Inactivation dates of the human and guinea pig vitamin C genes

Abstract

The capacity to biosynthesize ascorbic acid has been lost in a number of species including primates, guinea pigs, teleost fishes, bats, and birds. This inability results from mutations in the GLO gene coding for L-gulono-γ-lactone oxidase, the enzyme responsible for catalyzing the last step in the vitamin C biosynthetic pathway. We analyzed available primate and rodent GLO gene sequences to determine their evolutionary history. We used a method based on sequence comparisons of lineages with and without functional GLO genes to calculate inactivation dates of 61 and 14 MYA for the primate and guinea pig genes, respectively. These estimates are consistent with previous phylogeny-based estimates. An analysis of transposable element distribution in the primate and rodent GLO sequences did not reveal conclusive evidence that illegitimate recombination between repeats has contributed to the loss of exons in the primate and guinea pig genes.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Bánhegyi G, Csala M, Braun L, Garzó T, Mandl J (1996) Ascorbate synthesis-dependent glutathione consumption in mouse liver. FEBS Lett 381:39–41

    Article  PubMed  Google Scholar 

  2. Birney EC, Jenness R, Ayaz KM (1976) Inability of bats to synthesise L-ascorbic acid. Nature 260:626–628

    CAS  Article  PubMed  Google Scholar 

  3. Burns JJ (1957) Missing step in man, monkey and guinea pig required for the biosynthesis of L-ascorbic acid. Nature 180:553

    CAS  Article  PubMed  Google Scholar 

  4. Challem JJ (1997) Did the loss of endogenous ascorbate propel the evolution of anthropoidea and Homo sapiens? Med Hypotheses 48:387–392

    CAS  Article  PubMed  Google Scholar 

  5. Challem JJ, Taylor EW (1998) Retroviruses, ascorbate, and mutations, in the evolution of Homo sapiens. Free Radic Biol Med 25:130–132

    CAS  Article  PubMed  Google Scholar 

  6. Chatterjee IB (1973) Evolution and the biosynthesis of ascorbic acid. Science 182:1271–1272

    CAS  Article  PubMed  Google Scholar 

  7. Chaudhuri CR, Chatterjee IB (1969) L-ascorbic acid synthesis in birds: phylogenetic trend. Science 164:435–436

    CAS  Article  PubMed  Google Scholar 

  8. Chou H, Hayakawa T, Diaz S, Krings M, Indriati E, Leakey M, Paabo S, Satta Y, Takahata N, Varki A (2002) Inactivation of CMP-N-acetylneuraminic acid hydroxylase occurred prior to brain expansion during human evolution. Proc Natl Acad Sci USA 99:11736–11741

    CAS  Article  PubMed  Google Scholar 

  9. Coghlan A, Eichler EE, Oliver SG, Paterson AH, Stein L (2005) Chromosome evolution in eukaryotes: a multi-kingdom perspective. Trends Genet 21:673–682

    CAS  Article  PubMed  Google Scholar 

  10. Cooper DN (1999) Human gene evolution. BIOS Scientific, Oxford

    Google Scholar 

  11. Dabrowski K (1990) Gulonolactone oxidase is missing in teleost fish. The direct spectrophotometric assay. Biol Chem Hoppe Seyler 371:207–214

    CAS  PubMed  Google Scholar 

  12. Dabrowski K (1994) Primitive actinopterygian fishes are capable of ascorbic acid synthesis. Experimentia 50:745–748

    CAS  Article  Google Scholar 

  13. Drew KL, Osborne PG, Frerichs KU, Hu Y, Koren RE, Hallenbeck JM, Rice ME (1999) Ascorbate and glutathione regulation in hibernating ground squirrels. Brain Res 851:1–8

    CAS  Article  PubMed  Google Scholar 

  14. Drouin G, Prat F, Ell M, Clarke G (1999) Detecting and characterizing gene conversions between multigene family members. Mol Biol Evol 16:1369–1390

    CAS  PubMed  Google Scholar 

  15. Echols N, Harrison P, Balasubramanian S, Luscombe NM, Bertone P, Zhang Z, Gerstein M (2002) Comprehensive analysis of amino acid and nucleotide composition in eukaryotic genomes, comparing genes and pseudogenes. Nucleic Acids Res 30:2515–2523

    CAS  Article  PubMed  Google Scholar 

  16. Graur D, Li W-H (2000) Fundamentals of molecular evolution, 2nd edn. Sinauer Associates, Inc., Sunderland, Massachusetts

    Google Scholar 

  17. Huchon D, Chevret P, Jordan U, Kilpatrick CW, Ranwez V, Jenkins PD, Brosius J, Schmitz J (2007) Multiple molecular evidences for a living mammalian fossil. Proc Natl Acad Sci USA 104:7495–7499

    CAS  Article  PubMed  Google Scholar 

  18. Hwang D, Lin T (2002) Effect of temperature on dietary vitamin C requirement and lipid in common carp. Comp Biochem Physiol B Biochem Mol Biol 131:1–7

    Article  PubMed  Google Scholar 

  19. Kolomietz E, Meyn MS, Pandita A, Squire JA (2002) The role of Alu repeat clusters as mediators of recurrent chromosomal aberrations in tumors. Genes Chromosomes Cancer 35:97–112

    CAS  Article  PubMed  Google Scholar 

  20. Krasnov A, Reinisalo M, Pitkanen TI, Nishikimi M, Molsa H (1998) Expression of rat gene for L-gulono-gamma-lactone oxidase, the key enzyme of L-ascorbic acid biosynthesis, in guinea pig cells and in teleost fish rainbow trout (Oncorthynchus mykiss). Biochim Biophys Acta 1381:241–248

    CAS  PubMed  Google Scholar 

  21. Li W, Maeda N, Beck MA (2006) Vitamin C deficiency increases the lung pathology of influenza virus-infected Gulo -/- mice. J Nutr 136:2611–2626

    CAS  PubMed  Google Scholar 

  22. Linster CL, Van Schaftingen E (2007) Vitamin C biosynthesis, recycling and degradation in mammals. FEBS J 274:1–22

    CAS  Article  PubMed  Google Scholar 

  23. Moreau R, Dabrowski K (2000) Biosynthesis of ascorbic acid by extant actinopterigians. J Fish Biol 57:733–745

    CAS  Article  Google Scholar 

  24. Murphy WJ, Pevzner PA, O’Brien SJ (2004) Mammalian phylogenomics comes of age. Trends Genet 20:631–639

    CAS  Article  PubMed  Google Scholar 

  25. Nakayama K, Ishida T (2006) Alu-mediated 100-kb deletion in the primate genome: the loss of the agouti signaling protein gene in the lesser apes. Genome Res 16:485–490

    CAS  Article  PubMed  Google Scholar 

  26. Nishikimi M, Kawai T, Yagi K (1992) Guinea pigs possess a highly mutated gene for L-gulono-gamma-lactone oxidase, the key enzyme for L-ascorbic acid biosynthesis missing in this species. J Biol Chem 267(30):21967–21972

    CAS  PubMed  Google Scholar 

  27. Nishikimi M, Fukuyama R, Minoshiman I, Shimizux N, Yagis K (1994) Cloning and chromosomal mapping of the human nonfunctional gene for L-gulono-gamma-lactone oxidase, the enzyme for L-ascorbic acid biosynthesis missing in man. J Biol Chem 269:13685–13688

    CAS  PubMed  Google Scholar 

  28. Pace JK 2nd, Feschotte C (2007) The evolutionary history of human DNA transposons: evidence for intense activity in the primate lineage. Genome Res 17:422–432

    CAS  Article  PubMed  Google Scholar 

  29. Padh H (1990) Cellular functions of ascorbic acid. Biochem Cell Biol 68:1166–1173

    CAS  Article  PubMed  Google Scholar 

  30. Pascale E, Valle E, Furano A (1990) Amplification of an ancestral mammalian L1 family of long interspersed repeated DNA occurred just before the murine radiation. Proc Natl Acad Sci USA 87:9481–9485

    CAS  Article  PubMed  Google Scholar 

  31. Pauling L (1970) Evolution and the need for ascorbic acid. Proc Natl Acad Sci USA 67:1643–1648

    CAS  Article  PubMed  Google Scholar 

  32. Pollock JI, Mullin RJ (1987) Vitamin C biosynthesis in prosimians: evidence for the anthropoid affinity of tarsius. Am J Phys Anthropol 73:65–70

    CAS  Article  PubMed  Google Scholar 

  33. Price AL, Eskin E, Pevzner PA (2004) Whole-genome analysis of Alu repeat elements reveals complex evolutionary history. Genome Res 14:2245–2252

    CAS  Article  PubMed  Google Scholar 

  34. Ray DA, Pagan HJT, Thompson ML, Stevens RD (2007) Bats with hATs: evidence for recent DNA transposon activity in genus Myotis. Mol Biol Evol 24:632–639

    CAS  Article  PubMed  Google Scholar 

  35. Rowold DJ, Herrera RJ (2000) Alu elements and the human genome. Genetica 108:57–72

    CAS  Article  PubMed  Google Scholar 

  36. Steiper ME, Young NM (2006) Primate molecular divergence dates. Mol Phylogenet Evol 41:384–394

    CAS  Article  PubMed  Google Scholar 

  37. Szabó Z, Levi-Minzi SA, Christiano AM, Struminger C, Stoneking M, Batzer MA, Boyd CD (1999) Sequential loss of two neighboring exons of the tropoelastin gene during primate evolution. J Mol Evol 49:664–671

    Article  PubMed  Google Scholar 

  38. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    CAS  Article  PubMed  Google Scholar 

  39. Toth G, Deak G, Barta E, Kiss GB (2006) PLOTREP: a web tool for defragmentation and visual analysis of dispersed genomic repeats. Nucleic Acids Res 34:W708–W713

    CAS  Article  PubMed  Google Scholar 

  40. Toyohara H, Nakata T, Touhata K, Hashimoto H, Kinoshita M, Sakaguchi M, Nishikimi M, Yagi K, Wakamatsu Y, Ozato K (1996) Transgenic expression of L-gulono-gamma-lactone oxidase in medaka (Oryzias latipes), a teleost fish that lacks this enzyme necessary for L-ascorbic acid biosynthesis. Biochem Biophys Res Commun 223:650–653

    CAS  Article  PubMed  Google Scholar 

  41. Uddin RK, Zhang Y, Siu VM, Fan Y, O’Reilly RL, Rao J, Singh SM (2006) Breakpoint associated with a novel 2.3 mb deletion in the VCFS region of 22q11 and the role of Alu (SINE) in recurring microdeletions. BMC Med Genet 7:18

    Google Scholar 

  42. Winter H, Langbein L, Krawczak M, Cooper DN, Jave-Suarez LF, Rogers MA, Praetzel S, Heidt PJ, Schweizer J (2001) Human type I hair keratin pseudogene phihHaA has functional orthologs in the chimpanzee and gorilla: evidence for recent inactivation of the human gene after the Pan-Homo divergence. Hum Genet 108:37–42

    CAS  Article  PubMed  Google Scholar 

  43. Zhang Z, Harrison PM, Liu Y, Gerstein M (2003) Millions of years of evolution preserved: a comprehensive catalog of the processed pseudogenes in the human genome. Genome Res 13:2541–2558

    CAS  Article  PubMed  Google Scholar 

  44. Zhang ZD, Frankish A, Hunt T, Harrow J, Gerstein M (2010) Identification and analysis of unitary pseudogenes: historic and contemporary gene losses in humans and other primates. Genome Biol 11:R26

    Article  PubMed  Google Scholar 

  45. Zilva SS (1936) Vitamin C requirements of the guinea-pig. Biochem J 30:1419–1429

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the two anonymous referees for their useful and constructive comments on a previous version of this manuscript. This work was supported by a Discovery Grant from the Natural Science and Engineering Research Council of Canada to G. D.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Guy Drouin.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 39 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Lachapelle, M.Y., Drouin, G. Inactivation dates of the human and guinea pig vitamin C genes. Genetica 139, 199–207 (2011). https://doi.org/10.1007/s10709-010-9537-x

Download citation

Keywords

  • Vitamin C
  • L-gulono-γ-lactone oxidase
  • GLO gene
  • Unitary pseudogene
  • Human
  • Guinea pig