Journal of Molecular Modeling

, Volume 16, Issue 5, pp 919–928

Evaluation of the impact of functional diversification on Poaceae, Brassicaceae, Fabaceae, and Pinaceae alcohol dehydrogenase enzymes

  • Claudia E. Thompson
  • Cláudia L. Fernandes
  • Osmar Norberto de Souza
  • Loreta B. de Freitas
  • Francisco M. Salzano
Original Paper

Abstract

The plant alcohol dehydrogenases (ADHs) have been intensively studied in the last years in terms of phylogeny and they have been widely used as a molecular marker. However, almost no information about their three-dimensional structure is available. Several studies point to functional diversification of the ADH, with evidence of its importance, in different organisms, in the ethanol, norepinephrine, dopamine, serotonin, and bile acid metabolism. Computational results demonstrated that in plants these enzymes are submitted to a functional diversification process, which is reinforced by experimental studies indicating distinct enzymatic functions as well as recruitment of specific genes in different tissues. The main objective of this article is to establish a correlation between the functional diversification occurring in the plant alcohol dehydrogenase family and the three-dimensional structures predicted for 17 ADH belonging to Poaceae, Brassicaceae, Fabaceae, and Pinaceae botanical families. Volume, molecular weight and surface areas are not markedly different among them. Important electrostatic and pI differences were observed with the residues responsible for some of them identified, corroborating the function diversification hypothesis. These data furnish important background information for future specific structure-function and evolutionary investigations.

Keywords

ADH Alcohol dehydrogenase Functional diversification Molecular evolution Molecular modeling Protein structure 

Supplementary material

894_2009_576_MOESM1_ESM.doc (114 kb)
Table 1S(DOC 158 kb)
894_2009_576_MOESM2_ESM.doc (109 kb)
Table 2S(DOC 114 kb)
894_2009_576_MOESM3_ESM.doc (103 kb)
Table 3S(DOC 109 kb)
894_2009_576_MOESM4_ESM.doc (118 kb)
Table 4S(DOC 103 kb)
894_2009_576_MOESM5_ESM.doc (48 kb)
Table 5S(DOC 118 kb)
894_2009_576_MOESM6_ESM.doc (68 kb)
Fig. 1SMultiple alignment of the protein sequences modeled and the template used in the modeling (DOC 47 kb)
894_2009_576_MOESM7_ESM.doc (30 kb)
Fig. 2SPercent identity of the ADH sequences. The horizontal axis presents the data values being plotted. The vertical axis shows the fraction of data points with as small or smaller a data value (DOC 67 kb)
894_2009_576_MOESM8_ESM.doc (94 kb)
Fig. 3S3D_1D averaged scores, as determined by the VERIFY_3D program for the models of the Brassicaceae botanical family (DOC 30 kb)
894_2009_576_MOESM9_ESM.doc (170 kb)
Fig. 4S3D_1D averaged scores, as determined by the VERIFY_3D program for the models of the Poaceae botanical family (DOC 94 kb)
894_2009_576_MOESM10_ESM.doc (158 kb)
Fig. 5S3D_1D averaged scores, as determined by the VERIFY_3D program for the models of the Fabaceae and Pinaceae botanical families (DOC 169 kb)

References

  1. 1.
    Höög JO, Hedberg JJ, Stromberg P, Svesson S (2001) Mammalian alcohol dehydrogenase – functional and structural implications. J Biomed Sci 8:71–76CrossRefGoogle Scholar
  2. 2.
    Boleda MD, Saubi N, Farrés J, Parés X (1993) Physiological substrates for rat alcohol dehydrogenase classes: aldehydes of lipid peroxidation, omega-hydroxyfatty acids, and retinoids. Arch Biochem Biophys 307:85–90CrossRefGoogle Scholar
  3. 3.
    Martras S, Alvarez R, Martinez SE, Torres D, Gallego O, Duester G, Farrés J, de Lera AR, Parés X (2004) The specificity of alcohol dehydrogenase with cis-retinoids. Activity with 11-cis-retinol and localization in retina. Eur J Biochem 271:1660–1670CrossRefGoogle Scholar
  4. 4.
    Garabagi F, Duns G, Strommer J (2005) Selective recruitment of Adh genes for distinct enzymatic functions in Petunia hybrid. Plant Mol Biol 58:283–294CrossRefGoogle Scholar
  5. 5.
    Eklund H, Bränden CI (1979) Structural differences between apo- and holoenzyme of horse liver alcohol dehydrogenae. J Biol Chem 254:3458–3461Google Scholar
  6. 6.
    Danielsson O, Atrian S, Luque T, Hjelmqvist L, Gonzalez-Duarte R, Jörnvall H (1994) Fundamental molecular differences between alcohol dehydrogenase classes. Proc Natl Acad Sci USA 91:4980–4984CrossRefGoogle Scholar
  7. 7.
    Persson B, Bergman T, Keung WM, Waldenström U, Holmquist B, Vallee BL, Jörnvall H (1994) Structural and functional divergence of class II alcohol dehydrogenase – cloning and characterisation of rabbit liver isoforms of the enzyme. Eur J Biochem 216:49–56CrossRefGoogle Scholar
  8. 8.
    Chang C, Meyerowitz EM (1986) Molecular cloning and DNA sequence of the Arabidopsis thaliana alcohol dehydrogenase gene. Proc Natl Acad Sci USA 83:1408–1412CrossRefGoogle Scholar
  9. 9.
    Gaut BS, Clegg MT (1993) Molecular evolution of the Adh1 locus in the genus Zea. Proc Natl Acad Sci USA 90:5095–5099CrossRefGoogle Scholar
  10. 10.
    Perry DJ, Furnier GR (1996) Pinus banksiana has at least seven expressed alcohol dehydrogenase genes in two linked groups. Proc Natl Acad Sci USA 93:13020–13023CrossRefGoogle Scholar
  11. 11.
    Morton BR, Gaut BS, Clegg MT (1996) Evolution of alcohol dehydrogenase genes in the palm and grass families. Proc Natl Acad Sci USA 93:11735–11739CrossRefGoogle Scholar
  12. 12.
    Miyashita NT, Kawabe A, Innan H, Terauchi R (1998) Intra- and interspecific DNA variation and codon bias of the alcohol dehydrogenase (Adh) locus in Arabis and Arabidopsis species. Mol Biol Evol 15:1420–1429Google Scholar
  13. 13.
    Charleswort D, Liu FL, Zhang L (1998) The evolution of the alcohol dehydrogenase gene family by loss of introns in plants of the genus Leavenworthia (Brassicaceae). Mol Biol Evol 15:552–559Google Scholar
  14. 14.
    Gaut BS, Peek AS, Morton BR, Clegg MT (1999) Patterns of genetic diversification within the Adh gene family in the grasses (Poaceae). Mol Biol Evol 16:1086–1097Google Scholar
  15. 15.
    Koch MA, Haubold B, Mitchell-Olds T (2000) Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidospis, Arabis and related genera (Brassicaceae). Mol Biol Evol 17:1483–1498Google Scholar
  16. 16.
    Lin J-Z, Brown AHD, Clegg MT (2001) Heterogeneous geographic patterns of nucleotide sequence diversity between two alcohol dehydrogenase genes in wild barley (Hordeum vulgare subspecies spontaneum). Proc Natl Acad Sci USA 98:531–536CrossRefGoogle Scholar
  17. 17.
    Dolferus R, Jacobs M, Peacock WJ, Dennis ES (1994) Differential interactions of promoter elements in stress responses of the Arabidopsis Adh gene. Plant Physiol 105:1075–1087CrossRefGoogle Scholar
  18. 18.
    Martí-Renom MA, Stuart AC, Fiser A, Sánchez R, Melo F, Sali A (2000) Comparative protein structure modeling of genes and genomes. Annu Rev Biophys Biomol Struct 29:291–325CrossRefGoogle Scholar
  19. 19.
    Bucher M, Brander KA, Sbicego S, Mandel T, Kuhlemeier C (1995) Aerobic fermentation in tobacco pollen. Plant Mol Biol 28:739–750CrossRefGoogle Scholar
  20. 20.
    Zhang M, Maeda Y, Furihata Y, Nakamaru Y, Esashi Y (1994) A mechanism of seed deterioration in relation to the volatile compounds evolved by dry seeds themselves. Seed Sci Res 4:49–56CrossRefGoogle Scholar
  21. 21.
    Zhang M, Yajima H, Umezawa Y, Nakagawa Y, Esashi Y (1995) GC-MS identification of volatile compounds evolved by dry seeds in relation to storage conditions. Seed Sci Technol 23:59–68Google Scholar
  22. 22.
    Zhang M, Nakamaru Y, Tsuda S, Nagashima T, Esashi Y (1995) Enzymatic conversion of volatile metabolites in dry seeds during storage. Plant Cell Physiol 36:157–164Google Scholar
  23. 23.
    Zhang M, Nagata S, Miyazawa K, Kikuchi H, Esashi Y (1997) A competitive enzyme-linked immunosorbent assay to quantify acetaldehyde-protein adducts that accumulate in dry seed during aging. Plant Physiol 113:397–402CrossRefGoogle Scholar
  24. 24.
    Van Eldik GJ, Ruiter RK, Van Herpen MMA, Schrauwen JAM, Wullems GJ (1997) Induced ADH gene expression and enzyme activity in pollinated pistils of Solanum tuberosum. Sex Plant Reprod 10:107–109CrossRefGoogle Scholar
  25. 25.
    Thompson CE, Salzano FM, Souza ON, Freitas LB (2007) Sequence and structural aspects of the functional diversification of plant alcohol dehydrogenases. Gene 396:108–115CrossRefGoogle Scholar
  26. 26.
    Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405CrossRefGoogle Scholar
  27. 27.
    Nicholas KB, Nicholas HB Jr (1997) GeneDoc: a tool for editing and annotating multiple sequence alignment. Distributed by the authors (www.psc.edu/biomed/genedoc)
  28. 28.
    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410Google Scholar
  29. 29.
    Altschul SF, Madden TL, Schaffer AA, Zhang JZ, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefGoogle Scholar
  30. 30.
    Rubach JK, Plapp BV (2003) Amino acid residues in the nicotinamide binding site contribute to catalysis by horse liver alcohol dehydrogenase. Biochemistry 42:2907–2915CrossRefGoogle Scholar
  31. 31.
    Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalty and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefGoogle Scholar
  32. 32.
    Henikoff S, Henikoff JG (1992) Amino acid substitution matrices from protein blocks. Proc Natl Acad Sci USA 89:10915–10919CrossRefGoogle Scholar
  33. 33.
    Sali A, Blundell TL (1993) Comparative protein modeling by satisfaction of spatial restraints. J Mol Biol 243:779–815CrossRefGoogle Scholar
  34. 34.
    Laskowski RA, McArthur MW, Moss DS, Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26:283–291CrossRefGoogle Scholar
  35. 35.
    Lüthy R, Bowie JU, Eisenberg D (1992) Assessment of protein models with three-dimensional profiles. Nature 356:83–85CrossRefGoogle Scholar
  36. 36.
    Gattiker A, Gasteiger E, Bairoch A (2002) ScanProsite: a reference implementation of a PROSITE scanning tool. Appl Bioinformat 1:107–108Google Scholar
  37. 37.
    Richards FM (1974) The interpretation of protein structures: total volume, group volume distributions and packing density. J Mol Biol 82:1–14CrossRefGoogle Scholar
  38. 38.
    Richards FM (1977) Areas, volumes, packing and protein structure. Annu Rev Biophys Bioeng 6:151–176CrossRefGoogle Scholar
  39. 39.
    Voss NR (2006) The geometry of the ribosomal polypeptide exit tunnel. J Mol Biol 360:893–906CrossRefGoogle Scholar
  40. 40.
    Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy Server. In: Walker JM (ed) The proteomics protocols handbook. Humana Press, Totowa, pp 571–607CrossRefGoogle Scholar
  41. 41.
    Guex N, Peitsch MC (1997) SWISS-MODEL and Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2733CrossRefGoogle Scholar
  42. 42.
    Gu X (2001) Mathematical modeling for functional divergence after gene duplication. J Comp Biol 3:221–234CrossRefGoogle Scholar
  43. 43.
    Gu X, Vander Velden K (2002) DIVERGE: phylogeny-based analysis for functional-structural divergence of a protein family. Bioinformatics 18:500–501CrossRefGoogle Scholar
  44. 44.
    Small RL, Wendel JF (2000) Copy number lability and evolutionary dynamics of the Adh gene family in diploid and tetraploid cotton (Gossypium). Genetics 155:1913–1926Google Scholar
  45. 45.
    Schwartz D, Laughner WJ (1969) A molecular basis for heterosis. Science 166:626–627CrossRefGoogle Scholar
  46. 46.
    Freeling M, Bennet DC (1985) Maize Adh 1. Annu Rev Genet 19:297–323Google Scholar
  47. 47.
    Gemma S, Vichi S, Testai E (2006) Individual susceptibility and alcohol effects: biochemical and genetic aspects. Ann Ist Super Sanità 42:8–16Google Scholar
  48. 48.
    Lesk AM (1995) NAD-binding domains of dehydrogenases. Curr Opin Struct Biol 5:775–783CrossRefGoogle Scholar
  49. 49.
    Baker PJ, Britton KL, Fisher M, Esclapez J, Pire C, Bonete MJ, Ferrer J, Rice DW (2008) Active site dynamics in the zinc-dependent medium chain alcohol dehydrogenase superfamily. PNAS 106:779–784CrossRefGoogle Scholar
  50. 50.
    Valeyev NV, Downing AK, Sondek J, Deane C (2008) Electrostatic and functional analysis of the seven-bladed WD β-Propellers. Evol Bioinform 4:203–216Google Scholar
  51. 51.
    Jorrín JV, Maldonado AM, Castillejo MA (2007) Plant proteome analysis: a 2006 update. Proteomics 7:2947–2962CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Claudia E. Thompson
    • 1
  • Cláudia L. Fernandes
    • 2
  • Osmar Norberto de Souza
    • 2
  • Loreta B. de Freitas
    • 1
  • Francisco M. Salzano
    • 1
  1. 1.Departamento de Genética, Instituto de BiociênciasUniversidade Federal do Rio Grande do SulPorto AlegreBrazil
  2. 2.Laboratório de Bioinformática, Modelagem e Simulação de Biossistemas, Faculdade de InformáticaPontifícia Universidade Católica do Rio Grande do SulPorto AlegreBrazil

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