Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2003 Nov;165(3):975–983. doi: 10.1093/genetics/165.3.975

Evolution in Saccharomyces cerevisiae: identification of mutations increasing fitness in laboratory populations.

Victoria M Blanc 1, Julian Adams 1
PMCID: PMC1462841  PMID: 14668358

Abstract

Since the publication of the complete sequence of the genome of Saccharomyces cerevisiae, a number of comprehensive investigations have been initiated to gain insight into cellular function. The focus of these studies has been to identify genes essential for survival in specific environments or those that when mutated cause gross phenotypic defects in growth. Here we describe Ty1-based mutational approaches designed to identify genes, which when mutated generate evolutionarily significant phenotypes causing small but positive increments on fitness. As expected, Ty1 mutations with a positive fitness effect were in the minority. However, mutations in two loci, one inactivating FAR3 and one upstream of CYR1, identified in evolving populations, were shown to have small but significantly positive fitness effects.

Full Text

The Full Text of this article is available as a PDF (119.0 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997 Sep 1;25(17):3389–3402. doi: 10.1093/nar/25.17.3389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Boeke J. D., Eichinger D. J., Natsoulis G. Doubling Ty1 element copy number in Saccharomyces cerevisiae: host genome stability and phenotypic effects. Genetics. 1991 Dec;129(4):1043–1052. doi: 10.1093/genetics/129.4.1043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boeke J. D., Garfinkel D. J., Styles C. A., Fink G. R. Ty elements transpose through an RNA intermediate. Cell. 1985 Mar;40(3):491–500. doi: 10.1016/0092-8674(85)90197-7. [DOI] [PubMed] [Google Scholar]
  4. Casperson G. F., Walker N., Bourne H. R. Isolation of the gene encoding adenylate cyclase in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1985 Aug;82(15):5060–5063. doi: 10.1073/pnas.82.15.5060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cherkasova V., Lyons D. M., Elion E. A. Fus3p and Kss1p control G1 arrest in Saccharomyces cerevisiae through a balance of distinct arrest and proliferative functions that operate in parallel with Far1p. Genetics. 1999 Mar;151(3):989–1004. doi: 10.1093/genetics/151.3.989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Curcio M. J., Garfinkel D. J. Single-step selection for Ty1 element retrotransposition. Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):936–940. doi: 10.1073/pnas.88.3.936. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Eibel H., Philippsen P. Preferential integration of yeast transposable element Ty into a promoter region. 1984 Jan 26-Feb 1Nature. 307(5949):386–388. doi: 10.1038/307386a0. [DOI] [PubMed] [Google Scholar]
  9. Elion E. A., Brill J. A., Fink G. R. FUS3 represses CLN1 and CLN2 and in concert with KSS1 promotes signal transduction. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9392–9396. doi: 10.1073/pnas.88.21.9392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Farley F. W., Satterberg B., Goldsmith E. J., Elion E. A. Relative dependence of different outputs of the Saccharomyces cerevisiae pheromone response pathway on the MAP kinase Fus3p. Genetics. 1999 Apr;151(4):1425–1444. doi: 10.1093/genetics/151.4.1425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gartner A., Jovanović A., Jeoung D. I., Bourlat S., Cross F. R., Ammerer G. Pheromone-dependent G1 cell cycle arrest requires Far1 phosphorylation, but may not involve inhibition of Cdc28-Cln2 kinase, in vivo. Mol Cell Biol. 1998 Jul;18(7):3681–3691. doi: 10.1128/mcb.18.7.3681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gavin Anne-Claude, Bösche Markus, Krause Roland, Grandi Paola, Marzioch Martina, Bauer Andreas, Schultz Jörg, Rick Jens M., Michon Anne-Marie, Cruciat Cristina-Maria. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature. 2002 Jan 10;415(6868):141–147. doi: 10.1038/415141a. [DOI] [PubMed] [Google Scholar]
  13. Gietz R. D., Schiestl R. H., Willems A. R., Woods R. A. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast. 1995 Apr 15;11(4):355–360. doi: 10.1002/yea.320110408. [DOI] [PubMed] [Google Scholar]
  14. Goebl M. G., Petes T. D. Most of the yeast genomic sequences are not essential for cell growth and division. Cell. 1986 Sep 26;46(7):983–992. doi: 10.1016/0092-8674(86)90697-5. [DOI] [PubMed] [Google Scholar]
  15. Goffeau A., Barrell B. G., Bussey H., Davis R. W., Dujon B., Feldmann H., Galibert F., Hoheisel J. D., Jacq C., Johnston M. Life with 6000 genes. Science. 1996 Oct 25;274(5287):546, 563-7. doi: 10.1126/science.274.5287.546. [DOI] [PubMed] [Google Scholar]
  16. Horecka J., Sprague G. F., Jr Identification and characterization of FAR3, a gene required for pheromone-mediated G1 arrest in Saccharomyces cerevisiae. Genetics. 1996 Nov;144(3):905–921. doi: 10.1093/genetics/144.3.905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Iida H. Multistress resistance of Saccharomyces cerevisiae is generated by insertion of retrotransposon Ty into the 5' coding region of the adenylate cyclase gene. Mol Cell Biol. 1988 Dec;8(12):5555–5560. doi: 10.1128/mcb.8.12.5555. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ji H., Moore D. P., Blomberg M. A., Braiterman L. T., Voytas D. F., Natsoulis G., Boeke J. D. Hotspots for unselected Ty1 transposition events on yeast chromosome III are near tRNA genes and LTR sequences. Cell. 1993 Jun 4;73(5):1007–1018. doi: 10.1016/0092-8674(93)90278-x. [DOI] [PubMed] [Google Scholar]
  19. Kataoka T., Broek D., Wigler M. DNA sequence and characterization of the S. cerevisiae gene encoding adenylate cyclase. Cell. 1985 Dec;43(2 Pt 1):493–505. doi: 10.1016/0092-8674(85)90179-5. [DOI] [PubMed] [Google Scholar]
  20. Kim J. M., Vanguri S., Boeke J. D., Gabriel A., Voytas D. F. Transposable elements and genome organization: a comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res. 1998 May;8(5):464–478. doi: 10.1101/gr.8.5.464. [DOI] [PubMed] [Google Scholar]
  21. Kumar A., Cheung K. H., Ross-Macdonald P., Coelho P. S., Miller P., Snyder M. TRIPLES: a database of gene function in Saccharomyces cerevisiae. Nucleic Acids Res. 2000 Jan 1;28(1):81–84. doi: 10.1093/nar/28.1.81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ma D., Cook J. G., Thorner J. Phosphorylation and localization of Kss1, a MAP kinase of the Saccharomyces cerevisiae pheromone response pathway. Mol Biol Cell. 1995 Jul;6(7):889–909. doi: 10.1091/mbc.6.7.889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Maddock J. R., Roy J., Woolford J. L., Jr Six novel genes necessary for pre-mRNA splicing in Saccharomyces cerevisiae. Nucleic Acids Res. 1996 Mar 15;24(6):1037–1044. doi: 10.1093/nar/24.6.1037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Morishita T., Matsuura A., Uno I. Characterization of the cyr1-2 UGA mutation in Saccharomyces cerevisiae. Mol Gen Genet. 1993 Mar;237(3):463–466. doi: 10.1007/BF00279452. [DOI] [PubMed] [Google Scholar]
  25. Natsoulis G., Thomas W., Roghmann M. C., Winston F., Boeke J. D. Ty1 transposition in Saccharomyces cerevisiae is nonrandom. Genetics. 1989 Oct;123(2):269–279. doi: 10.1093/genetics/123.2.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ochman H., Gerber A. S., Hartl D. L. Genetic applications of an inverse polymerase chain reaction. Genetics. 1988 Nov;120(3):621–623. doi: 10.1093/genetics/120.3.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ross-Macdonald P., Coelho P. S., Roemer T., Agarwal S., Kumar A., Jansen R., Cheung K. H., Sheehan A., Symoniatis D., Umansky L. Large-scale analysis of the yeast genome by transposon tagging and gene disruption. Nature. 1999 Nov 25;402(6760):413–418. doi: 10.1038/46558. [DOI] [PubMed] [Google Scholar]
  28. Ross-Macdonald P., Coelho P. S., Roemer T., Agarwal S., Kumar A., Jansen R., Cheung K. H., Sheehan A., Symoniatis D., Umansky L. Large-scale analysis of the yeast genome by transposon tagging and gene disruption. Nature. 1999 Nov 25;402(6760):413–418. doi: 10.1038/46558. [DOI] [PubMed] [Google Scholar]
  29. Ross-Macdonald P., Sheehan A., Roeder G. S., Snyder M. A multipurpose transposon system for analyzing protein production, localization, and function in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1997 Jan 7;94(1):190–195. doi: 10.1073/pnas.94.1.190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Siebert P. D., Chenchik A., Kellogg D. E., Lukyanov K. A., Lukyanov S. A. An improved PCR method for walking in uncloned genomic DNA. Nucleic Acids Res. 1995 Mar 25;23(6):1087–1088. doi: 10.1093/nar/23.6.1087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Smith V., Botstein D., Brown P. O. Genetic footprinting: a genomic strategy for determining a gene's function given its sequence. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6479–6483. doi: 10.1073/pnas.92.14.6479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Smith V., Chou K. N., Lashkari D., Botstein D., Brown P. O. Functional analysis of the genes of yeast chromosome V by genetic footprinting. Science. 1996 Dec 20;274(5295):2069–2074. doi: 10.1126/science.274.5295.2069. [DOI] [PubMed] [Google Scholar]
  33. Thevelein J. M., de Winde J. H. Novel sensing mechanisms and targets for the cAMP-protein kinase A pathway in the yeast Saccharomyces cerevisiae. Mol Microbiol. 1999 Sep;33(5):904–918. doi: 10.1046/j.1365-2958.1999.01538.x. [DOI] [PubMed] [Google Scholar]
  34. Uetz P., Giot L., Cagney G., Mansfield T. A., Judson R. S., Knight J. R., Lockshon D., Narayan V., Srinivasan M., Pochart P. A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature. 2000 Feb 10;403(6770):623–627. doi: 10.1038/35001009. [DOI] [PubMed] [Google Scholar]
  35. Wach A., Brachat A., Pöhlmann R., Philippsen P. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast. 1994 Dec;10(13):1793–1808. doi: 10.1002/yea.320101310. [DOI] [PubMed] [Google Scholar]
  36. Wilke C. M., Adams J. Fitness effects of Ty transposition in Saccharomyces cerevisiae. Genetics. 1992 May;131(1):31–42. doi: 10.1093/genetics/131.1.31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wilke C. M., Heidler S. H., Brown N., Liebman S. W. Analysis of yeast retrotransposon Ty insertions at the CAN1 locus. Genetics. 1989 Dec;123(4):655–665. doi: 10.1093/genetics/123.4.655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Wilke C. M., Maimer E., Adams J. The population biology and evolutionary significance of Ty elements in Saccharomyces cerevisiae. Genetica. 1992;86(1-3):155–173. doi: 10.1007/BF00133718. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES