Skip to main content

Duplicated Gene Evolution of the Primate Alcohol Dehydrogenase Family

  • Chapter
  • First Online:
Post-Genome Biology of Primates

Part of the book series: Primatology Monographs ((PrimMono))

Abstract

The mammalian alcohol dehydrogenase (ADH: EC1.1.1.1) enzymes metabolize a wide range of alcohol and carbonyl compounds. The ADH enzyme family is classified into five classes (I–V) based on biochemical properties and nucleotide/amino acid sequence similarity. Each class of ADH shares 60–70% sequence similarity with other classes of ADH in the same species, and ADHs within the same class in the same species share more than 80% sequence similarity. The high similarity among ADHs suggests that their genes have evolved by multiple duplications. Previous studies based on Southern hybridization data have identified copy number variation of Class I ADH genes in mammals: the mouse has only one Class I gene, some other mammals have two genes, whereas all primates examined have at least three Class I genes. Our previous study showed that great apes (human, chimpanzee, bonobo, gorilla, orangutan) and Old World monkeys (baboon) have three or more Class I genes that have evolved independently, escaping from homogenization by gene conversion. In this review, we revisit the puzzle of the copy number variation in the primate ADH gene family by searching the literature and genome databases and propose a hypothesis that the primate frugivorous behavior has maintained the duplicated genes because of the necessity of digesting ethanol generated by fermentation of fruit sugar.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

ADH:

Alcohol dehydrogenase

ALDH:

Aldehyde dehydrogenase

BP:

Before present

cDNA:

Complementary DNA

kb:

Kilobase pairs

Km :

Inverse of enzyme affinity

mRNA:

Messenger RNA

My:

Million years

NWM:

New World monkey

OWM:

Old World monkey

PCR:

Polymerase chain reaction

WGS:

Whole genome sequencing

References

  • Barth G, Kunkel W (1979) Alcohol dehydrogenase (ADH) in yeasts. II. NAD  +  −and NADP  +  −dependent alcohol dehydrogenases in Saccharomycopsis lipolytica. Z Allg Mikrobiol 19:381–390

    Article  PubMed  CAS  Google Scholar 

  • Canestro C, Hjelmqvist L, Albalat R et al (2000) Amphioxus alcohol dehydrogenase is a class 3 form of single type and of structural conservation but with unique developmental expression. Eur J Biochem 267:6511–6518

    Article  PubMed  CAS  Google Scholar 

  • Cavalli-Sforza LL, Edwards AW (1967) Phylogenetic analysis. Models and estimation procedures. Am J Hum Genet 19:233–257

    PubMed  CAS  Google Scholar 

  • Ceci JD, Zheng YW, Felder MR (1987) Molecular analysis of mouse alcohol dehydrogenase: nucleotide sequence of the Adh-1 gene and genetic mapping of a related nucleotide sequence to chromosome 3. Gene 59:171–182

    Article  PubMed  CAS  Google Scholar 

  • Chen YC, Peng GS, Tsao TP et al (2009) Pharmacokinetic and pharmacodynamic basis for overcoming acetaldehyde-induced adverse reaction in Asian alcoholics, heterozygous for the variant ALDH2*2 gene allele. Pharmacogenet Genomics 19:588–599

    Article  PubMed  CAS  Google Scholar 

  • Cheung B, Holmes RS, Easteal S et al (1999) Evolution of class I alcohol dehydrogenase genes in catarrhine primates: gene conversion, substitution rates, and gene regulation. Mol Biol Evol 16:23–36

    PubMed  CAS  Google Scholar 

  • Dudelly R (2002) Fermenting fruit and the historical ecology of ethanol ingestion: is alcoholism in modern humans an evolutionary hangover? Addiction 97:381–388

    Article  Google Scholar 

  • Dudelly R (2004) Ethanol, fruit ripening, and the historical origins of human alcoholism in primate frugivory. Integr Comp Biol 44:315–323

    Article  Google Scholar 

  • Duester G, Smith M, Bilanchone V et al (1986) Molecular analysis of the human class I alcohol dehydrogenase gene family and nucleotide sequence of the gene encoding the beta subunit. J Biol Chem 261:2027–2033

    PubMed  CAS  Google Scholar 

  • Eklund H, Branden CI, Jornvall H (1976a) Structural comparisons of mammalian, yeast and bacillar alcohol dehydrogenases. J Mol Biol 102:61–73

    Article  PubMed  CAS  Google Scholar 

  • Eklund H, Nordstrom B, Zeppezauer E et al (1976b) Three-dimensional structure of horse liver alcohol dehydrogenase at 2–4 Ǻ resolution. J Mol Biol 102:27–59

    Article  PubMed  CAS  Google Scholar 

  • Engeland K, Maret W (1993) Extrahepatic, differential expression of four classes of human alcohol dehydrogenase. Biochem Biophys Res Commun 193:47–53

    Article  PubMed  CAS  Google Scholar 

  • Fischer JA, Maniatis T (1985) Structure and transcription of the Drosophila mulleri alcohol dehydrogenase genes. Nucleic Acids Res 13:6899–6917

    Article  PubMed  CAS  Google Scholar 

  • Fleagle JG (1999) Primate adaptation and evolution. Academic, London

    Google Scholar 

  • Funkenstein B, Jakowlew SB (1996) Molecular cloning of fish alcohol dehydrogenase cDNA (Amst). Gene 174:159–164

    Article  PubMed  CAS  Google Scholar 

  • Guagliardi A, Martino M, Iaccarino I et al (1996) Purification and characterization of the alcohol dehydrogenase from a novel strain of Bacillus stearothermophilus growing at 70 degrees C. Int J Biochem Cell Biol 28:239–246

    Article  PubMed  CAS  Google Scholar 

  • Han Y, Oota H, Osier MV et al (2005) Considerable haplotype diversity within the 23 kb encompassing the ADH7 gene. Alcohol Clin Exp Res 29:2091–2100

    Article  PubMed  CAS  Google Scholar 

  • Han Y, Gu S, Oota H et al (2007) Evidence of positive selection on a class I ADH locus. Am J Hum Genet 80:441–456

    Article  PubMed  CAS  Google Scholar 

  • Harada S, Okubo T, Nakamura T et al (1999) A novel polymorphism (−357G/A) of the ALDH2 gene: linkage disequilibrium and an association with alcoholism. Alcohol Clin Exp Res 23:958–962

    PubMed  CAS  Google Scholar 

  • Hayashi T, Makino K, Ohnishi M et al (2001) Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12. DNA Res 8:11–22

    Article  PubMed  CAS  Google Scholar 

  • Holmes RS (2009) Opossum alcohol dehydrogenases: sequences, structures, phylogeny and evolution. Evidence for the tandem location of ADH genes on opossum chromosome 5. Chem Biol Interact 178:8–15

    Article  PubMed  CAS  Google Scholar 

  • Hoog JO, Hedberg JJ, Stromberg P et al (2001) Mammalian alcohol dehydrogenase: functional and structural implications. J Biomed Sci 8:71–76

    Article  PubMed  CAS  Google Scholar 

  • Hur MW, Edenberg HJ (1992) Cloning and characterization of the ADH5 gene encoding human alcohol dehydrogenase 5, formaldehyde dehydrogenase. Gene 121:305–311

    Article  PubMed  CAS  Google Scholar 

  • Innan H (2003) A two-locus gene conversion model with selection and its application to the human RHCE and RHD genes. Proc Natl Acad Sci USA 100:8793–8798

    Article  PubMed  CAS  Google Scholar 

  • Kay RNB, Davies AG (1994) Colobinem monkeys: their ecology, behaviour and evolution. In: Oate JF (ed) Davis AG. Cambridge University Press, Cambridge, pp 229–250

    Google Scholar 

  • Kent WJ, Sugnet CW, Furey TS et al (2002) The human genome browser at UCSC. Genome Res 12:996–1006

    PubMed  CAS  Google Scholar 

  • Lander ES, Linton LM, Birren B et al (2001) Initial sequencing and analysis of the human genome. Nature (Lond) 409:860–921

    Article  CAS  Google Scholar 

  • Li H, Gu S, Cai X et al (2008) Ethnic related selection for an ADH Class I variant within East Asia. PLoS One 3:e1881

    Article  PubMed  Google Scholar 

  • Li H, Borinskaya S, Yoshimura K et al (2009) Refined geographic distribution of the oriental ALDH2*504Lys (nee 487Lys) variant. Ann Hum Genet 73:335–345

    Article  PubMed  CAS  Google Scholar 

  • Louchart A, Wesselman H, Blumenschine RJ et al (2009) Taphonomic, avian, and small-vertebrate indicators of Ardipithecus ramidus habitat. Science 326:66e61–66e64

    Article  Google Scholar 

  • Lu RB, Ko HC, Lee JF et al (2005) No alcoholism-protection effects of ADH1B*2 allele in antisocial alcoholics among Han Chinese in Taiwan. Alcohol Clin Exp Res 29:2101–2107

    Article  PubMed  CAS  Google Scholar 

  • Martin RD (1993) Primate origins: plugging the gaps. Nature (Lond) 363:223–234

    Article  CAS  Google Scholar 

  • Martinez MC, Achkor H, Persson B et al (1996) Arabidopsis formaldehyde dehydrogenase. Molecular properties of plant class III alcohol dehydrogenase provide further insights into the origins, structure and function of plant class P and liver class I alcohol dehydrogenases. Eur J Biochem 241:849–857

    Article  PubMed  CAS  Google Scholar 

  • Matsuo Y, Yokoyama S (1989) Molecular structure of the human alcohol dehydrogenase 1 gene. FEBS Lett 243:57–60

    Article  PubMed  CAS  Google Scholar 

  • Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426

    PubMed  CAS  Google Scholar 

  • Ohta T (1988) Evolution by gene duplication and compensatory advantageous mutations. Genetics 120:841–847

    PubMed  CAS  Google Scholar 

  • Ohta T (1993) Pattern of nucleotide substitutions in growth hormone-prolactin gene family: a paradigm for evolution by gene duplication. Genetics 134:1271–1276

    PubMed  CAS  Google Scholar 

  • Ohta T (2000) Evolution of gene families. Gene (Amst) 259:45–52

    Article  CAS  Google Scholar 

  • Oota H, Pakstis AJ, Bonne-Tamir B et al (2004) The evolution and population genetics of the ALDH2 locus: random genetic drift, selection, and low levels of recombination. Ann Hum Genet 68:93–109

    Article  PubMed  CAS  Google Scholar 

  • Oota H, Dunn CW, Speed WC et al (2007) Conservative evolution in duplicated genes of the primate Class I ADH cluster. Gene (Amst) 392:64–76

    Article  CAS  Google Scholar 

  • Osier M, Pakstis AJ, Kidd JR et al (1999) Linkage disequilibrium at the ADH2 and ADH3 loci and risk of alcoholism. Am J Hum Genet 64:1147–1157

    Article  PubMed  CAS  Google Scholar 

  • Osier MV, Pakstis AJ, Goldman D et al (2002a) A proline-threonine substitution in codon 351 of ADH1C is common in Native Americans. Alcohol Clin Exp Res 26:1759–1763

    Article  PubMed  CAS  Google Scholar 

  • Osier MV, Pakstis AJ, Soodyall H et al (2002b) A global perspective on genetic variation at the ADH genes reveals unusual patterns of linkage disequilibrium and diversity. Am J Hum Genet 71:84–89

    Article  PubMed  CAS  Google Scholar 

  • Peng GS, Wang MF, Chen CY et al (1999) Involvement of acetaldehyde for full protection against alcoholism by homozygosity of the variant allele of mitochondrial aldehyde dehydrogenase gene in Asians. Pharmacogenetics 9:463–476

    PubMed  CAS  Google Scholar 

  • Peng GS, Yin JH, Wang MF et al (2002) Alcohol sensitivity in Taiwanese men with different alcohol and aldehyde dehydrogenase genotypes. J Formos Med Assoc 101:769–774

    PubMed  Google Scholar 

  • Reimers MJ, Hahn ME, Tanguay RL (2004) Two zebrafish alcohol dehydrogenases share common ancestry with mammalian class I, II, IV, and V alcohol dehydrogenase genes but have distinct functional characteristics. J Biol Chem 279:38303–38312

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Satre MA, Zgombic-Knight M, Duester G (1994) The complete structure of human class IV alcohol dehydrogenase (retinol dehydrogenase) determined from the ADH7 gene. J Biol Chem 269:15606–15612

    PubMed  CAS  Google Scholar 

  • Sherman DI, Ward RJ, Yoshida A et al (1994) Alcohol and acetaldehyde dehydrogenase gene polymorphism and alcoholism. EXS 71:291–300

    PubMed  CAS  Google Scholar 

  • Slutske WS, Heath AC, Madden PA et al (1995) Is alcohol-related flushing a protective factor for alcoholism in Caucasians? Alcohol Clin Exp Res 19:582–592

    Article  PubMed  CAS  Google Scholar 

  • Suwa G, Kono RT, Simpson SW et al (2009) Paleobiological implications of the Ardipithecus ramidus dentition. Science 326:94–99

    PubMed  CAS  Google Scholar 

  • Szalai G, Duester G, Friedman R et al (2002) Organization of six functional mouse alcohol dehydrogenase genes on two overlapping bacterial artificial chromosomes. Eur J Biochem 269:224–232

    Article  PubMed  CAS  Google Scholar 

  • Takahata N, Satta Y (1997) Evolution of the primate lineage leading to modern humans: phylogenetic and demographic inferences from DNA sequences. Proc Natl Acad Sci USA 94:4811–4815

    Article  PubMed  CAS  Google Scholar 

  • Teshima KM, Innan H (2004) The effect of gene conversion on the divergence between duplicated genes. Genetics 166:1553–1560

    Article  PubMed  CAS  Google Scholar 

  • Venter JC, Adams MD, Myers EW et al (2001) The sequence of the human genome. Science 291:1304–1351

    Article  PubMed  CAS  Google Scholar 

  • von Bahr-Lindstrom H, Hoog JO, Heden LO et al (1986) cDNA and protein structure for the alpha subunit of human liver alcohol dehydrogenase. Biochemistry 25:2465–2470

    Article  Google Scholar 

  • von Bahr-Lindstrom H, Jornvall H, Hoog JO (1991) Cloning and characterization of the human ADH4 gene. Gene 103:269–274

    Article  Google Scholar 

  • Waterston RH, Lindblad-Toh K, Birney E et al (2002) Initial sequencing and comparative analysis of the mouse genome. Nature (Lond) 420:520–562

    Article  CAS  Google Scholar 

  • White TD, Ambrose SH, Suwa G et al (2009) Macrovertebrate paleontology and the Pliocene habitat of Ardipithecus ramidus. Science 326:87–93

    PubMed  CAS  Google Scholar 

  • WoldeGabriel G, Ambrose SH, Barboni D et al (2009) The geological, isotopic, botanical, invertebrate, and lower vertebrate surroundings of Ardipithecus ramidus. Science 326:65e61–65e65

    Article  Google Scholar 

  • Yasunami M, Chen CS, Yoshida A (1990) Multiplication of the class I alcohol dehydrogenase locus in mammalian evolution. Biochem Genet 28:591–599

    Article  PubMed  CAS  Google Scholar 

  • Yasunami M, Chen CS, Yoshida A (1991) A human alcohol dehydrogenase gene (ADH6) encoding an additional class of isozyme. Proc Natl Acad Sci USA 88:7610–7614

    Article  PubMed  CAS  Google Scholar 

  • Yokoyama S, Matsuo Y, Rajasekharan S et al (1992) Molecular structure of the human alcohol dehydrogenase 3 gene. Jpn J Genet 67:167–171

    Article  PubMed  CAS  Google Scholar 

  • Yoshida A (1990) Isozymes of human alcohol dehydrogenase and aldehyde dehydrogenase. Prog Clin Biol Res 344:327–340

    PubMed  CAS  Google Scholar 

  • Yoshida A (1994) Genetic polymorphisms of alcohol metabolizing enzymes related to alcohol sensitivity and alcoholic diseases. Alcohol Alcohol 29:693–696

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We must thank Drs. H. Hirai and H. Imai for kindly giving us the opportunity to write this book chapter.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hiroki Oota .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer

About this chapter

Cite this chapter

Oota, H., Oota, H., Kidd, K.K. (2012). Duplicated Gene Evolution of the Primate Alcohol Dehydrogenase Family. In: Hirai, H., Imai, H., Go, Y. (eds) Post-Genome Biology of Primates. Primatology Monographs. Springer, Tokyo. https://doi.org/10.1007/978-4-431-54011-3_9

Download citation

Publish with us

Policies and ethics