Skip to main content

Ancient origin of lactalbumin from lysozyme: Analysis of DNA and amino acid sequences

Summary

Parsimony trees relating DNA sequences coding for lysozymesc and α-lactalbumins suggest that the gene duplication that allowed lactalbumin to evolve from lysozyme preceded the divergence of mammals and birds. Comparisons of the amino acid sequences of additional lysozymes and lactalbumins are consistent with this view. When all base positions are considered, the probability that the duplication leading to the lactalbumin gene occurred after the start to mammalian evolution is estimated to be 0.05–0.10. Elimination of the phylogenetic noise generated by fast evolution and compositional bias at third positions of codons reduced this probability to 0.002–0.03. Thus the gene duplication may have long preceded the acquisition of lactalbumin function.

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

References

  1. Beg OU, von Bahr-Lindström H, Zaidi ZH, Jörnvall H (1985) The primary structure of α-lactalbumin from camel milk. Eur J Biochem 147:233–239

    PubMed  Google Scholar 

  2. Bernardi G, Bernardi G (1986) Compositional constraints and genome evolution. J Mol Evol 24:1–11

    PubMed  Google Scholar 

  3. Castañón MJ, Spevak W, Adolf GR, Chlebowicz-Sledziewska E, Sledziewski A (1988) Cloning of human lysozyme and expression in the yeastSaccharomyces cerevisiae. Gene 66:223–234

    PubMed  Google Scholar 

  4. DeSalle R, Freedman T, Prager EM, Wilson AC (1987) Tempo and mode of sequence evolution in mitochondrial DNA of HawaiianDrosophila. J Mol Evol 26:157–164

    PubMed  Google Scholar 

  5. Engström Å, Xanthopoulos KG, Boman HG, Bennich H (1985) Amino acid and cDNA sequences of lysozyme fromHyalophora cecropia. EMBO J 4:2119–2122

    Google Scholar 

  6. Hall L, Craig RK, Edbrooke MR, Campbell PN (1982) Comparison of the nucleotide sequence of cloned human and guineapig pre-α-lactalbumin cDNA with that of chicken pre-lysozyme cDNA suggests evolution from a common ancestral gene. Nucleic Acids Res 10:3503–3514

    PubMed  Google Scholar 

  7. Hayssen V, Blackburn DG (1985) α-lactalbumin and the origins of lactation. Evolution 39:1147–1149

    Google Scholar 

  8. Jollès P, Jollès J (1984) What's new in lysozyme research? Mol Cell Biochem 63:165–189

    PubMed  Google Scholar 

  9. Jollès J, Sen A, Prager EM, Jollès P (1977) Structural data concerning reptilian (tortoise) egg lysozyme. J Mol Evol 10:261–264

    PubMed  Google Scholar 

  10. Jollès J, Ibrahimi IM, Prager EM, Schoentgen F, Jollès P, Wilson AC (1979a) Amino acid sequence of pheasant lysozyme. Evolutionary change affecting processing of prelysozyme. Biochemistry 18:2744–2752

    PubMed  Google Scholar 

  11. Jollès J, Schoentgen F, Croizier G, Croizier L, Jollès P (1979b) Insect lysozymes from three species of Lepidoptera: their structural relatedness to the c (chicken) type lysozyme. J Mol Evol 14:267–271

    PubMed  Google Scholar 

  12. Jollès P, Schoentgen F, Jollès J, Dobson DE, Prager EM, Wilson AC (1984) Stomach lysozymes of ruminants. II. Amino acid sequence of cow lysozyme 2 and immunological comparisons with other lysozymes. J Biol Chem 259:11617–11625

    PubMed  Google Scholar 

  13. Jung A, Sippel AE, Grez M, Schütz G (1980) Exons encode functional and structural units of chicken lysozyme. Proc Natl Acad Sci USA 77:5759–5763

    PubMed  Google Scholar 

  14. Kaminogawa S, McKenzie HA, Shaw DC (1984) The amino acid sequence of equine α-lactalbumin. Biochem Int 9:539–546

    PubMed  Google Scholar 

  15. Kumagai I, Tamaki E, Kakinuma S, Miura K-I (1987) Molecular cloning and sequencing of cDNA encoding goat pre α-lactalbumin. J Biochem 101:511–517

    PubMed  Google Scholar 

  16. Lake JA (1987) A rate-independent technique for analysis of nucleic acid sequences: evolutionary parsimony. Mol Biol Evol 4:167–191

    PubMed  Google Scholar 

  17. McKenzie HA, Shaw DC (1985) The amino acid sequence of equine milk lysozyme. Biochem Int 10:23–31

    PubMed  Google Scholar 

  18. McKenzie HA, White FH Jr (1987) Studies of a trace cell lytic activity associated with α-lactalbumin. Biochem Int 14:347–356

    PubMed  Google Scholar 

  19. Nitta K, Tsuge H, Sugai S, Shimazaki K (1987) The calciumbinding property of equine lysozyme. FEBS Lett 223:405–408

    PubMed  Google Scholar 

  20. Pervaiz S, Brew K (1986) Purification and characterization of the major whey proteins from the milks of the bottlenosed dolphin (Tursiops truncatus), the Florida manatee (Trichecus manatus latirostris) and the beagle (Canis familiaris). Arch Biochem Biophys 246:846–854

    PubMed  Google Scholar 

  21. Preparata G, Saccone C (1987) A simple quantitative model of the molecular clock. J Mol Evol 26:7–15

    PubMed  Google Scholar 

  22. Qasba PK, Safaya SK (1984) Similarity of the nucleotide sequences of rat α-lactalbumin and chicken lysozyme genes. Nature 308:377–380

    PubMed  Google Scholar 

  23. Rodríguez R, Menéndez-Arias L, González de Buitrago G, Gavilanes JG (1985) Amino acid sequence of pigeon egg-white lysozyme. Biochem Int 11:841–843

    PubMed  Google Scholar 

  24. Rodríguez R, Menéndez-Arias L, González de Buitrago G, Gavilanes JG (1987) Structure of the pigeon lysozyme and its relationship with other typec lysozymes. Comp Biochem Physiol 88B:791–796

    Google Scholar 

  25. Sarich VM (1985) Rodent macromolecular systematics. In: Luckett WP, Hartenberger J-L (eds) Evolutionary relationships among rodents. A multidisciplinary analysis. Plenum, New York, pp 423–452

    Google Scholar 

  26. Shewale JG, Sinha SK, Brew K (1984) Evolution of α-lactalbumins. The complete amino acid sequence of the α-lactalbumin from a marsupial (Macropus rufogriseus) and corrections to regions of sequence in bovine and goat α-lactalbumins. J Biol Chem 259:4947–4956

    PubMed  Google Scholar 

  27. Spicer SS, Erlandsen SL, Wilson AC, Hammer MF, Hennigar RA, Schulte BA (1987) Genetic differences in the histochemically defined structure of oligosaccharides in mice. J Histochem Cytochem 35:1231–1244

    PubMed  Google Scholar 

  28. Stewart C-B, Schilling JW, Wilson AC (1987) Adaptive evolution in the stomach lysozymes of foregut fermenters. Nature 330:401–404

    PubMed  Google Scholar 

  29. Stuart DI, Acharya KR, Walker NPC, Smith SG, Lewis M, Phillips DC (1986) α-lactalbumin possesses a novel calcium binding loop. Nature 324:84–87

    PubMed  Google Scholar 

  30. Swofford DL (1985) Phylogenetic analysis using parsimony (PAUP), Version 2.4 Illinois Natural History Survey, Champaign, IL

    Google Scholar 

  31. White TJ, Mross GA, Osserman EF, Wilson AC (1977) Primary structure of rat lysozyme. Biochemistry 16:1430–1436

    PubMed  Google Scholar 

  32. Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639

    PubMed  Google Scholar 

  33. Wilson AC, Ochman H, Prager EM (1987) Molecular time scale for evolution. Trends Genet 3:241–247

    Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ellen M. Prager.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Prager, E.M., Wilson, A.C. Ancient origin of lactalbumin from lysozyme: Analysis of DNA and amino acid sequences. J Mol Evol 27, 326–335 (1988). https://doi.org/10.1007/BF02101195

Download citation

Key words

  • Parsimony
  • Evolutionary parsimony
  • Statistical testing
  • Phylogenetic noise
  • Base composition
  • Transversions
  • Mammals
  • Birds
  • Insects
  • Mammary gland