Plant Molecular Biology

, Volume 34, Issue 6, pp 843–854

Maize glutathione-dependent formaldehyde dehydrogenase cDNA: a novel plant gene of detoxification

  • Judith Fliegmann
  • Heinrich SandermannJr.
Article

Abstract

We have previously shown that intact plants and cultured plant cells can metabolize and detoxify formaldehyde through the action of a glutathione-dependent formaldehyde dehydrogenase (FDH), followed by C-1 metabolism of the initial metabolite (formic acid). The cloning and heterologous expression of a cDNA for the glutathione-dependent formaldehyde dehydrogenase from Zea mays L. is now described. The functional expression of the maize cDNA in Escherichia coli proved that the cloned enzyme catalyses the NAD+- and glutathione (GSH)-dependent oxidation of formaldehyde. The deduced amino acid sequence of 41 kDa was on average 65% identical with class III alcohol dehydrogenases from animals and less than 60% identical with conventional plant alcohol dehydrogenases (ADH) utilizing ethanol. Genomic analysis suggested the existence of a single gene for this cDNA. Phylogenetic analysis supports the convergent evolution of ethanol-consuming ADHs in animals and plants from formaldehyde-detoxifying ancestors. The high structural conservation of present-day glutathione-dependent FDH in microorganisms, plants and animals is consistent with a universal importance of these detoxifying enzymes.

alcohol dehydrogenase enzyme evolution formaldehyde detoxification glutathione-dependent formaldehyde dehydrogenase heterologous expression 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Anonymous: Environmental Health Criteria 89: Formaldehyde. World Health Organization, Geneva (1989).Google Scholar
  2. 2.
    Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K: Current Protocols in Molecular Biology, 1987-1988. John Wiley, New York (1987).Google Scholar
  3. 3.
    Barber RD, Rott MA, Donohue TJ: Characterization of a glutathione-dependent formaldehyde dehydrogenase from Rhodobacter sphaeroides. J Bact 178: 1386-1393 (1996).PubMedGoogle Scholar
  4. 4.
    Danielsson O, Atrian S, Luque T, Hjelmqvist L, Gonzälez-Duarte R, Jörnvall H: Fundamental molecular differences between alcohol dehydrogenase classes. Proc Natl Acad Sci USA 91: 4980-4984 (1994).PubMedGoogle Scholar
  5. 5.
    Danielsson O, Shafquat J, Estonius M, Jörnvall H: Alcohol dehydrogenase class III contrasted to class I. Eur J Biochem 225: 1081-1088 (1994).PubMedGoogle Scholar
  6. 6.
    Danielsson O, Jörnvall H: ‘Enzymogenesis’: classical liver alcohol dehydrogenase originate from the glutathionedependent formaldehyde dehydrogenase line. Proc Natl Acad Sci USA 89: 9247-9251 (1992).PubMedGoogle Scholar
  7. 7.
    Das OP, Cruz-Alvarez M, Chaudhuri S, Messing J: Molecular methods for genetic analysis of maize. Meth Mol Cell Biol 1: 213-222 (1990).Google Scholar
  8. 8.
    Dellaporta S: Plant DNA miniprep and microprep: versions 2.1-2.3. In: Freeling M, Walbot V (eds) The Maize Handbook, pp. 522-525. Springer-Verlag, New York (1994).Google Scholar
  9. 9.
    Dennis ES, Sachs MM, Gerlach WL, Finnegan EJ, Peacock WJ: Molecular analysis of the alcohol dehydrogenase 2 (Adh2) gene of maize. Nucl Acids Res 13: 727-743 (1985).PubMedGoogle Scholar
  10. 10.
    Eklund H, Brändén C-I, Jörnvall H: Structural comparisons of mammalian, yeast and bacillar alcohol dehydrogenases. J Mol Biol 102: 61-73 (1976).PubMedGoogle Scholar
  11. 11.
    Eklund H, Nordström B, Zeppezauer E, Söderlund G, Ohlson I, Boiwe T, Söderberg B-O, Tapia O, Brändén C-I: Threedimensional structure of horse liver alcohol dehydrogenase at 2.4 Å resolution. J Mol Biol 102: 27-59 (1976).PubMedGoogle Scholar
  12. 12.
    Eklund H, Müller-Wille P, Horjales E, Futer O, Holmquist B, Vallee BL, Höög J-O, Kaiser R, Jörnvall H: Comparison of three classes of human liver alcohol dehydrogenase. Eur J Biochem 193: 303-310 (1990).PubMedGoogle Scholar
  13. 13.
    Elliston K, Messing J: In: Kahl G (ed) The Architecture of Eukaryotic Genes, pp. 21-56. Verlag Chemie, Weinheim (1988).Google Scholar
  14. 14.
    Engeland K, Höög J-O, Holmquist B, Estonius M, Jörnvall H, Vallee BL: Mutation of Arg-115 of human class III alcohol dehydrogenase: a binding site required for formaldehyde dehydrogenase activity and fatty acid activation. Proc Natl Acad Sci USA 90: 2491-2494 (1993).PubMedGoogle Scholar
  15. 15.
    Estonius M, Danielsson O, Karlsson C, Persson H, Jörnvall H, Höög J-O: Distribution of alcohol and sorbitol dehydrogenases. Eur J Biochem 215: 497-503 (1993).PubMedGoogle Scholar
  16. 16.
    Estonius M, Höög J-O, Danielsson O, Jörnvall H: Residues specific for class III alcohol dehydrogenase. Site-directed mutagenesis of the human enzyme. Biochemistry 33: 15080-15085 (1994).PubMedGoogle Scholar
  17. 17.
    Fernández MR, Biosca JA, Norin A, Jörnvall H, Parés X: Class III alcohol dehydrogenase from Saccharomyces cerevisiae: structural and enzymatic features differ toward the human/mammalian forms in a manner consistent with functional needs in formaldehyde detoxication. FEBS Lett 370: 23-26 (1995).CrossRefPubMedGoogle Scholar
  18. 18.
    Fernández MR, Jörnvall H, Moreno A, Kaiser R, Parés X: Cephalopod alcohol dehydrogenase: purification and enzymatic characterization. FEBS Lett 328: 235-238 (1993).CrossRefPubMedGoogle Scholar
  19. 19.
    Frohman MA, Dush MK, Martin GR: Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci USA 85: 8998-9002 (1988).PubMedGoogle Scholar
  20. 20.
    Garvin DF, Weeden NF, Doyle JJ: The reduced stability of a plant alcohol dehydrogenase is due to the substitution of serine for a highly conserved phenylalanine residue. Plant Mol Biol 26: 643-655 (1994).CrossRefPubMedGoogle Scholar
  21. 21.
    Gerlach WL, Pryor AJ, Dennis ES, Ferl RJ, Sachs MM, Peacock WJ: cDNA cloning and induction of the alcohol dehydrogenase gene (Adh1) of maize. Proc Natl Acad Sci USA 79: 2981-2985 (1982).Google Scholar
  22. 22.
    Giese M, Bauer-Doranth U, Langebartels C, Sandermann H Jr.: Detoxification of formaldehyde by the spider plant (Chlorophytum comosumL.) and by soybean (Glycine maxL.) cellsuspension cultures. Plant Physiol 104: 1301-1309 (1994).PubMedGoogle Scholar
  23. 23.
    Glasner JD, Kocher TD, Collins JJ: Caenorhabditis eleganscontains genes encoding two new members of the Zncontaining alcohol dehydrogenase family. J Mol Evol 41: 46- 53 (1995).CrossRefPubMedGoogle Scholar
  24. 24.
    Gömpel-Klein P, Mack M, Brendel M: Molecular characterization of the two genes SNQ and SFA that confer hyperresistance to 4-nitroquinoline-N-oxide and formaldehyde in Saccharomyces cerevisiae. Curr Genet 16: 65-74 (1989).PubMedGoogle Scholar
  25. 25.
    Gotttlieb LD: Conservation and duplication of isozymes in plants. Science 216: 373-380 (1982).Google Scholar
  26. 26.
    Gutheil WG, Holmquist B, Vallee BL: Purification, characterization, and partial sequence of the glutathione-dependent formaldehyde dehydrogenase from Escherichia coli: a class III alcohol dehydrogenase. Biochemistry 31: 475-481 (1992).PubMedGoogle Scholar
  27. 27.
    Hjelmqvist L, Hackett M, Shafqat J, Danielsson O, Iida J, Hendrickson RC, Michel H, Shabanowitz J, Hunt DF, Jörnvall H: Multiplicity of N-terminal structures of mediumchain alcohol dehydrogenases. FEBS Lett 367: 237-240 (1995).CrossRefPubMedGoogle Scholar
  28. 28.
    Hjelmqvist L, Shafquat J, Rehman SA, Jörnvall H: Alcohol dehydrogenase of class III: consistent patterns of structural and functional conservation in relation to class I and other proteins. FEBS Lett 373: 212-216 (1995).CrossRefPubMedGoogle Scholar
  29. 29.
    Holmquist B, Moulis J-M, Engeland K, Vallee BL: Role of arginine 115 in fatty acid activation and formaldehyde dehydrogenase activity of human class III alcohol dehydrogenase. Biochemistry 32: 5139-5144 (1993).PubMedGoogle Scholar
  30. 30.
    Hunt AG: Messenger RNA 3′ end formation in plants. Annu Rev Plant Phys Plant Mol Biol 45: 47-60 (1994).Google Scholar
  31. 31.
    Hur M-W, Edenberg HJ: Cloning and characterization of the ADH5 gene encoding human alcohol dehydrogenase 5, formaldehyde dehydrogenase. Gene 121: 305-311 (1992).CrossRefPubMedGoogle Scholar
  32. 32.
    Jörnvall H, Höög J-O: Nomenclature of alcohol dehydrogenases. Alcohol Alcoholism 30: 153-161 (1995).Google Scholar
  33. 33.
    Kaiser R, Fernández MR, Parés X, Jörnvall H: Origin of the human alcohol dehydrogenase system: Implications from the structure and properties of the octopus protein. Proc Natl Acad Sci USA 90: 11222-11226 (1993).PubMedGoogle Scholar
  34. 34.
    Komoßa D, Gennity I, Sandermann H Jr.: Plant metabolism of herbicides with C-P bonds: glyphosate. Pestic Biochem Physiol 43: 85-94 (1992).Google Scholar
  35. 35.
    Mason RP, Sanders JKM, Crawford A, Hunter BK: Formaldehyde metabolism by Escherichia coli. Detection by in vivo 13C NMR spectroscopy of S-(hydroxymethyl) glutathione as a transient intracellular intermediate. Biochemistry 25: 4504- 4507 (1986).PubMedGoogle Scholar
  36. 36.
    Pryor A, Huppatz JL: Purification of maize alcohol dehydrogenase and competitive inhibition by pyrazoles. Biochem Int 4: 431-438 (1982).Google Scholar
  37. 37.
    Ras J, Van Ophem PW, Reijenders WNM, Van Spanning RJM, Duine JA, Stouthamer AH, Harms N: Isolation, sequencing, and mutagenesis of the gene encoding NAD-and glutathionedependent formaldehyde dehydrogenase (GD-FALDH) from Paracoccus denitrificans, in which GD-FALDH is essential for methylotrophic growth. J Bact 177: 247-251 (1994).Google Scholar
  38. 38.
    Sachs MM, Dennis ES, Gerlach WL, Peacock WJ: Two alleles of maize alcohol dehydrogenase 1have 3′ structural and poly(A) addition polymorphisms. Genetics 113: 449-467 (1986).Google Scholar
  39. 39.
    Sachs MM, Freeling M, Okimoto R: The anaerobic proteins of maize. Cell 20: 761-767 (1980).PubMedGoogle Scholar
  40. 40.
    Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).Google Scholar
  41. 41.
    Sandermann H Jr.: Higher plantmetabolism of xenobiotics: the ‘green liver’ concept. Pharmacogenetics 4: 225-241 (1994).PubMedGoogle Scholar
  42. 42.
    Sasnauskas K, Jomantiene R, Januska A, Lebediene E, Lebedys J, Janulaitis A: Cloning and analysis of a Candida maltosagene which confers resistance to formaldehyde in Saccharomyces cerivisiae. Gene 122: 207-211 (1992).CrossRefPubMedGoogle Scholar
  43. 43.
    Schröder J, Kreuzaler F, Schäfer E, Hahlbrock K: Concomitant induction of phenylalanine ammonia-lyase and flavanone synthase mRNAs in irradiated plant cells. J Biol Chem 254: 57-65 (1979).PubMedGoogle Scholar
  44. 44.
    Shafqat J, El-Ahmad M, Danielsson O, Martínez MC, Persson B, Parés X, Jörnvall H: Pea formaldehyde-active class III alcohol dehydrogenase: common derivation of the plant and animal forms but not of the corresponding ethanol-active forms (classes I and P). Proc Natl Acad Sci USA 93: 5595- 5599 (1996).CrossRefPubMedGoogle Scholar
  45. 45.
    Strittmatter P, Ball EG: Formaldehyde dehydrogenase, a glutathione-dependent enzyme system. J Biol Chem 213: 445- 461 (1955).PubMedGoogle Scholar
  46. 46.
    Thompson JD, Higgins DG, Gibson TJ: Clustal W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nuc Acids Res 22: 4673-4680 (1994).Google Scholar
  47. 47.
    Uotila L, Koivusalo M: Purification of formaldehyde and formate dehydrogenases from pea seeds by affinity chromatography and S-formylglutathione as the intermediate of formaldehyde metabolism. Arch Biochem Biophys 196: 33-45 (1979).PubMedGoogle Scholar
  48. 48.
    Uotila L, Koivusalo M: Formaldehyde dehydrogenase. In: Larsson A, Orrenius S, Holmgren A, Mannervik B (eds), Functions of Glutathione: Biochemical, Physiological, Toxicological and Clinical Aspects, pp. 175-186. Raven Press, New York (1983).Google Scholar
  49. 49.
    Uotila L, Koivusalo M: Glutathione-dependent oxidoreductases: formaldehyde dehydrogenase. In: Dolphin D, Poulson R, Avramovic O (eds) Coenzymes and Cofactors, Vol. III. Glutathione, pp. 517-551. John Wiley, New York (1989).Google Scholar
  50. 50.
    Wehner EP, Rao E, Brendel M: Molecular structure and genetic regulation of SFA, a gene responsible for resistance to formaldehyde in Saccharomyces cerevisiae, and characterization of its gene product. Mol Gen Genet 237: 351-358 (1993).PubMedGoogle Scholar
  51. 51.
    Yokoyama S, Harry DE: Molecular phylogeny and evolutionary rates of alcohol dehydrogenases in vertebrates and plants. Mol Biol Evol 10: 1215-1226 (1993).PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1997

Authors and Affiliations

  • Judith Fliegmann
    • 1
  • Heinrich SandermannJr.
    • 1
  1. 1.GSF – Forschungszentrum für Umwelt und GesundheitInstitut für Biochemische PflanzenpathologieOberschleissheimGermany
  2. 2.Botanisches Institut der UniversitätMünchenGermany

Personalised recommendations