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. 2004 Jul;167(3):1109–1121. doi: 10.1534/genetics.104.029256

Defects arising from whole-genome duplications in Saccharomyces cerevisiae.

Alex A Andalis 1, Zuzana Storchova 1, Cora Styles 1, Timothy Galitski 1, David Pellman 1, Gerald R Fink 1
PMCID: PMC1470947  PMID: 15280227

Abstract

Comparisons among closely related species have led to the proposal that the duplications found in many extant genomes are the remnants of an ancient polyploidization event, rather than a result of successive duplications of individual chromosomal segments. If this interpretation is correct, it would support Ohno's proposal that polyploidization drives evolution by generating the genetic material necessary for the creation of new genes. Paradoxically, analysis of contemporary polyploids suggests that increased ploidy is an inherently unstable state. To shed light on this apparent contradiction and to determine the effects of nascent duplications of the entire genome, we generated isogenic polyploid strains of the budding yeast Saccharomyces cerevisiae. Our data show that an increase in ploidy results in a marked decrease in a cell's ability to survive during stationary phase in growth medium. Tetraploid cells die rapidly, whereas isogenic haploids remain viable for weeks. Unlike haploid cells, which arrest growth as unbudded cells, tetraploid cells continue to bud and form mitotic spindles in stationary phase. The stationary-phase death of tetraploids can be prevented by mutations or conditions that result in growth arrest. These data show that whole-genome duplications are accompanied by defects that affect viability and subsequent survival of the new organism.

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Selected References

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

  1. Adams I. R., Kilmartin J. V. Spindle pole body duplication: a model for centrosome duplication? Trends Cell Biol. 2000 Aug;10(8):329–335. doi: 10.1016/s0962-8924(00)01798-0. [DOI] [PubMed] [Google Scholar]
  2. Brandriss M. C., Magasanik B. Genetics and physiology of proline utilization in Saccharomyces cerevisiae: mutation causing constitutive enzyme expression. J Bacteriol. 1979 Nov;140(2):504–507. doi: 10.1128/jb.140.2.504-507.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Byers B., Goetsch L. Behavior of spindles and spindle plaques in the cell cycle and conjugation of Saccharomyces cerevisiae. J Bacteriol. 1975 Oct;124(1):511–523. doi: 10.1128/jb.124.1.511-523.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Costigan C., Snyder M. SLK1, a yeast homolog of MAP kinase activators, has a RAS/cAMP-independent role in nutrient sensing. Mol Gen Genet. 1994 May 10;243(3):286–296. doi: 10.1007/BF00301064. [DOI] [PubMed] [Google Scholar]
  5. Crouzet M., Urdaci M., Dulau L., Aigle M. Yeast mutant affected for viability upon nutrient starvation: characterization and cloning of the RVS161 gene. Yeast. 1991 Oct;7(7):727–743. doi: 10.1002/yea.320070708. [DOI] [PubMed] [Google Scholar]
  6. DeRisi J. L., Iyer V. R., Brown P. O. Exploring the metabolic and genetic control of gene expression on a genomic scale. Science. 1997 Oct 24;278(5338):680–686. doi: 10.1126/science.278.5338.680. [DOI] [PubMed] [Google Scholar]
  7. Eisen M. B., Spellman P. T., Brown P. O., Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):14863–14868. doi: 10.1073/pnas.95.25.14863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fabrizio P., Pozza F., Pletcher S. D., Gendron C. M., Longo V. D. Regulation of longevity and stress resistance by Sch9 in yeast. Science. 2001 Apr 5;292(5515):288–290. doi: 10.1126/science.1059497. [DOI] [PubMed] [Google Scholar]
  9. Feldman M., Liu B., Segal G., Abbo S., Levy A. A., Vega J. M. Rapid elimination of low-copy DNA sequences in polyploid wheat: a possible mechanism for differentiation of homoeologous chromosomes. Genetics. 1997 Nov;147(3):1381–1387. doi: 10.1093/genetics/147.3.1381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Galitski T., Saldanha A. J., Styles C. A., Lander E. S., Fink G. R. Ploidy regulation of gene expression. Science. 1999 Jul 9;285(5425):251–254. doi: 10.1126/science.285.5425.251. [DOI] [PubMed] [Google Scholar]
  11. Gibson T. J., Spring J. Evidence in favour of ancient octaploidy in the vertebrate genome. Biochem Soc Trans. 2000 Feb;28(2):259–264. doi: 10.1042/bst0280259. [DOI] [PubMed] [Google Scholar]
  12. Gietz D., St Jean A., Woods R. A., Schiestl R. H. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 1992 Mar 25;20(6):1425–1425. doi: 10.1093/nar/20.6.1425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Guo M., Davis D., Birchler J. A. Dosage effects on gene expression in a maize ploidy series. Genetics. 1996 Apr;142(4):1349–1355. doi: 10.1093/genetics/142.4.1349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kellis Manolis, Birren Bruce W., Lander Eric S. Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature. 2004 Mar 7;428(6983):617–624. doi: 10.1038/nature02424. [DOI] [PubMed] [Google Scholar]
  15. Lin H., de Carvalho P., Kho D., Tai C. Y., Pierre P., Fink G. R., Pellman D. Polyploids require Bik1 for kinetochore-microtubule attachment. J Cell Biol. 2001 Dec 24;155(7):1173–1184. doi: 10.1083/jcb.200108119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Mittelsten Scheid O., Jakovleva L., Afsar K., Maluszynska J., Paszkowski J. A change of ploidy can modify epigenetic silencing. Proc Natl Acad Sci U S A. 1996 Jul 9;93(14):7114–7119. doi: 10.1073/pnas.93.14.7114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ohno S., Wolf U., Atkin N. B. Evolution from fish to mammals by gene duplication. Hereditas. 1968;59(1):169–187. doi: 10.1111/j.1601-5223.1968.tb02169.x. [DOI] [PubMed] [Google Scholar]
  18. Ozkan H., Levy A. A., Feldman M. Allopolyploidy-induced rapid genome evolution in the wheat (Aegilops-Triticum) group. Plant Cell. 2001 Aug;13(8):1735–1747. doi: 10.1105/TPC.010082. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Shaked H., Kashkush K., Ozkan H., Feldman M., Levy A. A. Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. Plant Cell. 2001 Aug;13(8):1749–1759. doi: 10.1105/TPC.010083. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Sobering Andrew K., Jung Un Sung, Lee Kyung S., Levin David E. Yeast Rpi1 is a putative transcriptional regulator that contributes to preparation for stationary phase. Eukaryot Cell. 2002 Feb;1(1):56–65. doi: 10.1128/EC.1.1.56-65.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Song K., Lu P., Tang K., Osborn T. C. Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):7719–7723. doi: 10.1073/pnas.92.17.7719. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Tyers M., Tokiwa G., Futcher B. Comparison of the Saccharomyces cerevisiae G1 cyclins: Cln3 may be an upstream activator of Cln1, Cln2 and other cyclins. EMBO J. 1993 May;12(5):1955–1968. doi: 10.1002/j.1460-2075.1993.tb05845.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Werner-Washburne M., Braun E., Johnston G. C., Singer R. A. Stationary phase in the yeast Saccharomyces cerevisiae. Microbiol Rev. 1993 Jun;57(2):383–401. doi: 10.1128/mr.57.2.383-401.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Wodicka L., Dong H., Mittmann M., Ho M. H., Lockhart D. J. Genome-wide expression monitoring in Saccharomyces cerevisiae. Nat Biotechnol. 1997 Dec;15(13):1359–1367. doi: 10.1038/nbt1297-1359. [DOI] [PubMed] [Google Scholar]
  25. de Nobel J. G., Klis F. M., Priem J., Munnik T., van den Ende H. The glucanase-soluble mannoproteins limit cell wall porosity in Saccharomyces cerevisiae. Yeast. 1990 Nov-Dec;6(6):491–499. doi: 10.1002/yea.320060606. [DOI] [PubMed] [Google Scholar]

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