Hu H, Couvillon GA: Activities of catalase and pentose phosphate pathway dehydrogenases during dormancy release in nectarine seed. J Am Soc Hort Sci 115: 987–990 (1990).

    Google Scholar 

  19. Jacobson FS, Morgan RW, Christman MF, Ames BN: An alkyl hydroperoxide reductase fromSalmonella typhimurium involved in the defence of DNA against oxidative damage. J Biol Chem 264: 1488–1496 (1989).

    Google Scholar 

  20. Jakobsen K, Klemsdal SS, Aalen RB, Bosnes M, Alexander D, Olsen O-A: Barley aleurone cell development: molecular cloning of aleurone-specific cDNAs from immature grains. Plant Mol Biol 12: 285–293 (1989).

    Google Scholar 

  21. Jakobsen KS, Breivold E, Hornes E: Purification of mRNA directly from crude plant tissues in 15 minutes using magnetic oligo dT microspheres. Nucl Acids Res 18: 3669 (1990).

    Google Scholar 

  22. Jefferson RA, Kavanagh TA, Bevan MW: GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901–3907 (1987).

    Google Scholar 

  23. Johnson RR, Cranston HJ, Chaverra ME, Dyer WE: Characterization of cDNA clones for differentially expressed genes in embryos of dormant and nondormantAvena fatua L. caryopses. Plant Mol Biol 28: 113–122 (1995).

    Google Scholar 

  24. Kawai S, Takeshita S, Okazaki M, Kikuno R, Kudo A, Amann E: Cloning and characterization of OSF-3, a new member of theMER5 family, expressed in mouse osteoblastic cells. J Biochem 115: 641–643 (1994).

    Google Scholar 

  25. Kim K, Kim IH, Lee K-Y, Rhee SG, Stadtman ER: The isolation and purification of a specific "protector" protein which inhibits enzyme inactivation by a thiol/Fe(III)/O2 mixed-function oxidation system. J Biol Chem 263: 4704–4711 (1988).

    Google Scholar 

  26. Klein TM, Wolf ED, Wu R, Sanford JC: High-velocity microprojectiles for delivering nucleic acids into living cells. Nature 327, 70–73 (1987).

    Google Scholar 

  27. Kleinhofs A: Barley Steptoe × Morex map. File available via Internet Gopher, host greengenes.cit.cornell.edu. port7ϕ, menu "Grain files to browse"/"Barley Steptoe × Morex map" (1994).

  28. Klemsdal SS, Hughes W, Lönneborg A, Aalen RB, Olsen O-A: Primary structure of a novel barley gene differentially expressed in immature aleurone layers. Mol Gen Genet 228: 9–16 (1991).

    Google Scholar 

  29. Kwon SJ, Park J-W, Choi W-K, Kim IH, Kim K: Inhibition of metal-catalyzed oxidation systems by a yeast protector protein in the presence of thioredoxin. Biochem Biophys Res Comm 201: 8–15 (1994).

    Google Scholar 

  30. Leprince O, Hendry GAF, McKersie BD: The mechanisms of desiccation tolerance in developing seeds. Seed Sci Res 3: 231–246 (1993).

    Google Scholar 

  31. Leprince O, Atherton NM, Deltour R, Hendry GAF: The involvement of respiration in free radical processes during loss of desiccation tolerance in germinatingZea mays L. Plant Physiol 104: 1333–1339 (1994).

    Google Scholar 

  32. Li B, Foley ME: Differential polypeptide patterns in imbibed and after-ripenedAvena fatua embryos. J Expt Bot 45: 275–279 (1994).

    Google Scholar 

  33. Li B, Foley ME: Cloning and characterization of differentially expressed genes in imbibed dormant and afterripenedAvena fatua embryos. Plant Mol Biol 29: 823–831 (1995).

    Google Scholar 

  34. Lim YS, Cha MK, Kim HK, Uhm TB, Park JW, Kim K, Kim IH: Removals of hydrogen peroxide and hydroxyl radical by thiol-specific antioxidant protein as a possible rolein vivo. Biochem Biophys Res Comm 192: 273–280 (1993).

    Google Scholar 

  35. Lim Y-S, Cha M-K, Yun C-H, Kim H-K, Kim K, Kim I-H: Purification and characterization of thiol-specific antioxidant protein from human red blood cell: a new type of antioxidant protein. Biochem Biophys Res Comm 199: 199–206 (1994).

    Google Scholar 

  36. Maas C, Laufs J, Grant S, Korfhage C, Werr W: The combination of a novel stimulatory element in the first exon of the maizeShrunken-1 gene with the following intron 1 enhances reporter gene expression up to 1000-fold. Plant Mol Biol 16: 199–207 (1991).

    Google Scholar 

  37. McElroy D, Zhan W, Cao J, Wu R: Isolation of an efficient actin promoter for use in rice transformation. Plant Cell 2: 163–171 (1990).

    Google Scholar 

  38. Mordhorst AP, Stirn S, Dresselhaus T, Lörz H: Controlling factors and markers for embryogenic potential and regeneration capacity in barley (Hordeum vulgare L.) cell cultures. In: Terzi M, Cella R, Falavigna A (eds) Current Issues in Plant Molecular and Cellular Biology, Proceedings of the VIIIth International Congress on Plant Tissue and Cell Culture, pp. 383–388. Kluwer Academic Publishers, Dordrecht (1994).

    Google Scholar 

  39. Morris CF, Anderberg RJ, Goldmark PJ, Walker-Simmons MK: Molecular cloning and expression of abscisic acid-responsive genes in embryos of dormant wheat seeds. Plant Physiol 95: 814–821 (1991).

    Google Scholar 

  40. Mundy J, Chua N-H: Abscisic acid and water-stress induce the expression of a novel rice gene. EMBO J 8: 2279–2286 (1988).

    Google Scholar 

  41. Nolan RC, Ho DT-H: Hormonal regulation of gene expression in barley aleurone layers: induction and suppression of specific genes. Planta 174: 551–560 (1988).

    Google Scholar 

  42. Olsen O-A, Jakobsen KS, Schmelzer E: Development of barley aleurone cells: temporal and spatial patterns of accumulation of cell-specific mRNAs. Planta 181: 462–466 (1990).

    Google Scholar 

  43. Prospéri M-T, Ferbus D, Karczinski I, Goubin G: A human cDNA corresponding to a gene overexpressed during cell proliferation encodes a product sharing homology with amoebic and bacterial proteins. J Biol Chem 268: 11050–11056 (1993).

    Google Scholar 

  44. Puntarulo S, Galleano M, Sanchez RA, Boveris A: Superoxide anion and hydrogen peroxide metabolism in soybean embryonic axes during germination. Biochim Biophys Acta 1074: 277–283 (1991).

    Google Scholar 

  45. Roberts EH, Smith RD: Dormancy and the pentose phosphate pathway. In: Khan AA (ed) The Physiology and Biochemistry of Seed Dormancy and Germination, pp. 385–411. North-Holland Publishing Co., Amsterdam (1977).

    Google Scholar 

  46. Rogers JC, Milliman C: Coordinate increase in major transcripts from the high pI α-amylase multigene family in barley aleurone cells stimulated with gibberellic acid. J Biol Chem 259: 12234–12240 (1984).

    Google Scholar 

  47. Ross JD: Metabolic aspects of dormancy. In: Murray DR (ed) Seed Physiology Vol 2: Germination and Reserve Mobilization, pp. 45–76. Academic Press, Sydney (1984).

    Google Scholar 

  48. Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).

    Google Scholar 

  49. Scandalios JG: The antioxidant enzyme genesCat andSod of maize: regulation, functional significance, and molecular biology. In: Rattazzi MC, Scandalios JG, Whitt GS (eds) Isozymes: Current Topics in Biological and Medical Research, Vol. 14: Molecular and Cellular Biology, pp. 19–44. Alan R. Liss, New York (1987).

    Google Scholar 

  50. Schuurink RC, Sedee NJA, Wang M: Dormancy of the barley grain is correlated with gibberellic acid responsiveness of the isolated aleurone layer. Plant Physiol. 100: 1834–1839 (1992).

    Google Scholar 

  51. Storz G, Jacobson FS, Tartaglia TA, Morgan RW, Silveira LA, Ames BN: An alkyl hydroperoxide reductase induced by oxidative stress inSalmonella typhimurium andEscherichia coli: genetic characterization and cloning ofahp. J Bact 171: 2049–2055 (1989).

    Google Scholar 

  52. vanBeckum JMM, Libbenga KR, Wang M: Abscisic acid and gibberellic acid-regulated responses of embryos and aleurone layers isolated from dormant and nondormant barley grains. Physiol Plant 89: 483–489 (1993).

    Google Scholar 

  53. Walker-Simmons MK, Goldmark PJ: Characterization of genes expressed when dormant seeds of cereals and wild grasses are hydrated and remain growth-arrested. In: Lang GA (ed) Plant Dormancy: Its Physiology, Biochemistry and Molecular Biology. CAB International, Oxon, UK (in press).

  54. Yim MB, Chae HZ, Rhee SG, Chock PB, Stadtman ER: On the protective mechanism of the thiol-specific antioxidant enzyme against the oxidative damage of biomacromolecules. J Biol Chem 269: 1621–1626 (1994).

    Google Scholar 

  55. Zhu D, Scandalios JG: Maize mitochondrial manganese super-oxide dismutases are encoded by a differentially expressed multigene family. Proc Natl Acad Sci USA 90: 9310–9314 (1993).

    Google Scholar 

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Stacy, R.A.P., Munthe, E., Steinum, T. et al. A peroxiredoxin antioxidant is encoded by a dormancy-related gene,Per1, expressed during late development in the aleurone and embryo of barley grains. Plant Mol Biol 31, 1205–1216 (1996). https://doi.org/10.1007/BF00040837

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