Abstract
We have analyzed all di-, tri-, and tetranucleotide repeats in the partially sequenced genomes of 13 hemiascomycetous yeast species, and compared their sequences, lengths, and distributions to those observed in the genome of Saccharomyces cerevisiae. We found that most of the 13 species exhibit a unique distribution of microsatellites, not correlated to the base composition of their genome. Species close to S. cerevisiae exhibit a similar distribution, while species more distantly related show a more divergent distribution. We propose that de novo formation and continuous loss of microsatellites are active processes generating new DNA sequences. We also show that hemiascomycete-specific genes encoding transcription factors contain trinucleotide repeats more frequently than expected from their average frequency distribution. These transcription factors might play an important role in the speciation process, by regulating gene expression through DNA–protein or protein–protein interactions mediated by stretches of charged amino acids encoded by trinucleotide repeats.
Similar content being viewed by others
References
MM Alba MF Santibanez-Koref JM Hancock (1999) ArticleTitleAmino acid reiterations in yeast are overrepresented in particular classes of proteins and show evidence of a slippage-like mutational process. J Moll Evol 49 789–797 Occurrence Handle1:CAS:528:DC%2BD3cXks1Gq
AL Bacon SM Farrington MG Dunlop (2000) ArticleTitleSequence interruptions confer differential stability at microsatellite alleles in mismatch repair-deficient cells. Hum Mol Genet 9 2707–2713 Occurrence Handle1:CAS:528:DC%2BD3cXosVKktbo%3D Occurrence Handle11063729
G Benson MS Waterman (1994) ArticleTitleA method for fast database search for all k-nucleotide repeats. Nuc Acids Res 22 4828–4836 Occurrence Handle1:CAS:528:DyaK2MXitlSns74%3D
J Bowers J-M Boursiquot P This K Chu H Johansson C Meredith (1999) ArticleTitleHistorical genetics: the parentage of Chardonnay, Gamay, and other wine grapes of northeastern France. Science 285 1562–1565 Occurrence Handle10.1126/science.285.5433.1562 Occurrence Handle1:CAS:528:DyaK1MXlslOrt7g%3D Occurrence Handle10477519
B Charlesworth P Sniegowski W Stephan (1994) ArticleTitleThe evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371 215–220 Occurrence Handle1:CAS:528:DyaK2cXmt1emu7o%3D Occurrence Handle8078581
H Debrauwère CG Gendrel S Lechat M Dutreix (1997) ArticleTitleDifferences and similarities between various tandem repeat sequences: minisatellites and microsatellites. Biochimie 79 577–586 Occurrence Handle9466695
C Dib S Faure C Fizames D Samson N Drouot A Vignal et al. (1996) ArticleTitleA comprehensive genetic map of the human genome based on 5,264 sequences. Nature 380 152–154 Occurrence Handle8600387
C Hennequin A Thierry G-F Richard G Lecointre HV Nguyen C Gaillardin B Dujon (2001) ArticleTitleMicrosatellite typing as a new tool for identification of Saccharomyces cerevisiae strains. J Clin Microbiol 39 551–559 Occurrence Handle1:CAS:528:DC%2BD3MXhtlGrtb0%3D Occurrence Handle11158105
H Innan R Terauchi NT Miyashita (1997) ArticleTitleMicrosatellite polymorphism in natural populations of the wild plant Arabidopsis thaliana. Genetics 146 1441–1452 Occurrence Handle1:STN:280:ByiH3czjtFM%3D Occurrence Handle9258686
S Karlin C Burge (1996) ArticleTitleTrinucleotide repeats and long homopeptides in genes and proteins associated with nervous system disease and development. Proc Natl Acad Sci USA 93 1560–1565 Occurrence Handle1:CAS:528:DyaK28Xht1ensbc%3D Occurrence Handle8643671
RJ Kokoska L Stefanovic AB Buermeyer RM Liskay TD Petes (1999) ArticleTitleA mutation of the yeast gene encoding PCNA destabilizes both microsatellite and minisatellite DNA sequences. Genetics 151 511–519 Occurrence Handle1:CAS:528:DyaK1MXhtlChu7k%3D Occurrence Handle9927447
RJ Kokoska L Stefanovic HT Tran MA Resnick DA Gordenin TD Petes (1998) ArticleTitleDestabilization of yeast micro- and minisatellite DNA sequences by mutations affecting a nuclease involved in Okazaki fragment processing (rad27) and DNA polymerase δ (pol3-t). Mol Cell Biol 18 2779–2788 Occurrence Handle1:CAS:528:DyaK1cXis1Gnu7w%3D Occurrence Handle9566897
AT Lloyd PM Sharp (1992) ArticleTitleEvolution of codon usage patterns: the extent and nature of divergence between Candida albicans and Saccharomyces cerevisiae. Nuc Acids Res 20 5289–5295 Occurrence Handle1:CAS:528:DyaK3sXjtlyqsA%3D%3D
FV Lunel L Licciardello S Stefani HA Verbrugh W Melchers JF Meis et al. (1998) ArticleTitleLack of consistent short sequence repeat polymorphisms in genetically homologous colonizing and invasive Candida albicans strains. J Bacteriol 180 3771–3778 Occurrence Handle1:CAS:528:DyaK1cXlt1ChsLw%3D Occurrence Handle9683470
A Malpertuy F Tekaia S Casaregola M Aigle F Artiguenave G Blandin et al. (2000) ArticleTitleGenomic exploration of the hemiascomycetous yeasts: 19. Ascomycetes-specific genes. FEBS Lett 487 113–121 Occurrence Handle10.1016/S0014-5793(00)02290-0 Occurrence Handle1:CAS:528:DC%2BD3MXisVSmtg%3D%3D Occurrence Handle11152894
HT Orr (2001) ArticleTitleBeyond the Qs in the polyglutamine diseases. Genes Dev 15 925–932 Occurrence Handle1:CAS:528:DC%2BD3MXjtVOku7w%3D Occurrence Handle11316786
SB Prusiner MR Scott SJ DeArmond FE Cohen (1998) ArticleTitlePrion protein biology. Cell 93 337–348 Occurrence Handle1:CAS:528:DyaK1cXjtFCjtLw%3D Occurrence Handle9590169
G-F Richard B Dujon (1996) ArticleTitleDistribution and variability of trinucleotide repeats in the genome of the yeast Saccharomyces cerevisiae. Gene 174 165–174 Occurrence Handle1:CAS:528:DyaK28XmtV2iur8%3D Occurrence Handle8863744
G-F Richard B Dujon (1997) ArticleTitleTrinucleotide repeats in yeast. Res Microbiol 148 731–744 Occurrence Handle1:CAS:528:DyaK1cXptlGnsg%3D%3D Occurrence Handle9765857
G-F Richard C Hennequin A Thierry B Dujon (1999) ArticleTitleTrinucleotide repeats and other microsatellites in yeasts. Res Microbiol 150 589–602 Occurrence Handle1:CAS:528:DC%2BD3cXoslWnsQ%3D%3D Occurrence Handle10672999
G-F Richard F Pâques (2000) ArticleTitleMini- and microsatellite expansions: the recombination connection. EMBO Reports 1 122–126 Occurrence Handle1:CAS:528:DC%2BD3cXnt1yrs7c%3D Occurrence Handle11265750
RI Richards (2001) ArticleTitleDynamic mutations: a decade of unstable expanded repeats in human genetic disease. Hum Mol Genet 10 2187–2194
MS Röder V Korzun K Wendehake J Plaschke M-H Tixier P Leroy MW Ganal (1998) ArticleTitleA microsatellite map of wheat. Genetics 149 2007–2023 Occurrence Handle9691054
T Sakamoto RG Danzmann K Gharbi P Howard A Ozaki SK Khoo et al. (2000) ArticleTitleA microsatellite linkage map of rainbow trout (Oncorhynchus mykiss) characterized by large sex-specific differences in recombination rates. Genetics 155 1331–1345 Occurrence Handle1:CAS:528:DC%2BD3cXlsFSku7Y%3D Occurrence Handle10880492
A Santoso P Chien LZ Osherovich JS Weissman (2000) ArticleTitleMolecular basis of a yeast prion species barrier. Cell 100 277–288 Occurrence Handle1:CAS:528:DC%2BD3cXotFChug%3D%3D Occurrence Handle10660050
E Scherzinger R Lurz M Turmaine L Mangiarini B Hollenbach R Hasenbank et al. (1997) ArticleTitleHuntingtin-encoded polyglutamine expansions form amyloid-like protein aggregates in vitro and in vivo. Cell 90 549–558 Occurrence Handle1:CAS:528:DyaK2sXlsVKrsL4%3D Occurrence Handle9267034
J Souciet M Aigle F Artiguenave G Blandin M Bolotin-Fukuhara E Bon et al. (2000) ArticleTitleGenomic exploration of the hemiascomycetous yeasts: 1. A set of yeast species for molecular evolution studies. FEBS Lett 487 3–12 Occurrence Handle11152876
M Strand TA Prolla RM Liskay TD Petes (1993) ArticleTitleDestabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair. Nature 365 274–276 Occurrence Handle1:CAS:528:DyaK3sXms1equr0%3D Occurrence Handle8371783
F Tekaia G Blandin A Malpertuy B Llorente P Durrens C Toffano-Nioche et al. (2000) ArticleTitleGenomic exploration of the hemiascomycetous yeasts: 3. Methods and strategies used for sequence analysis and annotation. FEBS 487 17–30 Occurrence Handle1:CAS:528:DC%2BD3MXisVSgug%3D%3D Occurrence Handle11152878
G Toth Z Gaspari J Jurka (2000) ArticleTitleMicrosatellites in different eukaryotic genomes: survey and analysis. Genome Res 10 967–981 Occurrence Handle10899146
HT Tran JD Keen M Kricker MA Resnick DA Gordenin (1997) ArticleTitleHypermutability of homonucleotide runs in mismatch repair and DNA polymerase proofreading yeast mutants. Mol Cell Biol 17 2859–2865 Occurrence Handle1:CAS:528:DyaK2sXislCms7g%3D Occurrence Handle9111358
M Wierdl M Dominska TD Petes (1997) ArticleTitleMicrosatellite instability in yeast: dependence on the length of the microsatellite. Genetics 146 769–779 Occurrence Handle1:CAS:528:DyaK2sXmsVartLw%3D Occurrence Handle9215886
X Xu M Peng Z Fang X Xu (2000) ArticleTitleThe direction of microsatellite mutations is dependent upon allele length. Nat Genet 24 396–399 Occurrence Handle10.1038/74238 Occurrence Handle1:CAS:528:DC%2BD3cXisVCjsbc%3D Occurrence Handle10742105
ET Young JS Sloan K Van Riper (2000) ArticleTitleTrinucleotide repeats are clustered in regulatory genes in Saccharomyces cerevisiae. Genetics 154 1053–1068 Occurrence Handle1:CAS:528:DC%2BD3cXitVOiu7k%3D Occurrence Handle10757753
Y Zhu DC Queller JE Strassmann (2000) ArticleTitleA phylogenetic perspective on sequence evolution in microsatellite loci. J Mol Evol 50 324–338 Occurrence Handle1:CAS:528:DC%2BD3cXivFyjtbc%3D Occurrence Handle10795824
Acknowledgements
We are grateful to our colleagues of the Génolevures project (http://cbi.labri.u-bordeaux.fr/Genolevures ) for giving us access to their sequence data before publication. We thank Florence Ricard, Gäelle Blandin, and Fredj Tekaia for excellent computer assistance and our colleagues of the Unité de Génétique Moléculaire des Levures for fruitful discussions. This work was supported by CNRS as part of the GDR 2354. B.D. is a member of the Institut Universitaire de France.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Malpertuy, A., Dujon, B. & Richard, GF. Analysis of Microsatellites in 13 Hemiascomycetous Yeast Species: Mechanisms Involved in Genome Dynamics . J Mol Evol 56, 730–741 (2003). https://doi.org/10.1007/s00239-002-2447-5
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s00239-002-2447-5