Abstract
Recruitment of lysozyme to a digestive function in ruminant artiodactyls is associated with amplification of the gene. At least four of the approximately ten genes are expressed in the stomach, and several are expressed in nonstomach tissues. Characterization of additional lysozymelike sequences in the bovine genome has identified most, if not all, of the members of this gene family. There are at least six stomachlike lysozyme genes, two of which are pseudogenes. The stomach lysozyme pseudogenes show a pattern of concerted evolution similar to that of the functional stomach genes. At least four nonstomach lysozyme genes exist. The nonstomach lysozyme genes are not monophyletic. A gene encoding a tracheal lysozyme was isolated, and the stomach lysozyme of advanced ruminants was found to be more closely related to the tracheal lysozyme than to the stomach lysozyme of the camel or other nonstomach lysozyme genes of ruminants. The tracheal lysozyme shares with stomach lysozymes of advanced ruminants the deletion of amino acid 103, and several other adaptive sequence characteristics of stomach lysozymes. I suggest here that tracheal lysozyme has reverted from a functional stomach lysozyme. Tracheal lysozyme then represents a second instance of a change in lysozyme gene expression and function within ruminants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Cross M, Manglsdorf I, Wedel A, Renkawitz R (1988) Mouse lysozyme M gene: isolation, characterization, and expression studies. Proc Natl Acad Sci USA 85:6232–6236
Dobson DE, Prager EM, Wilson AC (1984) Stomach lysozymes of ruminants: 1. Distribution and catalytic properties. J Biol Chem 259:11607–11616
Gallagher DS Jr, Threadgill DW, Ryan AM, Womack JE, Irwin DM (1993) Physical mapping of the lysozyme gene family in cattle. Mam Genome 4:368–373
Irwin DM, Wilson AC (1989) Multiple cDNA sequences and the evolution of bovine stomach lysozyme. J Biol Chem 264:11387–11393
Irwin DM, Wilson AC (1990) Concerted evolution of ruminant stomach lysozymes. Characterization of lysozyme cDNA clones from sheep and deer. J Biol Chem 265:4944–4952
Irwin DM, Sidow A, White RT, Wilson AC (1989) Multiple genes for ruminant lysozymes. In: Smith-Gill SJ, Sercarz E (eds) The immune response to structurally defined proteins: the lysozyme model. Adenine Press, Schenectady, NY, pp 73–85
Irwin DM, Kocher TD, Wilson AC (1991) Evolution of the cytochromeb gene of mammals. J Mol Evol 32:128–144
Irwin DM, Prager EM, Wilson AC (1992) Evolutionary genetics of ruminant lysozymes. Anim Genet 23:193–202
Irwin DM, White RT, Wilson AC (1993) Characterization of the cow stomach lysozyme genes: repetitive DNA and concerted evolution. J Mol Evol 37:355–366
Ito Y, Yamada H, Nakamura M, Yoshikawa A, Ueda T, Imoto T (1993) The primary structures and properties of non-stomach lysozymes of sheep and cow, and implication for functional divergence of lysozyme. Eur J Biochem 213:649–658
Jollès J, Jolles P, Bowman BH, Prager EM, Stewart C-B, Wilson AC (1989) Episodic evolution in the stomach lysozymes of ruminants. J Mol Evol 28:528–535
Jollès J, Prager EM, Alnemri ES, Jolles P, Ibrahimi IM, Wilson AC (1990) Amino acid sequences of stomach and non-stomach lysozymes of ruminants. J Mol Evol 30:370–382
Jollès P, Schontgen 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
Kumar S, Tamura K, Nei M (1993) MEGA: Molecular evolutionary genetics analysis, version 1.0, software and documentation. The Pennsylvania State University, University Park, PA
Li W-H, Tanimura M, Sharp PM (1987) An evaluation of the molecular clock hypothesis using mammalian DNA sequences. J Mot Evol 25:330–342
Peters CWB, Kruse U, Pollwein R, Grzeschik K-H, Sippel AE (1989) The human lysozyme gene. Eur J Biochem 182:507–516
Prieur DJ (1986) Tissue specific deficiency of lysozyme in ruminants. Comp Biochem Physiol 8513:349–353
Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239: 487–491
Sambrook J, Fritscuh EF, Maniatis T (1989) Molecular cloning, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
Savage DE, Russell DE (1983) Mammalian paleofaunas of the world. Addison-Wesley, Reading MA
Steinhoff UM, Senfit B, Seyfert H-M (1994) Lysozyme-encoding bovine cDNAs from neutrophile granulocytes and mammary gland are derived from a different gene than stomach lysozymes. Gene 143:271–276
Stewart C-B, Wilson AC (1987) Sequence convergence and functional adaptation of stomach lysozymes from foregut fermenters. Cold Spring Harbor Syrup Quant Biol 52:891–899
Stewart C-B, Schilling JW, Wilson AC (1987) Adaptive evolution in the stomach lysozymes of foregut fermenters. Nature 330:401–404
Swanson KW, Irwin DM, Wilson AC (1991) Stomach lysozyme gene of the langur monkey: tests for convergence and positive selection. J Mol Evol 33:418–425
Swofford DL (1993) PAUP: Phylogenetic analysis using parsimony, version 3.1.1, software and documentation. Smithsonian Institution, Washington, DC
Takeuchi K, Irwin DM, Gallup M, Shinbrot E, Kai H, Stewart C-B, Basbum C (1993) Multiple cDNA sequences of bovine tracheal lysozyme. J Biol Chem 268:27440–27446
White FH Jr, McKenzie HA, Shaw DC, Pearce RJ (1988) Studies on a partially purified bovine milk lysozyme. Biochem Int 16:521–528
Wistow G (1993) Lens crystallins: gene recruitment and evolutionary dynamism. Trends Biochem Sci 18:301–306
Yeh TC, Wilson AC, Irwin DM (1993) Evolution of rodent lysozymes: isolation and sequence of the rat lysozyme genes. Mol Phylogenet Evol 2:65–75
Author information
Authors and Affiliations
Additional information
Correspondence to: D.M. Irwin
Rights and permissions
About this article
Cite this article
Irwin, D.M. Evolution of the bovine lysozyme gene family: Changes in gene expression and reversion of function. J Mol Evol 41, 299–312 (1995). https://doi.org/10.1007/BF01215177
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01215177