1887

Abstract

Exponential-phase yeast cells readily enter stationary phase when transferred to fresh, carbon-deficient medium, and can remain fully viable for up to several months. It is known that stationary-phase prokaryotic cells may still synthesize substantial amounts of DNA. Although the basis of this phenomenon remains unclear, this DNA synthesis may be the result of DNA maintenance and repair, recombination, and stress-induced transposition of mobile elements, which may occur in the absence of DNA replication. To the best of our knowledge, the existence of DNA turnover in stationary-phase unicellular eukaryotes remains largely unstudied. By performing cDNA-spotted (i.e. ORF) microarray analysis of stationary cultures of a haploid strain, we demonstrated on a genomic scale the localization of a DNA-turnover marker [5-bromo-2′-deoxyuridine (BrdU); an analogue of thymidine], indicative of DNA synthesis in discrete, multiple sites across the genome. Exponential-phase cells on the other hand, exhibited a uniform, total genomic DNA synthesis pattern, possibly the result of DNA replication. Interestingly, BrdU-labelled sites exhibited a significant overlap with highly expressed features. We also found that the distribution among chromosomes of BrdU-labelled and expressed features deviates from random distribution; this was also observed for the overlapping set. Ty retrotransposon genes were also found to be labelled with BrdU, evidence for transposition during stationary phase; however, they were not significantly expressed. We discuss the relevance and possible connection of these results to DNA repair, mutation and related phenomena in higher eukaryotes.

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2010-06-01
2020-08-13
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References

  1. Andalis A. A., Storchova Z., Styles C., Galitski T., Pellman D., Fink G. R.. 2004; Defects arising from whole-genome duplications in Saccharomyces cerevisiae. Genetics167:1109–1121
    [Google Scholar]
  2. Arava Y., Wang Y., Storey J. D., Liu C. L., Brown P. O., Herschlag D.. 2003; Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A100:3889–3894
    [Google Scholar]
  3. Ashrafi K., Sinclair D., Gordon J. I., Guarente L.. 1999; Passage through stationary phase advances replicative aging in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A96:9100–9105
    [Google Scholar]
  4. Benjamini Y., Hochberg Y.. 1995; Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol57:289–300
    [Google Scholar]
  5. Blow J. J., Hodgson B.. 2002; Replication licensing – defining the proliferative state?. Trends Cell Biol12:72–78
    [Google Scholar]
  6. Bolstad B. M., Irizarry R. A., Astrand M., Speed T. P.. 2003; A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics19:185–193
    [Google Scholar]
  7. Cairns J., Overbaugh J., Miller S.. 1988; The origin of mutants. Nature335:142–145
    [Google Scholar]
  8. Caporale L. H.. 1999; Chance favors the prepared genome. Ann N Y Acad Sci870:1–21
    [Google Scholar]
  9. Caporale L. H.. 2000; Mutation is modulated: implications for evolution. Bioessays22:388–395
    [Google Scholar]
  10. Caporale L. H.. 2003; Natural selection and the emergence of a mutation phenotype: an update of the evolutionary synthesis considering mechanisms that affect genome variation. Annu Rev Microbiol57:467–485
    [Google Scholar]
  11. Causton H. C., Ren B., Koh S. S., Harbison C. T., Kanin E., Jennings E. G., Lee T. I., True H. L., Lander E. S., Young R. A.. 2001; Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell12:323–337
    [Google Scholar]
  12. Chen Q., Ding Q., Keller J. N.. 2005; The stationary phase model of aging in yeast for the study of oxidative stress and age-related neurodegeneration. Biogerontology6:1–13
    [Google Scholar]
  13. Chevalier S., Blow J. J.. 1996; Cell cycle control of replication initiation in eukaryotes. Curr Opin Cell Biol8:815–821
    [Google Scholar]
  14. Cimbora D. M., Schubeler D., Reik A., Hamilton J., Francastel C., Epner E. M., Groudine M.. 2000; Long-distance control of origin choice and replication timing in the human β-globin locus are independent of the locus control region. Mol Cell Biol20:5581–5591
    [Google Scholar]
  15. Dai J., Xie W., Brady T. L., Gao J., Voytas D. F.. 2007; Phosphorylation regulates integration of the yeast Ty 5 retrotransposon into heterochromatin. Mol Cell27:289–299
    [Google Scholar]
  16. Datta A., Jinks-Robertson S.. 1995; Association of increased spontaneous mutation rates with high levels of transcription in yeast. Science268:1616–1619
    [Google Scholar]
  17. DeRisi J. L., Iyer V. R., Brown P. O.. 1997; Exploring the metabolic and genetic control of gene expression on a genomic scale. Science278:680–686
    [Google Scholar]
  18. Ebina H., Levin H. L.. 2007; Stress management: how cells take control of their transposons. Mol Cell27:180–181
    [Google Scholar]
  19. Finch C. E., Goodman M. F.. 1997; Relevance of ‘adaptive’ mutations arising in non-dividing cells of microorganisms to age-related changes in mutant phenotypes of neurons. Trends Neurosci20:501–507
    [Google Scholar]
  20. Foster P. L.. 1999; Mechanisms of stationary phase mutation: a decade of adaptive mutation. Annu Rev Genet33:57–88
    [Google Scholar]
  21. Fuge K., Werner-Washburne M.. 1997; Stationary phase in the yeast Saccharomyces cerevisiae. In Yeast Stress Responses pp53–69 Edited by Hohmann S., Mager W. H. Heidelberg: Springer;
  22. Gasch A. P., Werner-Washburne M.. 2002; The genomics of yeast responses to environmental stress and starvation. Funct Integr Genomics2:181–192
    [Google Scholar]
  23. Gasch A. P., Spellman P. T., Kao C. M., Carmel-Harel O., Eisen M. B., Storz G., Botstein D., Brown P. O.. 2000; Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell11:4241–4257
    [Google Scholar]
  24. Gershon H., Gershon D.. 2000; The budding yeast, Saccharomyces cerevisiae, as a model for aging research: a critical review. Mech Ageing Dev120:1–22
    [Google Scholar]
  25. Gray J. V., Petsko G. A., Johnston G. C., Ringe D., Singer R. A., Werner-Washburne M.. 2004; “Sleeping beauty”: quiescence in Saccharomyces cerevisiae. Microbiol Mol Biol Rev68:187–206
    [Google Scholar]
  26. Heidenreich E., Eisler H.. 2004; Non-homologous end joining dependency of γ-irradiation-induced adaptive frameshift mutation formation in cell cycle-arrested yeast cells. Mutat Res556:201–208
    [Google Scholar]
  27. Heidenreich E., Wintersberger U.. 2001; Adaptive reversions of a frameshift mutation in arrested Saccharomyces cerevisiae cells by simple deletions in mononucleotide repeats. Mutat Res473:101–107
    [Google Scholar]
  28. Heidenreich E., Novotny R., Kneidinger B., Holzmann V., Wintersberger U.. 2003; Non-homologous end joining as an important mutagenic process in cell cycle-arrested cells. EMBO J22:2274–2283
    [Google Scholar]
  29. Hohmann S., Mager W. H.. (editors) 1997; Yeast Stress Responses, 1st edn. Heidelberg: Springer;
  30. Kaiser C., Michaelis S., Mitchell A.. 1994; Methods in Yeast Genetics: a laboratory course manual (1994 edn) Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  31. Kandpal R. P., Kandpal G., Weissman S. M.. 1994; Construction of libraries enriched for sequence repeats and jumping clones, and hybridization selection for region-specific markers. Proc Natl Acad Sci U S A91:88–92
    [Google Scholar]
  32. Keshet I., Schlesinger Y., Farkash S., Rand E., Hecht M., Segal E., Pikarski E., Young R. A., Niveleau A.. other authors 2006; Evidence for an instructive mechanism of de novo methylation in cancer cells. Nat Genet38:149–153
    [Google Scholar]
  33. Kim N., Abdulovic A. L., Gealy R., Lippert M. J., Jinks-Robertson S.. 2007; Transcription-associated mutagenesis in yeast is directly proportional to the level of gene expression and influenced by the direction of DNA replication. DNA Repair (Amst6:1285–1296
    [Google Scholar]
  34. Lengronne A., Pasero P., Bensimon A., Schwob E.. 2001; Monitoring S phase progression globally and locally using BrdU incorporation in TK+ yeast strains. Nucleic Acids Res29:1433–1442
    [Google Scholar]
  35. Lindahl T.. 1993; Instability and decay of the primary structure of DNA. Nature362:709–715
    [Google Scholar]
  36. Martin D., Brun C., Remy E., Mouren P., Thieffry D., Jacq B.. 2004; GOToolBox: functional analysis of gene datasets based on Gene Ontology. Genome Biol5:R101
    [Google Scholar]
  37. Nouspikel T., Hanawalt P. C.. 2002; DNA repair in terminally differentiated cells. DNA Repair (Amst ) 1:59–75
    [Google Scholar]
  38. Nouspikel T. P., Hyka-Nouspikel N., Hanawalt P. C.. 2006; Transcription domain-associated repair in human cells. Mol Cell Biol26:8722–8730
    [Google Scholar]
  39. Selby C. P., Sancar A.. 1994; Mechanisms of transcription–repair coupling and mutation frequency decline. Microbiol Rev58:317–329
    [Google Scholar]
  40. Singer B., Kuśmierek J. T.. 1982; Chemical mutagenesis. Annu Rev Biochem51:655–693
    [Google Scholar]
  41. Todeschini A. L., Morillon A., Springer M., Lesage P.. 2005; Severe adenine starvation activates Ty1 transcription and retrotransposition in Saccharomyces cerevisiae. Mol Cell Biol25:7459–7472
    [Google Scholar]
  42. Uppuluri P., Chaffin W. L.. 2007; Defining Candida albicans stationary phase by cellular and DNA replication, gene expression and regulation. Mol Microbiol64:1572–1586
    [Google Scholar]
  43. Weiner A. M.. 2002; SINEs and LINEs: the art of biting the hand that feeds you. Curr Opin Cell Biol14:343–350
    [Google Scholar]
  44. Werner-Washburne M., Braun E. L., Crawford M. E., Peck V. M.. 1996; Stationary phase in Saccharomyces cerevisiae. Mol Microbiol19:1159–1166
    [Google Scholar]
  45. Wierdl M., Greene C. N., Datta A., Jinks-Robertson S., Petes T. D.. 1996; Destabilization of simple repetitive DNA sequences by transcription in yeast. Genetics143:713–721
    [Google Scholar]
  46. Wright B. E.. 2004; Stress-directed adaptive mutations and evolution. Mol Microbiol52:643–650
    [Google Scholar]
  47. Wright B. E., Longacre A., Reimers J. M.. 1999; Hypermutation in derepressed operons of Escherichia coli K12. Proc Natl Acad Sci U S A96:5089–5094
    [Google Scholar]
  48. Wright B. E., Schmidt K. H., Minnick M. F.. 2004; Mechanisms by which transcription can regulate somatic hypermutation. Genes Immun5:176–182
    [Google Scholar]
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