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Characterization of the cow stomach lysozyme genes: Repetitive DNA and concerted evolution

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Abstract

Cow stomach lysozyme genes have evolved in a mosaic pattern. The majority of the intronic and flanking sequences show an amount of sequence difference consistent with divergent evolution since duplication of the genes 40–50 million years ago. In contrast, exons 1, 2, and 4 and immediately adjacent intronic sequences differ little between genes and show evidence of recent concerted evolution. Exon 3 appears to be evolving divergently. The three characterized genes vary from 5.6 to 7.9 kilobases in length. Different distributions of repetitive DNA are found in each gene, which accounts for the majority of length differences between genes. The different distributions of repetitive DNA in each gene suggest the repetitive elements were inserted into each gene after the duplications that give rise to these three genes and provide additional support for divergent evolution for the majority of each gene. The observation that intronic and flanking sequences are evolving divergently suggests that the concerted evolution events involved in homogenizing the coding regions of lysozyme genes involve only one exon at a time. This model of concerted evolution would allow the shuffling of exon-sized pieces of information between genes, a phenomenon that may have aided in the early adaptive evolution of stomach lysozyme.

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References

  • Benton WD, Davis RW (1977) Screening λgt recombinant clones by hybridization to single plaques in situ. Science 196:180–182

    Google Scholar 

  • Bilofsky HS, Burks C (1988) The GenBank® genetic sequence data bank. Nucleic Acids Res 16:1861–1863

    Google Scholar 

  • Bonifer C, Vidal M, Grosveld F, Sippel AE (1990) Tissue specific and position independent expression of the complete gene domain for chicken lysozyme in transgenic mice. EMBO J 9:2843–2848

    Google Scholar 

  • Castañón MJ, Spevak W, Adolf GR, Chlebowicz-Śledziewska E, Śledziewski A (1988) Cloning of human lysozyme gene and expression in the yeast Saccharomyces cerevisiae. Gene 66: 223–234

    Google Scholar 

  • Chung LP, Keshav S, Gordon S (1988) Cloning the human lysozyme cDNA. Proc Natl Acad Sci USA 85:6227–6231

    Google Scholar 

  • Cortopassi GA, Wilson AC (1990) Recent origin of the P lysozyme gene in mice. Nucleic Acids Res 18:1911

    Google Scholar 

  • Cortopassi GA, Wilson AC (1991) Genetic analysis of a switch in cell specificity of P lysozyme expression in molossinus mice. Genet Res 58:111–114

    Google Scholar 

  • Cross M, Renkawitz R (1990) Repetitive sequence involvement in the duplication and divergence of mouse lysozyme genes. EMBO J 9:1283–1288

    Google Scholar 

  • Cross M, Mangelsdorf I, Wedel A, Renkawitz R (1988) Mouse lysozyme M gene. Proc Natl Acad Sci USA 85:6232–6236

    Google Scholar 

  • Dobson DE, Prager EM, Wilson AC (1984) Stomach lysozymes of ruminants. I. Distribution and catalytic properties. J Biol Chem 259:11607–11616

    Google Scholar 

  • Duncan CH (1987) Novel Alu-type repeat in artiodactyls. Nucleic Acids Res 15:1340

    Google Scholar 

  • Elgin SCR (1988) The formation and function of DNase I hypersensitive sites in the process of gene activation. J Biol Chem 263:19259–19262

    Google Scholar 

  • Elgin SCR (1990) Chromatin structure and gene activity. Curr Opin Cell Biol 2:437–445

    Google Scholar 

  • Ellis NA, Goodfellow PJ, Pym B, Smith M, Palmer M, Frischauf A-M, Goodfellow PN (1989) The pseudoautosomal boundary in man is defined by an AN repeat sequence inserted on the Y chromosome. Nature 337:81–84

    Google Scholar 

  • Ellis N, Yen P, Neiswanger K, Shapiro LJ, Goodfellow PN (1990) Evolution of the pseudoautosomal boundary in Old-World monkeys and great apes. Cell 63:977–986

    Google Scholar 

  • Feinberg AP, Vogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13

    CAS  PubMed  Google Scholar 

  • Frischauf A-M (1987) Construction and characterization of a genomic library. Methods Enzymol 152:190–199

    Google Scholar 

  • Hammer MF, Schilling JW, Prager EM, Wilson AC (1987) Recruitment of lysozyme as a major enzyme in the mouse gut: duplication, divergence, and regulatory evolution. J Mol Evol 24:272–279

    Google Scholar 

  • Henikoff S (1984) Unidirectional digestion with Exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28: 351–359

    Google Scholar 

  • Irwin DM, Wilson AC (1989) Multiple cDNA sequences and the evolution of bovine stomach lysozyme. J Biol Chem 264: 11387–11393

    Google Scholar 

  • Irwin DM, Wilson AC (1990) Concerted evolution of ruminant stomach lysozymes. Characterization of cDNA clones from sheep and deer. J Biol Chem 265:4944–4952

    Google Scholar 

  • Irwin DM, Sidow A, White RT, Wilson AC (1989) Multiple genes for ruminant lysozymes. In: Smith-Gill SJ, Sercarz EE (eds) The immune response to structurally defined proteins: the lysozyme model. Adenine Press, Schenectady NY, pp 73–85

    Google Scholar 

  • Irwin DM, Kocher TD, Wilson AC (1991) Evolution of the cytochrome b gene of mammals. J Mol Evol 32:128–144

    CAS  PubMed  Google Scholar 

  • Irwin DM, Prager EM, Wilson AC (1992) Evolutionary genetics of ruminant lysozymes. Animal Genetics 23:193–202

    Google Scholar 

  • 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

    Google Scholar 

  • Jollès J, Jollbs 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

    Google Scholar 

  • Jollès J, Prager EM, Alnemri ES, Jolles P, Ibrahimi IM, Wilson AC (1990) Amino acid sequences of stomach and nonstomach lysozymes of ruminants. J Mol Evol 30:370–382

    Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    CAS  PubMed  Google Scholar 

  • Kraus F, Miyamoto MM (1991) Rapid cladogenesis among the pecoran ruminants: evidence from mitochondrial DNA sequences. Syst Zool 40:117–130

    Google Scholar 

  • Koop BF, Siemieniak D, Slightom JL, Goodman M, Dunbar J, Wright PC, Simons EL (1989) Tarsier δ- and β-globin genes. J Biol Chem 264:68–79

    Google Scholar 

  • Li Q, Zhou B, Powers P, Enver T, Stamatoyannopoulos G (1991) Primary structure of the goat β-globin locus control region. Genomics 9:488–499

    Google Scholar 

  • Li W-H, Wu C-I, Luo C-C (1985) A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol Biol Evol 2:150–174

    Google Scholar 

  • Li W-H, Tanimura M, Sharp PM (1987) An evaluation of the molecular clock hypothesis using mammalian DNA sequences. J Mol Evol 25:330–342

    Google Scholar 

  • Mazan S, Bachellerie J-P (1990) Organization of the gene family encoding mouse U313 RNA: role of gene conversions in its concerted evolution. Gene 94:263–272

    Google Scholar 

  • Mierendorf RC, Pfeffer D (1987) Direct sequencing of denatured plasmid DNA. Methods Enzymol 152:556–562

    Google Scholar 

  • Peters CWB, Kruse U, Pollwein R, Grzeschik K-H, Sippel AE (1989) The human lysozyme gene. Eur J Biochem 182:507–516

    CAS  PubMed  Google Scholar 

  • Phi-Van L, von Kries JP, Ostertag W, Strätling WH (1990) The chicken lysozyme 5' matrix attachment region increases transcription from a heterologous promoter in heterologous cells and dampens position effects on the expression of transfected genes. Mol Cell Biol 10:2302–2307

    Google Scholar 

  • Prieur DJ (1986) Tissue specific deficiency of lysozyme in ruminants. Comp Biochem Physiol 85B:349–353

    Google Scholar 

  • Quentin Y (1988) The Alu family developed through successive waves of fixation closely connected with primate lineage history. J Mol Evol 27:194–202

    Google Scholar 

  • Quentin Y (1989) Successive waves of fixation of B1 variants in rodent lineage history. J Mol Evol 28:299–305

    Google Scholar 

  • Rogers JH (1985) The origin and evolution of retroposons. Int Rev Cytol 93:187–279

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, 2 ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor NY

    Google Scholar 

  • Schimenti JC, Duncan CH (1984) Ruminant globin gene structures suggest an evolutionary role for Alu-type repeats. Nucleic Acids Res 12:1641–1655

    Google Scholar 

  • Slagel V, Flemington E, Traina-Dorge V, Bradshaw H, Deininger P (1987) Clustering and subfamily relationships of the Alu family in the human genome. Mol Biol Evol 4:19–29

    Google Scholar 

  • Soulier S, Mercier JC, Vilotte JL, Anderson J, Clark AJ, Provot C (1989) The bovine and ovine genomes contain multiple sequences homologous to the α-lactalbumin-encoding gene. Gene 83:331–338

    Google Scholar 

  • Spence SE, Young RM, Garner KJ, Lingrel JB (1985) Localization and characterization of members of a family of repetitive sequences in the goat β-globin locus. Nucleic Acids Res 13: 2171–2186

    Google Scholar 

  • Stewart C-B, Wilson AC (1987) Sequence convergence and functional adaptation of stomach lysozymes from foregut fermenters. Cold Spring Harbor Symp Quant Biol 52:891–899

    Google Scholar 

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

    Google Scholar 

  • Stief A, Winter DM, Strätling WH, Sippel AE (1989) A nuclear DNA attachment element mediates elevated and position-independent gene activity. Nature 341:343–345

    Google Scholar 

  • 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

    Google Scholar 

  • Watanabe Y, Tsukada T, Notake M, Nakanishi S, Numa S (1982) Structural analysis of repetitive DNA sequences in the bovine corticotropin-β-lipotropin precursor gene region. Nucleic Acids Res 10:1459–1469

    Google Scholar 

  • Weiner AM, Deininger PL, Efstratiadis A (1986) Nonviral retroposons: genes, pseudogenes, and transposable elements generated by the reverse flow of genetic information. Annu Rev Biochem 55:631–661

    Google Scholar 

  • White FH Jr, McKenzie HA, Shaw DC, Pearce RJ (1988) Studies on a partially purified bovine milk lysozyme. Biochem Int 16:521–528

    Google Scholar 

  • Yoshimura K, Toibana A, Nakahama K (1988) Human lysozyme: sequencing of a cDNA, and expression and secretion by Saccharomyces cerevisiae. Biochem Biophys Res Commun 150:794–801

    Google Scholar 

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Deceased July 21, 1991

Correspondence to: D.M. Irwin

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Irwin, D.M., White, R.T. & Wilson, A.C. Characterization of the cow stomach lysozyme genes: Repetitive DNA and concerted evolution. J Mol Evol 37, 355–366 (1993). https://doi.org/10.1007/BF00178866

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  • DOI: https://doi.org/10.1007/BF00178866

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