Skip to main content
SpringerLink
Log in

Molecular evolution of theSaccharomyces cerevisiae histone gene loci

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Summary

The core histone genes ofSaccharomyces cerevisiae are arranged as duplicate nonallelic sets of specifically paired genes. The identity of structural organization between the duplicated gene pairs would have its simplest evolutionary origin in the duplication of a complete locus in a single event. In such a case, the time since the duplication of one of the genes should be identical to that since duplication of the gene adjacent to it on the chromosome. A calculation of the evolutionary distances between the coding DNA sequences of the histone genes leads to a duplication paradox: The extents of sequence divergence in the silent component of third-base positions for adjacent pairs of genes are not identical. Estimates of the evolutionary distance between the two H3-H4 noncoding intergene DNA sequences are large; the divergence between the two separate sequences is indistinguishable from the divergence between either of the regions and a randomly generated permutation of itself. These results suggest that the duplication event may have occurred much earlier than previously estimated. The potential age of the duplication, and the attractive simplicity of the duplication of both the H3-H4 and the H2A-H2B gene pairs having taken place in a single event, leads to the hypothesis that modern haploidS. cerevisiae may have evolved by diploidization or fusion of two ancient fungi.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abovich N, Gritz L, Tung L, Rosbash M (1985) Effect of RP51 gene dosage alterations on ribosome synthesis inSaccharomyces cerevisiae. Mol Cell Biol 5:3429–3435

    PubMed  Google Scholar 

  • Bennetzen JL, Hall BD (1982a) Codon selection in yeast. J Biol Chem 257:3026–3031

    PubMed  Google Scholar 

  • Bennetzen JL, Hall BD (1982b) The primary structure of theSaccharomyces cerevisiae gene for alcohol dehydrogenase I. J Biol Chem 257:3018–3025

    PubMed  Google Scholar 

  • Choe J, Kolodrubetz D, Grunstein M (1982) The two yeast histone H2A genes encode similar protein subtypes. Proc Natl Acad Sci USA 79:1484–1487

    PubMed  Google Scholar 

  • Choe J, Schuster T, Grunstein M (1985) Organization, primary structure, and evolution of the histone H2A and H2B genes of the fission yeastSchizosaccharomyces pombe. Mol Cell Biol 5:3261–3269

    PubMed  Google Scholar 

  • Defeo-Jones D, Scolnick E, Koller R, Dhar R (1983) ras-Related gene sequences identified and isolated fromSaccharomyces cerevisiae. Nature 306:707–709

    PubMed  Google Scholar 

  • Dhar R, Nieto A, Koller R, Defeo-Jones D, Scolnick E (1984) Nucleotide sequence of two rasH-related genes isolated from the yeastSaccharomyces cerevisiae. Nucleic Acids Res 12:3611–3618

    PubMed  Google Scholar 

  • Ernst JF, Stewart JW, Sherman F (1981) The cycl-11 mutation in yeast reverts by recombination with a nonallelic gene: composite genes determining the iso-cyctochromes c. Proc Natl Acad Sci USA 78:6334–6338

    PubMed  Google Scholar 

  • Fogel S, Mortimer RK, Lusnak K (1981) Mechanisms of meiotic gene conversion, or “Wanderings on a Foreign Strand”. In: Strathern JN, Jones EW, Broach JR (eds) The molecular biology of the yeastSaccharomyces. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, pp 289–339

    Google Scholar 

  • Fried HM, Pearson NJ, Kim CH, Warner JR (1981) The genes for fifteen ribosomal proteins ofSaccharomyces cerevisiae. J Biol Chem 256:10176–10183

    PubMed  Google Scholar 

  • Goad WB, Kanehisa MI (1982) Pattern recognition in nucleic acid sequences. I. A general method for finding local homologies and symmetries. Nucleic Acids Res 10:247–263

    PubMed  Google Scholar 

  • Graur D (1985) Amino acid composition and the evolutionary rates of protein-coding genes. J Mol Evol 22:53–62

    PubMed  Google Scholar 

  • Grunstein M, Rykowski M, Kolodrubetz D, Choe J, Wallis JW (1984) A genetic analysis of histone protein subtypes in yeast. In: Stein GS, Stein JL, Marzluff WF (eds) Histone genes. John Wiley & Sons, New York, pp 35–63

    Google Scholar 

  • Guarente L, Yocum RR, Gifford P (1982) A GAL10-CYC1 hybrid yeast promoter identifies the GAL4 regulatory region as an upstream site. Proc Natl Acad Sci USA 79:7410–7414

    PubMed  Google Scholar 

  • Hentschel CC, Birnstiel ML (1981) The organization and expression of histone gene families. Cell 25:301–313

    PubMed  Google Scholar 

  • Hereford L, Fahrner K, Woolford J Jr, Rosbash M, Kaback DB (1979) Isolation of yeast histone genes H2A and H2B. Cell 18:1261–1271

    PubMed  Google Scholar 

  • Holland JP, Holland MJ (1980) Structural comparison of two non-tandemly repeated yeast glyceraldehyde-3-phosphate dehydrogenase genes. J Biol Chem 255:2596–2605

    PubMed  Google Scholar 

  • Holland MJ, Holland JP, Thill GP, Jackson KA (1981) The primary structures of two yeast enolase genes. J Biol Chem 256:1385–1395

    PubMed  Google Scholar 

  • Jackson JA, Fink GR (1981) Gene conversion between duplicated genetic elements in yeast. Nature 292:306–311

    PubMed  Google Scholar 

  • Jinks-Robertson S, Petes TD (1985) High-frequency meiotic gene conversion between repeated genes on nonhomologous chromosomes in yeast. Proc Natl Acad Sci USA 82:3350–3354

    PubMed  Google Scholar 

  • Johnson ML, Frasier SG (1985) Non-linear least squares analysis. Methods Enzymol 117:301–342

    Google Scholar 

  • Johnston M, Davis RW (1984) Sequences that regulate the divergent GAL1-GAL10 promoter inSaccharomyces cerevisiae. Mol Cell Biol 4:1440–1448

    PubMed  Google Scholar 

  • Kedes LH (1979) Histone genes and histone messengers. Annu Rev Biochem 48:837–870

    PubMed  Google Scholar 

  • Kimura M (1977) Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature 267:275–276

    PubMed  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

    PubMed  Google Scholar 

  • Kimura M (1981) Estimation of evolutionary distances between homologous nucleotide sequences. Proc Natl Acad Sci USA 78:454–458

    PubMed  Google Scholar 

  • Korn LJ, Queen CL, Wegman MN (1977) Computer analysis of nucleic acid regulatory sequences. Proc Natl Acad Sci USA 74:4401–4405

    PubMed  Google Scholar 

  • Mao J, Appel B, Schaack J, Sharp S, Yamada H, Söll D (1982) The 5S RNA genes ofSchizosaccharomyces pombe. Nucleic Acids Res 10:487–500

    PubMed  Google Scholar 

  • Matsumoto S, Yanagida M (1985) Histone gene organization of a fission yeast: a common upstream sequence. EMBO J 4: 3531–3538

    PubMed  Google Scholar 

  • Maxson R, Cohn R, Kedes L (1983) Expression and organization of histone genes. Annu Rev Genet 17:239–277

    PubMed  Google Scholar 

  • McKnight GL, Cardillo TS, Sherman F (1981) An extensive deletion causing overproduction of yeast iso-2-cytochrome c. Cell 25:409–419

    PubMed  Google Scholar 

  • Miyata T, Hayashida H (1981) Extraordinarily high evolution rate of pseudogenes: evidence for the presence of selective pressure against changes between synonymous codons. Proc Natl Acad Sci USA 78:5739–5743

    PubMed  Google Scholar 

  • Miyata T, Yasunaga T, Nishida T (1980) Nucleotide sequence divergence and functional constraint in mRNA evolution. Proc Natl Acad Sci USA 77:7328–7332

    PubMed  Google Scholar 

  • Montgomery DL, Leung DW, Smith M, Shalit P, Faye G, Hall BD (1980) Isolation and sequence of the gene coding for iso-2 cytochrome c inSaccharomyces cerevisiae. Proc Natl Acad Sci USA 77:541–545

    PubMed  Google Scholar 

  • Nasmyth KA, Tatchell K (1980) The structure of transposable yeast mating type loci. Cell 19:753–764

    PubMed  Google Scholar 

  • Powers S, Kataoka T, Fasano O, Goldfarb M, Strathern J, Broach J, Wigler M (1984) Genes inS. cerevisiae encoding proteins with domains homologous to the mammalian ras proteins. Cell 36:607–612

    PubMed  Google Scholar 

  • Russell PR, Hall BD (1982) Structure of theSchizosaccharomyces pombe cytochrome c gene. Mol Cell Biol 2:106–116

    PubMed  Google Scholar 

  • Russell PR, Hall BD (1983) The primary structure of the alcohol dehydrogenase gene from the fission yeastSchizosaccharomyces pombe. J Biol Chem 258:143–149

    PubMed  Google Scholar 

  • Scherer S, Davis RW (1980) Recombination of dispersed repeated DNA sequences in yeast. Science 209:1380–1384

    PubMed  Google Scholar 

  • Smith MM (1984) The organization of the yeast histone genes. In: Stein GS, Stein JL, Marzluff WF (eds) Histone genes. John Wiley & Sons, New York, pp 3–33

    Google Scholar 

  • Smith MM, Andrésson ÓS (1983) DNA sequences of yeast H3 and H4 histone genes from two non-allelic gene sets encode identical H3 and H4 proteins. J Mol Biol 169:663–690

    PubMed  Google Scholar 

  • Smith MM, Murray K (1983) Yeast H3 and H4 histone messenger RNAs are transcribed from two non-allelic gene sets. J Mol Biol 169:641–661

    PubMed  Google Scholar 

  • Smith M, Leung DW, Gillam S, Astell CR, Montgomery DL, Hall BD (1979) Sequence of the gene for iso-1-cytochrome c inSaccharomyces cerevisiae. Cell 16:753–761

    PubMed  Google Scholar 

  • Stiles JI, Friedman LR, Sherman F (1981) Studies on transposable elements in yeast. II. Deletions, duplications, and transpositions of the COR segment that encompasses the structural gene of yeast iso-1-cytochrome c. Cold Spring Harbor Symp Quant Biol 45:602–607

    Google Scholar 

  • St John TP, Davis RW (1981) The organization and transcription of the galactose gene cluster ofSaccharomyces cerevisiae. J Mol Biol 152:285–315

    PubMed  Google Scholar 

  • St John TP, Scherer S, McDonell W, Davis RW (1981) Deletion analysis of theSaccharomyces GAL gene cluster. J Mol Biol 152:317–334

    PubMed  Google Scholar 

  • Strathern JN, Spatola E, McGill C, Hicks JB (1980) Structure and organization of transposable mating type cassettes inSaccharomyces cerevisiae. Proc Natl Acad Sci USA 77:2839–2843

    PubMed  Google Scholar 

  • Wilbur WJ, Lipman DJ (1983) Rapid similarity searches of nucleic acid and protein data banks. Proc Natl Acad Sci 80:726–730

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology, School of Medicine, University of Virginia, Box 441 Jordan Building, 22908, Charlottesville, Virginia, USA

    M. Mitchell Smith

Authors
  1. M. Mitchell Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Smith, M.M. Molecular evolution of theSaccharomyces cerevisiae histone gene loci. J Mol Evol 24, 252–259 (1987). https://doi.org/10.1007/BF02111238

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02111238

Key words

Search

Navigation