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Regulation by biotic and abiotic stress of a wheat germin gene encoding oxalate oxidase, a H2O2-producing enzyme

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Abstract

Germins and germin-like proteins (GLPs) constitute a ubiquitous family of plant proteins that seem to be involved in many developmental and stress-related processes. Wheat germin has been extensively studied at the biochemical level: it is found in the apoplast and the cytoplasm of germinating embryo cells and it has oxalate oxidase activity (EC 1.2.3.4). Germin synthesis can also be induced in adult wheat leaves by auxins and by a fungal pathogen but it remains to be determined whether the same gene is involved in developmental, hormonal and stress response. In this work, we have studied the expression of one of the wheat germin genes, named gf-2.8, in wheat as well as in transgenic tobacco plants transformed with either this intact gene or constructs with GUS driven by its promoter. This has allowed us to demonstrate that expression of this single gene is both developmentally and pathogen- regulated. In addition, we show that expression of the wheat gf-2.8 germin gene is also stimulated by some abiotic stresses, especially the heavy metal ions Cd2+, Cu2+ and Co2+. Several chemicals involved in stress signal transduction pathways were also tested: only polyamines were shown to stimulate expression of this gene. Because regulation of the wheat gf-2.8 germin gene is complex and because its product results in developmental and stress-related release of hydrogen peroxide in the apoplast, it is likely that it plays an important role in several aspects of plant growth and defence mechanisms.

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References

  1. Angelini R, Bragaloni M, Federico R, Infantino A, Porta-Puglia A: Involvement of polyamines, diamine oxidase and peroxidase in resistance of chickpea to Ascochyta rabiei. J Plant Physiol 142: 704–709(1993).

    Google Scholar 

  2. Bäumlein H, Brain H, Kakhovskaya IA, Shutov AD: Seed storage proteins of Spermatophytes share a common ancestor with dessication proteins of Fungi. J Mol Evol 41: 1070–1075 (1995).

    PubMed  Google Scholar 

  3. Berna A: Involvement of residues within putative α helix mo-tifs in the behavior of the alfalfa and tobacco mosaic virus movement proteins. Phytopathology 85: 1441–1448(1995).

    Google Scholar 

  4. Berna A, Bernier F: Regulated expression of a wheat ger-min gene in tobacco: oxalate oxidase activity and apoplastic localization of the heterologous protein. Plant Mol Biol 33: 417–429(1997).

    PubMed  Google Scholar 

  5. Bernier F, Lemieux G, Pallotta D: Gene families encode the major encystment-specific proteins of Physarum poly-cephalum plasmodia. Gene 59: 265–277(1987).

    Google Scholar 

  6. Brain H, Czihal A, Shutov AD, Bäumlein H: A vicilin-like seed protein of cycads: similarity to sucrose binding proteins. Plant Mol Biol 31: 35–44(1996).

    PubMed  Google Scholar 

  7. Daigle N, Lane BG, Bernier F: Expression of the wheat germin promoter in transgenic tobacco plants. In: Cô me D, Corbineai F (eds) Fourth International Workshop on Seeds: Basic and Applied Aspects of Seed Physiology, vol 2, pp. 305–309. ASFIS, Paris (1993).

  8. Domon J-M, Dumas B, Lainé E, Meyer Y, David A, David H: Three glycosylated polypeptides secreted by several em-bryogenic cell cultures of pine show highly specific serolog-ical affinity to antibodies directed against the wheat germin apoprotein monomer. Plant Physiol 108: 141–148(1995).

    PubMed  Google Scholar 

  9. Dumas B, Sailland A, Cheviet J-P, Freyssinet G, Pallett K: Identification of barley oxalate oxidase as a germin-like pro-tein. CR Acad Sci, Life Sci 316: 793–798(1993).

    Google Scholar 

  10. Dumas B, Freyssinet G, Pallett K: Tissue-specific expression of germin-like OxO during development and fungal infection of barley seedlings. Plant Physiol 107: 1091–1096(1995).

    PubMed  Google Scholar 

  11. Dunwell JM:Cupins: A new superfamily of functionally di-verse proteins that include germins and plant storage proteins. Biotech Genet Enging Rev 15: 1–32(1998).

    Google Scholar 

  12. Dunwell JM, Gane PJ: Microbial relatives of seed storage proteins: Conservation of motifs in a functionally diverse superfamily of enzymes. J Mol Evol46: 147–154(1998).

    PubMed  Google Scholar 

  13. Durner J, Shah J, Klessig DF: Salicylic acid and disease resistance in plants. Trends Plant Sci 2: 266–274(1997).

    Google Scholar 

  14. Fodor J, Gullner G, Ádám AL, Barna B, Kömives T, Király Z: Local and systemic responses of antioxidants to tobacco mosaic virus infection and to salicylic acid in tobacco. Plant Physiol 114: 1443–1451(1997).

    PubMed  Google Scholar 

  15. Gallego SM, Benavides MP, Tomaro ML: Effect of heavy metal ion excess on sunflower leaves: evidence for involve-ment of oxidative stress. Plant Sci 121: 151–159(1996).

    Google Scholar 

  16. Galston AW, Kair-Sawhney R, Altabella T, Tiburcio AF: Plant polyamines in reproductive activity and response to abiotic stress. Bot Acta 110: 197–207(1997).

    Google Scholar 

  17. Gane PJ, Dunwell JM, Warwicker J: Modelling based on the structure of vicilins predicts a histidine cluster in the active site of oxalate oxidase. J Mol Evol 46: 488–493(1998).

    PubMed  Google Scholar 

  18. Heintzen C, Fischer R, Melzer S, Kappeler S, Apel K, Staiger D: Circadian oscillations of a transcript encoding a germin-like protein that is associated with cell walls in young leaves of the long-day plant Sinapis alba L. Plant Physiol 106: 905–915 (1994).

    PubMed  Google Scholar 

  19. Hurkman WJ, Lane GB, Tanaka CK: Nucleotide sequence of a transcript encoding a germin-like protein that is present in salt-stressed barley (Hordeum vulgare L.) roots. Plant Physiol 104: 803–804(1994).

    PubMed  Google Scholar 

  20. Hurkman WJ, Tanaka CK: Effect of salt stress on germin gene expression in barley roots. Plant Physiol 110: 971–977(1996).

    PubMed  Google Scholar 

  21. Hurkman WJ, Tanaka CK: Germin gene expression is induced in wheat leaves by powdery mildew infection. Plant Physiol 111: 735–739(1996).

    PubMed  Google Scholar 

  22. Hurkman WJ, Tao HP, Tanaka CK: Germin-like polypeptides increase in barley roots during salt stress. Plant Physiol 97: 366–374(1991).

    Google Scholar 

  23. Kusaba M, Takahashi Y, Nagata T: A multiple-stimuli-responsive as-1-related element of parA gene confers respon-siveness to cadmium but not to copper. Plant Physiol 111: 1161–1167(1996).

    Article  PubMed  Google Scholar 

  24. Lane BG: Cellular dessication and hydration: developmentally regulated proteins, and the maturation and germination of seed embryos. FASEB J 5: 2893–2901(1991).

    PubMed  Google Scholar 

  25. Lane BG: Oxalate, germin, and the extracellular matrix of higher plants. FASEB J 8: 294–301(1994).

    PubMed  Google Scholar 

  26. Lane BG, Bernier F, Dratewka-Kos E, Shafai R, Kennedy TD, Pyne C, Munro JR, Vaighan T, Walters D, Altomare F:Homologies between members of the germin gene fam-ily in hexaploid wheat and similarities between these wheat germins and certain Physarum spherulins. J Biol Chem 266: 10461–10469(1991).

    PubMed  Google Scholar 

  27. Lane BG, Cuming AC, Frégeai J, Carpita NC, Hurkman WH, Bernier F, Dratewka-Kos E, Kennedy TD: Germin isoforms are discrete temporal markers of wheat develop-ment: pseudogermin is a unique thermostable water-soluble oligomeric protein in ungerminated embryos and like germin in germinated embryos it is incorporated into cell wall. Eur J Biochem 209: 961–969(1992).

    PubMed  Google Scholar 

  28. Lane BG, Dunwell JM, Ray JA, Schmitt MR, Cuming AC: Germin, a protein marker of early plant development, is an oxalate oxidase. J Biol Chem 268: 12239–12242(1993).

    PubMed  Google Scholar 

  29. Lane BG, Grzelczak Z, Kennedy T, Kajioka R, Orr J, D'Agostino S, Jaikaran A: Germin: compartmentation of the two forms of the protein by washing growing wheat embryos. Biochem Cell Biol 64: 1025–1037(1986).

    Google Scholar 

  30. Martin-Tanguy J, Negrel J, Paynod M, Martin C: Hydrox-ycinnamic acid amides, hypersensitivity, flowering and sexual organogenesis in plants. Pp. 253–263. In: von Wettstein D, Chua N-H (eds) Plant Molecular Biology, NATO-ASI Series, vol 140. Plenum Press, New York (1987).

    Google Scholar 

  31. McCubbin WC, Kay CM, Kennedy TD, Lane BG: Germin: physiochemical properties of the glycoprotein which signals onset of growth in the germinating wheat embryo. Biochem Cell Biol 65: 1039–1048(1987).

    Google Scholar 

  32. Membré N, Berna A, Neutelings G, David A, David H, Staiger D, Sáez Vásquez J, Raynal M, Delseny M, Bernier F: cDNA sequence, genomic organization and differential expression of three Arabidopsis genes for germin/oxalate oxidase-like proteins. Plant Mol Biol 35: 459–469(1997).

    PubMed  Google Scholar 

  33. Membré N, Bernier F: The rice genome contains at least six different genes for oxalate oxidase/germin-like proteins (GenBank AF032971, AF032972, AF032973, AF032974, AF032975, AF032976) (PGR98–021). Plant Physiol 116: 868 (1998).

    Google Scholar 

  34. Michalowski CB, Bohnert HJ: Nucleotide sequence of a root-specific transcript encoding a germin-like protein from the halophyte Mesembryanthemum crystallinum. Plant Physiol 100: 537–538(1992).

    Google Scholar 

  35. Olson PD, Varner JE: Hydrogen peroxide and lignification. Plant J 4: 887–892(1993).

    Google Scholar 

  36. Ono M, Sage-Ono K, Inoue M, Kamada H, Harada H: Tran-sient increase in the level of mRNA for a germin-like protein in leaves of the short-day plant Pharbitis nil during the pho-toinduction of flowering. Plant Cell Physiol 37: 855–861 (1996).

    PubMed  Google Scholar 

  37. Schaffrath U, Freydl E, Dudler R: Evidence for different sig-naling pathways activated by inducers of acquired resistance in wheat. Mol Plant-Microbe Inter. 10: 779–783(1997).

    Google Scholar 

  38. Shutov AD, Brain H, Chesnokov YV, Bäumlein H: A gene encoding a vicilin-like protein is specifically expressed in fern spores. Evolutionary pathway of seed storage globulins. Eur J Biochem 252: 79–89(1998).

    PubMed  Google Scholar 

  39. Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB: Sub-cellular localization of H 2 O 2 in plants. H 2 O 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11: 1187–1194(1997).

    Google Scholar 

  40. Ulmasov T, Hagen G, Guilfoyle T: The ocs element in the soybean GH2/4 promoter is activated by both active and in-active aixin and salicylic acid analogues. Plant Mol Biol 26: 1055–1064(1994).

    PubMed  Google Scholar 

  41. Weckx JEJ, Clijsters HMM: Oxidative damage and defense mechanisms in primary leaves of Phaseolus vulgaris as a re-sult of root assimilation of toxic amounts of copper. Physiol Plant 96: 506–512(1996).

    Google Scholar 

  42. Wei Y, Zhang Z, Andersen CH, Schmelzer E, Gregersen PL, Collinge DB, Smedegaard-Petersen V, Thordal-Christensen H: An epidermis/papilla-specific oxalate oxidase-like protein in the defence response of barley attacked by the powdery mildew fungus. Plant Mol Biol 36: 101–112(1998).

    PubMed  Google Scholar 

  43. Zhang Z, Collinge DB, Thordal-Christensen H: Germin-like OxO, a H 2 O 2-producing enzyme, accumulates in barley at-tacked by the powdery mildew fungus. Plant J 8: 139–145 (1995).

    Google Scholar 

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  1. Institut de Biologie Moléculaire des Plantes, Institut de Botanique, 28 rue Goethe, 67083, Strasbourg Cedex, France

    Anne Berna & François Bernier

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  1. Anne Berna
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  2. François Bernier
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Berna, A., Bernier, F. Regulation by biotic and abiotic stress of a wheat germin gene encoding oxalate oxidase, a H2O2-producing enzyme. Plant Mol Biol 39, 539–549 (1999). https://doi.org/10.1023/A:1006123432157

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