Skip to main content
SpringerLink
Log in

Prevalence and distribution of introns in non-ribosomal protein genes of yeast

  • Original Paper
  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Abstract

Relatively few genes in the yeast Saccharornyces cerevisiae are known to contain intervening sequences. As a group, yeast ribosomal protein genes exhibit a higher prevalence of introns when compared to non-ribosomal protein genes. In an effort to quantify this bias we have estimated the prevalence of intron sequences among non-ribosomal protein genes by assessing the number of prp2-sensitive mRNAs in an in vitro translation assay. These results, combined with an updated survey of the GenBank DNA database, support an estimate of 2.5% for intron-containing non-ribosomal protein genes. Furthermore, our observations reveal an intriguing distinction between the distributions of ribosomal protein and non-ribosomal protein intron lengths, suggestive of distinct, gene class-specific evolutionary pressures.

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

  • Chen J-H, Lin J-R (1990) The yeast PRP2 protein, a putative RNA-dependent ATPase, shares extensive sequence homology with two other pre-mRNA splicing factors. Nucleic Acids Res 18:6447

    Google Scholar 

  • Dabeva MD, Post-Beittenmiller MA, Warner JR (1986) Autogenous regulation of the transcript of a yeast ribosomal protein gene. Proc Nat Acad Sci USA 83:5854–5857

    Google Scholar 

  • Derr LK, Strathern JN (1993) A role for reverse transcripts in gene conversion. Nature 361:170–173

    Google Scholar 

  • Derr LK, Strathern JN, Garfinkel DJ (1991) RNA-mediated recombination in S. cerevisiae. Cell 67:355–364

    Google Scholar 

  • Eng FA, Warner JR (1991) Structural basis for the regulation of splicing of a yeast messenger RNA. Cell 65:797–804

    Google Scholar 

  • Engebrecht J, Voelkel-Meiman K, Roeder GS (1991) Meiosisspecific RNA splicing in yeast. Cell 66:1257–1268

    Google Scholar 

  • Fink GR (1987) Pseudogenes in yeast? Cell 49:5–6

    Google Scholar 

  • Frank D, Guthrie C (1992) An essential splicing factor, SLU7, mediates 3′ splice-site choice in yeast. Genes Dev 6:2112–2124

    Google Scholar 

  • Goguel V, Rosbash M (1993) Splice site choice and splicing efficiency are positively influenced by pre-mRNA intramolecular base-pairing in yeast. Cell 72:893–901

    Google Scholar 

  • Gurr SJ, Unkles SE, Kinghorn JR (1987) The structure and function of nuclear genes of filamentous fungi. In: Kinghorn JR (ed) Gene structure in eukaryotic microbes. IRL Press, Oxford, England, pp 93–139

    Google Scholar 

  • Hawkins JD (1988) A survey on intron and exon lengths. Nucleic Acids Res 16:9893–9908

    Google Scholar 

  • Iggo RD, Jamieson DJ, MacNeill SA, Southgate J, McPheat J, Lane DP (1991) p68 RNA helicase: identification of a nucleolar form and cloning of related genes containing a conserved intron in yeasts. Mol Cell Biol 11:1326–1333

    Google Scholar 

  • Jank B, Waldherr M, Schweyen RJ (1993) Yeast single copy gene URP1 is a homolog of rat ribosomal protein gene L21. Curr Genet 23:15–81

    Google Scholar 

  • Kis S-H, Smith J, Claude A, Lin R-J (1992) The purified yeast pre-RNA splicing factor PRP2 is an RNA-dependent NT-Pase. EMBO J 11:2319–2326

    Google Scholar 

  • Klinz F-J, Gallwitz D (1985) Size and position of intervening sequences are critical for splicing efficiency of pre-mRNA in the yeast Saccharomyces cerevisiae. Nucleic Acids Res 13:3791–3804

    Google Scholar 

  • Konarska MM, Padgett RA, Sharp PA (1984) Recognition of cap structures in splicing in vitro of mRNA precursors. Cell 38:731–736

    Google Scholar 

  • Lin R-J, Lusting AJ, Abelson J (1987) Splicing of yeast nuclear pre-mRNA in vitro requires a functional 40S spliceosome and several extrinsic factors. Genes Dev 1:7–18

    Google Scholar 

  • Lusting AJ, Lin R-J, Abelson J (1986) The yeast RNA gene products are essential for mRNA splicing in vitro. Cell 47:953–963

    Google Scholar 

  • Metz LJ, Bogorad L (1974) Two dimensional polyacrylamide gel electrophoresis: an improved method for ribosomal proteins. Anal Biochem 57:200–210

    Google Scholar 

  • Mizuta K, Hashimoto T, Suzuki K, Otaka E (1991a) Yeast ribosomal proteins: XII. YS11 of Saccharomyces cerevisiae is a homolog to E. coli S4 according to the gene analysis. Nucleic Acids Res 19:2603–2608

    Google Scholar 

  • Mizuta K, Hashimoto T, Otaka E (1991b) Yeast ribosomal proteins: XIII. Saccharomyces cerevisiae YL8A gene interrupted with two introns, encodes a homolog of mammalian L7. Nucleic Acids Res 20:1011–1016

    Google Scholar 

  • O'Farrell PA (1975) High resolution two dimensional electrophoresis of proteins. J Biol Chem 250:4007–4021

    Google Scholar 

  • Oliver SG et al. (1992) The complete DNA sequence of yeast chromosome III. Nature 357:38–46

    Google Scholar 

  • Olsen MV (1991) Genome structure and organization in Saccharomyces cerevisiae. In. Broach JR, Pringle JR, Jones EW (eds) The molecular and cellular biology of the yeast Saccharomyces: dynamics, protein synthesis and energetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York pp 1–40

    Google Scholar 

  • Parker R, Patterson B (1987) Architecture of fungal introns: Implications for spliceosome assembly. In: Inomye M, Dudock BS (eds) Molecular biology of RNA: new perspectives. Academic Press, San Diego, pp 133–149

    Google Scholar 

  • Pikielny CW, Rosbash M (1985) mRNA splicing efficiency in yeast and the contributions of nonconserved sequences. Cell 41:119–126

    Google Scholar 

  • Pikielny CW, Teem JL, Rosbash M (1983) Evidence for the biochemical role of an internal sequence in yeast nuclear mRNA introns: implications for U1 RNA and metazoan mRNA splicing. Cell 34:395–403

    Google Scholar 

  • Roberts BE, Paterson BM (1973) Efficient translation of tobacco mosaic virus RNA and rabbit globin 9S RNA in a cell-free system from commercial wheat germ. Proc Nat Acad Sci USA 70:2330–2334

    Google Scholar 

  • Rosbash M, Harris PKW, Woolford JL Jr, Teem JL (1981) The effect of temperature-sensitive RNA mutants on the transcription products from cloned ribosomal protein genes of yeast. Cell 24:679–686

    Google Scholar 

  • Ruby SW, Abelson J (1991) Pre-mRNA splicing in yeast. Trends Genet 7:79–85

    Google Scholar 

  • Rymond BC, Rosbash M (1992) Yeast pre-mRNA splicing. Saccharomyces cerevisiae. In: Broach JR, Pringle JR, Jones EW (eds) The molecular and cellular biology of the yeast Saccharomyces: gene expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, pp 143–192

    Google Scholar 

  • Santangelo GM, Tornow J, McLaughlin CS, Moldave K (1991) Screening a yeast promoter library leads to the isolation of the RP29/L32 and SNR17B/RPL37A divergent promoters and the discovery of a gene encoding ribosomal protein L37. Gene 105:137–138

    Google Scholar 

  • Suzuki K, Otaka E (1993a) GenBank accession D14676

  • Suzuki K, Otaka E (1993b) GenBank accession D14677

  • Swida U, Thuroff E, Kaufer NF (1986) Intron mutations that affect the splicing of the CYH2 gene of Saccharomyces cerevisiae. Mol Gen Genet 203:300–304

    Google Scholar 

  • Teem JL, Rosbash M (1983) Expression of a β-galactosidase gene containing the ribosomal protein 51 intron is sensitive to the rna2 mutation of yeast. Proc Natl Acad Sci USA 80:4403–4407

    Google Scholar 

  • Thompson-Jager S, Domdey H (1987) Yeast pre-mRNA splicing requires a minimum distance between the 5′ splice site and the internal branch acceptor site. Mol Cell Biol 7:4010–4016

    Google Scholar 

  • Tomiyoshi A, Suzuki K, Otaka E (1993) GenBank accession D14675

  • Warner JR, Gorenstein, C (1977) The synthesis of eukaryotic ribosomal proteins in vitro. Cell 11:201–212

    Google Scholar 

  • Woolford JL (1989) Nuclear pre-mRNA splicing in yeast. Yeast 5:439–458

    Google Scholar 

  • Woolford JL Jr, Warner JR (1991) The ribosome and its synthesis. In Saccharomyces cerevisiae. In: Broach JR, Pringe JR, Jones EW (eds) The molecular and cellular biology of the yeast Saccharomyces: dynamics, protein synthesis and energetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, pp 587–626

    Google Scholar 

  • Yean S-L, Lin R-J (1991) U4 small nuclear RNA dissociates from a yeast spliceosome and does not participate in subsequent splicing reaction. Mol Cell Biol 11:5571–5577

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry, University of Puerto Rico, Medical Sciences Campus, P.O. Box 365067, 00936-5067, San Juan, Puerto Rico, USA

    Jose R. Rodriguez-Medina

  2. T. H. Morgan School of Biological Sciences, Molecular and Cell Biology Group, University of Kentucky, 101 Morgan Building, 40506-0225, Lexington, Kentucky, USA

    Brian C. Rymond

Authors
  1. Jose R. Rodriguez-Medina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brian C. Rymond
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by W. Gaiewski

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rodriguez-Medina, J.R., Rymond, B.C. Prevalence and distribution of introns in non-ribosomal protein genes of yeast. Molec. Gen. Genet. 243, 532–539 (1994). https://doi.org/10.1007/BF00284201

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00284201

Key words

Search

Navigation