Skip to main content
SpringerLink
Log in
Book cover

Subtelomeres pp 39–70Cite as

Subtelomeric Regions Promote Evolutionary Innovation of Gene Families in Yeast

  • Chapter
  • First Online:

Abstract

Subtelomeres, the regions proximal to telomeres, are extremely dynamic parts of eukaryotic genomes. Gene families that reside in subtelomeres differ profoundly from non-subtelomeric gene families: they show increased recombination and duplication rates and often reflect the lifestyle of the organism under study. In the baker’s yeast Saccharomyces cerevisiae, subtelomeric gene families can be classified into three broad categories: genes involved in the utilization of alternative substrates, adhesion genes, and lastly, poorly characterized genes. Although the mechanisms shaping these gene families are not yet completely unraveled, studies on two typical subtelomeric gene families exemplify how the dynamic nature of chromosome ends can be exploited to rapidly evolve and diversify. Gene duplication has driven the evolution of the MAL gene families and provided closely related yeast species with appropriate, environment-specific alleles to metabolize various disaccharides. A second subtelomeric gene family, the adhesion (FLO) genes, shows frequent intergenic recombination between different FLO copies, thereby creating new FLO alleles with distinct adhesive properties. Moreover, stochastic transcriptional silencing and desilencing of subtelomeric genes could allow cells to ‘test’ these newly evolved genes without committing all cells in a population to the same fate.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Abramova, N., Sertil, O., Mehta, S., & Lowry, C. V. (2001). Reciprocal regulation of anaerobic and aerobic cell wall mannoprotein gene expression in Saccharomyces cerevisiae. Journal of Bacteriology, 183, 2881–2887.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ai, W., Bertram, P. G., Tsang, C. K., Chan, T. F., & Zheng, X. F. (2002). Regulation of subtelomeric silencing during stress response. Molecular Cell, 10, 1295–1305.

    CAS  PubMed  Google Scholar 

  • Alimardani, P., Regnacq, M., Moreau-Vauzelle, C., Ferreira, T., Rossignol, T., Blondin, B., et al. (2004). SUT1-promoted sterol uptake involves the ABC transporter Aus1 and the mannoprotein Dan1 whose synergistic action is sufficient for this process. The Biochemical Journal, 381, 195–202.

    CAS  PubMed  Google Scholar 

  • Andrau, J. C., van de Pasch, L., Lijnzaad, P., Bijma, T., Koerkamp, M. G., van de Peppel, J., et al. (2006). Genome-wide location of the coactivator mediator: Binding without activation and transient Cdk8 interaction on DNA. Molecular Cell, 22, 179–192.

    CAS  PubMed  Google Scholar 

  • Aparicio, O. M., Billington, B. L., & Gottschling, D. E. (1991). Modifiers of position effect are shared between telomeric and silent mating-type loci in S. cerevisiae. Cell, 66, 1279–1287.

    CAS  PubMed  Google Scholar 

  • Barton, A. B., Su, Y., Lamb, J., Barber, D., & Kaback, D. B. (2003). A function for subtelomeric DNA in Saccharomyces cerevisiae. Genetics, 165, 929–934.

    CAS  PubMed  Google Scholar 

  • Barton, A. B., Pekosz, M. R., Kurvathi, R. S., & Kaback, D. B. (2008). Meiotic recombination at the ends of chromosomes in Saccharomyces cerevisiae. Genetics, 179, 1221–1235.

    CAS  PubMed  Google Scholar 

  • Bertuch, A. A., & Lundblad, V. (2003). The Ku heterodimer performs separable activities at double-strand breaks and chromosome termini. Molecular and Cellular Biology, 23, 8202–8215.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Biessmann, H., Mason, J. M., Ferry, K., d’Hulst, M., Valgeirsdottir, K., Traverse, K. L., et al. (1990). Addition of telomere-associated HeT DNA sequences “heals” broken chromosome ends in Drosophila. Cell, 61, 663–673.

    CAS  PubMed  Google Scholar 

  • Blitzblau, H. G., Bell, G. W., Rodriguez, J., Bell, S. P., & Hochwagen, A. (2007). Mapping of meiotic single-stranded DNA reveals double-stranded-break hotspots near centromeres and telomeres. Current Biology, 17, 2003–2012.

    CAS  PubMed  Google Scholar 

  • Boeke, J. D., Trueheart, J., Natsoulis, G., & Fink, G. R. (1987). 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods in Enzymology, 154, 164–175.

    CAS  PubMed  Google Scholar 

  • Borneman, A. R., Desany, B. A., Riches, D., Affourtit, J. P., Forgan, A. H., Pretorius, I. S., et al. (2011). Whole-genome comparison reveals novel genetic elements that characterize the genome of industrial strains of Saccharomyces cerevisiae. PLoS Genetics, 7, e1001287.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Boulton, S. J., & Jackson, S. P. (1998). Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO Journal, 17, 1819–1828.

    CAS  PubMed  Google Scholar 

  • Brown, C. A., Murray, A. W., & Verstrepen, K. J. (2010). Rapid expansion and functional divergence of subtelomeric gene families in yeasts. Current Biology, 20, 895–903.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Carlson, M., & Botstein, D. (1983). Organization of the SUC gene family in Saccharomyces. Molecular and Cellular Biology, 3, 351–359.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Carlson, M., Celenza, J. L., & Eng, F. J. (1985). Evolution of the dispersed SUC gene family of Saccharomyces by rearrangements of chromosome telomeres. Molecular and Cellular Biology, 5, 2894–2902.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chan, C. S., & Tye, B. K. (1983). A family of Saccharomyces cerevisiae repetitive autonomously replicating sequences that have very similar genomic environments. Journal of Molecular Biology, 168, 505–523.

    CAS  PubMed  Google Scholar 

  • Charron, M. J., Read, E., Haut, S. R., & Michels, C. A. (1989). Molecular evolution of the telomere-associated MAL loci of Saccharomyces. Genetics, 122, 307–316.

    CAS  PubMed  Google Scholar 

  • Chen, L., & Widom, J. (2005). Mechanism of transcriptional silencing in yeast. Cell, 120, 37–48.

    CAS  PubMed  Google Scholar 

  • Christiaens, J. F., Van Mulders, S. E., Duitama, J., Brown, C. A., Ghequire, M. G., De Meester, L., & Verstrepen, K. J. (2012). Functional divergence of gene duplicates through ectopic recombination.

    Google Scholar 

  • Cohn, M., Liti, G., & Barton, D. (2006). Telomeres in fungi. In P. Sunnerhagen, J. Piskur (Eds.), Comparative genomics using fungi as a model (pp. 101–130). Heidelberg: Springer.

    Google Scholar 

  • Des Marais, D. L., & Rausher, M. D. (2008). Escape from adaptive conflict after duplication in an anthocyanin pathway gene. Nature, 454, 762–765.

    CAS  PubMed  Google Scholar 

  • Eichler, E. E. (2001). Segmental duplications: What’s missing, misassigned, and misassembled–and should we care? Genome Research, 11, 653–656.

    CAS  PubMed  Google Scholar 

  • Eichler, E. E., Clark, R. A., & She, X. (2004). An assessment of the sequence gaps: Unfinished business in a finished human genome. Nature Reviews Genetics, 5, 345–354.

    CAS  PubMed  Google Scholar 

  • Flint, J., Bates, G. P., Clark, K., Dorman, A., Willingham, D., Roe, B. A., et al. (1997). Sequence comparison of human and yeast telomeres identifies structurally distinct subtelomeric domains. Human Molecular Genetics, 6, 1305–1313.

    CAS  PubMed  Google Scholar 

  • Francesconi, M., Jelier, R., & Lehner, B. (2011). Integrated genome-scale prediction of detrimental mutations in transcription networks. PLoS Genetics, 7, e1002077.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gatbonton, T., Imbesi, M., Nelson, M., Akey, J. M., Ruderfer, D. M., Kruglyak, L., et al. (2006). Telomere length as a quantitative trait: Genome-wide survey and genetic mapping of telomere length-control genes in yeast. PLoS Genetics, 2, e35.

    PubMed Central  PubMed  Google Scholar 

  • Gemayel, R., Vinces, M. D., Legendre, M., & Verstrepen, K. J. (2010). Variable tandem repeats accelerate evolution of coding and regulatory sequences. Annual Review of Genetics, 44, 445–477.

    CAS  PubMed  Google Scholar 

  • Gimeno, C. J., Ljungdahl, P. O., Styles, C. A., & Fink, G. R. (1992). Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: Regulation by starvation and RAS. Cell, 68, 1077–1090.

    CAS  PubMed  Google Scholar 

  • Goffeau, A., Barrell, B. G., Bussey, H., Davis, R. W., Dujon, B., Feldmann, H., et al. (1996). Life with 6000 genes. Science, 274(546), 547–563.

    Google Scholar 

  • Goldman, A. S., & Lichten, M. (1996). The efficiency of meiotic recombination between dispersed sequences in Saccharomyces cerevisiae depends upon their chromosomal location. Genetics, 144, 43–55.

    CAS  PubMed  Google Scholar 

  • Gottschling, D. E., Aparicio, O. M., Billington, B. L., & Zakian, V. A. (1990). Position effect at S. cerevisiae telomeres: Reversible repression of Pol II transcription. Cell, 63, 751–762.

    CAS  PubMed  Google Scholar 

  • Govender, P., Bester, M., & Bauer, F. F. (2010). FLO gene-dependent phenotypes in industrial wine yeast strains. Applied Microbiology and Biotechnology, 86, 931–945.

    CAS  PubMed  Google Scholar 

  • Gresham, D., Desai, M. M., Tucker, C. M., Jenq, H. T., Pai, D. A., Ward, A., et al. (2008). The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genetics, 4, e1000303.

    PubMed Central  PubMed  Google Scholar 

  • Guo, B., Styles, C. A., Feng, Q., & Fink, G. R. (2000). A Saccharomyces gene family involved in invasive growth, cell–cell adhesion, and mating. Proceedings of the National Academy of Sciences of the United States of America, 97, 12158–12163.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Halme, A., Bumgarner, S., Styles, C., & Fink, G. R. (2004). Genetic and epigenetic regulation of the FLO gene family generates cell-surface variation in yeast. Cell, 116, 405–415.

    CAS  PubMed  Google Scholar 

  • Hasin, Y., Olender, T., Khen, M., Gonzaga-Jauregui, C., Kim, P. M., Urban, A. E., et al. (2008). High-resolution copy-number variation map reflects human olfactory receptor diversity and evolution. PLoS Genetics, 4, e1000249.

    PubMed Central  PubMed  Google Scholar 

  • Hawk, J. D., Stefanovic, L., Boyer, J. C., Petes, T. D., & Farber, R. A. (2005). Variation in efficiency of DNA mismatch repair at different sites in the yeast genome. Proceedings of the National Academy of Sciences of the United States of America, 102, 8639–8643.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hediger, F., Neumann, F. R., Van Houwe, G., Dubrana, K., & Gasser, S. M. (2002). Live imaging of telomeres: yKu and Sir proteins define redundant telomere-anchoring pathways in yeast. Current Biology, 12, 2076–2089.

    CAS  PubMed  Google Scholar 

  • Horowitz, H., & Haber, J. E. (1985). Identification of autonomously replicating circular subtelomeric Y′ elements in Saccharomyces cerevisiae. Molecular and Cellular Biology, 5, 2369–2380.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hughes, T. R., Marton, M. J., Jones, A. R., Roberts, C. J., Stoughton, R., Armour, C. D., et al. (2000). Functional discovery via a compendium of expression profiles. Cell, 102, 109–126.

    CAS  PubMed  Google Scholar 

  • Ito-Harashima, S., Hartzog, P. E., Sinha, H., & McCusker, J. H. (2002). The tRNA-Tyr gene family of Saccharomyces cerevisiae: Agents of phenotypic variation and position effects on mutation frequency. Genetics, 161, 1395–1410.

    CAS  PubMed  Google Scholar 

  • Jablonka, E., Oborny, B., Molnar, I., Kisdi, E., Hofbauer, J., & Czaran, T. (1995). The adaptive advantage of phenotypic memory in changing environments. Philosophical Transactions of the Royal Society of London. Series B, Biological sciences, 350, 133–141.

    CAS  PubMed  Google Scholar 

  • Jeppesen, P. (1997). Histone acetylation: A possible mechanism for the inheritance of cell memory at mitosis. BioEssays, 19, 67–74.

    CAS  PubMed  Google Scholar 

  • Kellis, M., Birren, B. W., & Lander, E. S. (2004). Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature, 428, 617–624.

    CAS  PubMed  Google Scholar 

  • Kellis, M., Patterson, N., Endrizzi, M., Birren, B., & Lander, E. S. (2003). Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature, 423, 241–254.

    CAS  PubMed  Google Scholar 

  • Kim, J. M., Vanguri, S., Boeke, J. D., Gabriel, A., & Voytas, D. F. (1998). Transposable elements and genome organization: A comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Research, 8, 464–478.

    CAS  PubMed  Google Scholar 

  • Kimura, A., Umehara, T., & Horikoshi, M. (2002). Chromosomal gradient of histone acetylation established by Sas2p and Sir2p functions as a shield against gene silencing. Nature Genetics, 32, 370–377.

    PubMed  Google Scholar 

  • Kobayashi, O., Yoshimoto, H., & Sone, H. (1999). Analysis of the genes activated by the FLO8 gene in Saccharomyces cerevisiae. Current Genetics, 36, 256–261.

    CAS  PubMed  Google Scholar 

  • Kussell, E., & Leibler, S. (2005). Phenotypic diversity, population growth, and information in fluctuating environments. Science, 309, 2075–2078.

    CAS  PubMed  Google Scholar 

  • Kyrion, G., Boakye, K. A., & Lustig, A. J. (1992). C-terminal truncation of RAP1 results in the deregulation of telomere size, stability, and function in Saccharomyces cerevisiae. Molecular and Cellular Biology, 12, 5159–5173.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kyrion, G., Liu, K., Liu, C., & Lustig, A. J. (1993). RAP1 and telomere structure regulate telomere position effects in Saccharomyces cerevisiae. Genes and Development, 7, 1146–1159.

    CAS  PubMed  Google Scholar 

  • Lambrechts, M. G., Bauer, F. F., Marmur, J., & Pretorius, I. S. (1996). Muc1, a mucin-like protein that is regulated by Mss10, is critical for pseudohyphal differentiation in yeast. Proceedings of the National Academy of Sciences of the United States of America, 93, 8419–8424.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lang, G. I., & Murray, A. W. (2011). Mutation rates across budding yeast chromosome VI are correlated with replication timing. Genome Biology and Evolution, 3, 799–811.

    PubMed Central  PubMed  Google Scholar 

  • Laroche, T., Martin, S. G., Gotta, M., Gorham, H. C., Pryde, F. E., Louis, E. J., et al. (1998). Mutation of yeast Ku genes disrupts the subnuclear organization of telomeres. Current Biology, 8, 653–656.

    CAS  PubMed  Google Scholar 

  • Levis, R. W., Ganesan, R., Houtchens, K., Tolar, L. A., & Sheen, F. M. (1993). Transposons in place of telomeric repeats at a Drosophila telomere. Cell, 75, 1083–1093.

    CAS  PubMed  Google Scholar 

  • Linardopoulou, E. V., Williams, E. M., Fan, Y., Friedman, C., Young, J. M., & Trask, B. J. (2005). Human subtelomeres are hot spots of interchromosomal recombination and segmental duplication. Nature, 437, 94–100.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liti, G., & Louis, E. J. (2005). Yeast evolution and comparative genomics. Annual Review of Microbiology, 59, 135–153.

    CAS  PubMed  Google Scholar 

  • Liti, G., Carter, D. M., Moses, A. M., Warringer, J., Parts, L., James, S. A., et al. (2009). Population genomics of domestic and wild yeasts. Nature, 458, 337–341.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu, H., Styles, C. A., & Fink, G. R. (1996). Saccharomyces cerevisiae S288C has a mutation in FLO8, a gene required for filamentous growth. Genetics, 144, 967–978.

    CAS  PubMed  Google Scholar 

  • Lo, W. S., & Dranginis, A. M. (1996). FLO11, a yeast gene related to the STA genes, encodes a novel cell surface flocculin. Journal of Bacteriology, 178, 7144–7151.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lo, W. S., & Dranginis, A. M. (1998). The cell surface flocculin Flo11 is required for pseudohyphae formation and invasion by Saccharomyces cerevisiae. Molecular Biology of the Cell, 9, 161–171.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Louis, E. J., & Haber, J. E. (1990a). Mitotic recombination among subtelomeric Y′ repeats in Saccharomyces cerevisiae. Genetics, 124, 547–559.

    CAS  PubMed  Google Scholar 

  • Louis, E. J., & Haber, J. E. (1990b). The subtelomeric Y′ repeat family in Saccharomyces cerevisiae: An experimental system for repeated sequence evolution. Genetics, 124, 533–545.

    CAS  PubMed  Google Scholar 

  • Louis, E. J., & Haber, J. E. (1992). The structure and evolution of subtelomeric Y′ repeats in Saccharomyces cerevisiae. Genetics, 131, 559–574.

    CAS  PubMed  Google Scholar 

  • Louis, E. J., Naumova, E. S., Lee, A., Naumov, G., & Haber, J. E. (1994). The chromosome end in yeast: Its mosaic nature and influence on recombinational dynamics. Genetics, 136, 789–802.

    CAS  PubMed  Google Scholar 

  • Lundblad, V., & Szostak, J. W. (1989). A mutant with a defect in telomere elongation leads to senescence in yeast. Cell, 57, 633–643.

    CAS  PubMed  Google Scholar 

  • Luo, Z., & van Vuuren, H. J. (2009). Functional analyses of PAU genes in Saccharomyces cerevisiae. Microbiology, 155, 4036–4049.

    CAS  PubMed  Google Scholar 

  • Mak, H. C., Pillus, L., & Ideker, T. (2009). Dynamic reprogramming of transcription factors to and from the subtelomere. Genome Research, 19, 1014–1025.

    CAS  PubMed  Google Scholar 

  • Marks, V. D., Ho Sui, S. J., Erasmus, D., van der Merwe, G. K., Brumm, J., Wasserman, W. W., et al. (2008). Dynamics of the yeast transcriptome during wine fermentation reveals a novel fermentation stress response. FEMS Yeast Research, 8, 35–52.

    CAS  PubMed  Google Scholar 

  • Marvin, M. E., Becker, M. M., Noel, P., Hardy, S., Bertuch, A. A., & Louis, E. J. (2009a). The association of yKu with subtelomeric core X sequences prevents recombination involving telomeric sequences. Genetics, 183, 453–467 (451SI–413SI).

    Google Scholar 

  • Marvin, M. E., Griffin, C. D., Eyre, D. E., Barton, D. B., & Louis, E. J. (2009b). In Saccharomyces cerevisiae, yKu and subtelomeric core X sequences repress homologous recombination near telomeres as part of the same pathway. Genetics, 183, 441–451 (441SI–412SI).

    Google Scholar 

  • Mefford, H. C., & Trask, B. J. (2002). The complex structure and dynamic evolution of human subtelomeres. Nature Reviews Genetics, 3, 91–102.

    CAS  PubMed  Google Scholar 

  • Moretti, P., Freeman, K., Coodly, L., & Shore, D. (1994). Evidence that a complex of SIR proteins interacts with the silencer and telomere-binding protein RAP1. Genes and Development, 8, 2257–2269.

    CAS  PubMed  Google Scholar 

  • Naumov, G. I., Naumova, E. S., & Korhola, M. P. (1995). Chromosomal polymorphism of MEL genes in some populations of Saccharomyces cerevisiae. FEMS Microbiology Letters, 127, 41–45.

    CAS  PubMed  Google Scholar 

  • Naumov, G. I., Naumova, E. S., Turakainen, H., & Korhola, M. (1996). Identification of the alpha-galactosidase MEL genes in some populations of Saccharomyces cerevisiae: A new gene MEL11. Genetical Research, 67, 101–108.

    CAS  PubMed  Google Scholar 

  • Ness, F., & Aigle, M. (1995). RTM1: A member of a new family of telomeric repeated genes in yeast. Genetics, 140, 945–956.

    CAS  PubMed  Google Scholar 

  • Octavio, L. M., Gedeon, K., & Maheshri, N. (2009). Epigenetic and conventional regulation is distributed among activators of FLO11 allowing tuning of population-level heterogeneity in its expression. PLoS Genetics, 5, e1000673.

    PubMed Central  PubMed  Google Scholar 

  • Ogata, T., Izumikawa, M., Kohno, K., & Shibata, K. (2008). Chromosomal location of Lg-FLO1 in bottom-fermenting yeast and the FLO5 locus of industrial yeast. Journal of Applied Microbiology, 105, 1186–1198.

    CAS  PubMed  Google Scholar 

  • Ohno, S. (1970). Evolution by gene duplication. Berlin: Springer.

    Google Scholar 

  • Ottaviani, A., Gilson, E., & Magdinier, F. (2008). Telomeric position effect: From the yeast paradigm to human pathologies? Biochimie, 90, 93–107.

    CAS  PubMed  Google Scholar 

  • Palkova, Z., & Vachova, L. (2006). Life within a community: Benefit to yeast long-term survival. FEMS Microbiology Reviews, 30, 806–824.

    CAS  PubMed  Google Scholar 

  • Pryde, F. E., Huckle, T. C., & Louis, E. J. (1995). Sequence analysis of the right end of chromosome XV in Saccharomyces cerevisiae: An insight into the structural and functional significance of sub-telomeric repeat sequences. Yeast, 11, 371–382.

    CAS  PubMed  Google Scholar 

  • Pryde, F. E., Gorham, H. C., & Louis, E. J. (1997). Chromosome ends: All the same under their caps. Current Opinion in Genetics and Development, 7, 822–828.

    CAS  PubMed  Google Scholar 

  • Pryde, F. E., & Louis, E. J. (1997). Saccharomyces cerevisiae telomeres. A review. Biochemistry (Mosc), 62, 1232–1241.

    CAS  Google Scholar 

  • Pryde, F. E., & Louis, E. J. (1999). Limitations of silencing at native yeast telomeres. EMBO Journal, 18, 2538–2550.

    CAS  PubMed  Google Scholar 

  • Rando, O. J., & Verstrepen, K. J. (2007). Timescales of genetic and epigenetic inheritance. Cell, 128, 655–668.

    CAS  PubMed  Google Scholar 

  • Roberts, D. J., Craig, A. G., Berendt, A. R., Pinches, R., Nash, G., Marsh, K., et al. (1992). Rapid switching to multiple antigenic and adhesive phenotypes in malaria. Nature, 357, 689–692.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Robyr, D., Suka, Y., Xenarios, I., Kurdistani, S. K., Wang, A., Suka, N., et al. (2002). Microarray deacetylation maps determine genome-wide functions for yeast histone deacetylases. Cell, 109, 437–446.

    CAS  PubMed  Google Scholar 

  • Ross, L. O., Maxfield, R., & Dawson, D. (1996). Exchanges are not equally able to enhance meiotic chromosome segregation in yeast. Proceedings of the National Academy of Sciences of the United States of America, 93, 4979–4983.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rossignol, T., Dulau, L., Julien, A., & Blondin, B. (2003). Genome-wide monitoring of wine yeast gene expression during alcoholic fermentation. Yeast, 20, 1369–1385.

    CAS  PubMed  Google Scholar 

  • Rudd, M. K., Friedman, C., Parghi, S. S., Linardopoulou, E. V., Hsu, L., & Trask, B. J. (2007). Elevated rates of sister chromatid exchange at chromosome ends. PLoS Genetics, 3, e32.

    PubMed Central  PubMed  Google Scholar 

  • Rusche, L. N., Kirchmaier, A. L., & Rine, J. (2003). The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae. Annual Review of Biochemistry, 72, 481–516.

    CAS  PubMed  Google Scholar 

  • Schacherer, J., Shapiro, J. A., Ruderfer, D. M., & Kruglyak, L. (2009). Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature, 458, 342–345.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sekinger, E. A., & Gross, D. S. (2001). Silenced chromatin is permissive to activator binding and PIC recruitment. Cell, 105, 403–414.

    CAS  PubMed  Google Scholar 

  • Shampay, J., Szostak, J. W., & Blackburn, E. H. (1984). DNA sequences of telomeres maintained in yeast. Nature, 310, 154–157.

    CAS  PubMed  Google Scholar 

  • Sherman, J. M., & Pillus, L. (1997). An uncertain silence. Trends Genet, 13, 308–313.

    CAS  PubMed  Google Scholar 

  • Shore, D., & Nasmyth, K. (1987). Purification and cloning of a DNA binding protein from yeast that binds to both silencer and activator elements. Cell, 51, 721–732.

    CAS  PubMed  Google Scholar 

  • Smith, J. J., Miller, L. R., Kreisberg, R., Vazquez, L., Wan, Y., & Aitchison, J. D. (2011). Environment-responsive transcription factors bind subtelomeric elements and regulate gene silencing. Molecular Systems Biology, 7, 455.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Smukalla, S., Caldara, M., Pochet, N., Beauvais, A., Guadagnini, S., Yan, C., et al. (2008). FLO1 is a variable green beard gene that drives biofilm-like cooperation in budding yeast. Cell, 135, 726–737.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Strahl-Bolsinger, S., Hecht, A., Luo, K., & Grunstein, M. (1997). SIR2 and SIR4 interactions differ in core and extended telomeric heterochromatin in yeast. Genes and Development, 11, 83–93.

    CAS  PubMed  Google Scholar 

  • Su, Y., Barton, A. B., & Kaback, D. B. (2000). Decreased meiotic reciprocal recombination in subtelomeric regions in Saccharomyces cerevisiae. Chromosoma, 109, 467–475.

    CAS  PubMed  Google Scholar 

  • Suka, N., Luo, K., & Grunstein, M. (2002). Sir2p and Sas2p opposingly regulate acetylation of yeast histone H4 lysine16 and spreading of heterochromatin. Nature Genetics, 32, 378–383.

    CAS  PubMed  Google Scholar 

  • Svejstrup, J. Q. (2002). Mechanisms of transcription-coupled DNA repair. Nature Reviews Molecular Cell Biology, 3, 21–29.

    CAS  PubMed  Google Scholar 

  • Taddei, A., Hediger, F., Neumann, F. R., Bauer, C., & Gasser, S. M. (2004). Separation of silencing from perinuclear anchoring functions in yeast Ku80, Sir4 and Esc1 proteins. EMBO Journal, 23, 1301–1312.

    CAS  PubMed  Google Scholar 

  • Taddei, A., Van Houwe, G., Nagai, S., Erb, I., van Nimwegen, E., & Gasser, S. M. (2009). The functional importance of telomere clustering: Global changes in gene expression result from SIR factor dispersion. Genome Research, 19, 611–625.

    CAS  PubMed  Google Scholar 

  • Teste, M. A., Francois, J. M., & Parrou, J. L. (2010). Characterization of a new multigene family encoding isomaltases in the yeast Saccharomyces cerevisiae, the IMA family. Journal of Biological Chemistry, 285, 26815–26824.

    CAS  PubMed  Google Scholar 

  • Teytelman, L., Eisen, M. B., & Rine, J. (2008). Silent but not static: Accelerated base-pair substitution in silenced chromatin of budding yeasts. PLoS Genetics, 4, e1000247.

    PubMed Central  PubMed  Google Scholar 

  • Tirosh, I., Barkai, N., & Verstrepen, K. J. (2009). Promoter architecture and the evolvability of gene expression. J Biol, 8, 95.

    PubMed Central  PubMed  Google Scholar 

  • Trask, B. J., Friedman, C., Martin-Gallardo, A., Rowen, L., Akinbami, C., Blankenship, J., et al. (1998). Members of the olfactory receptor gene family are contained in large blocks of DNA duplicated polymorphically near the ends of human chromosomes. Human Molecular Genetics, 7, 13–26.

    CAS  PubMed  Google Scholar 

  • Trelles-Sticken, E., Loidl, J., & Scherthan, H. (1999). Bouquet formation in budding yeast: Initiation of recombination is not required for meiotic telomere clustering. Journal of Cell Science, 112(Pt 5), 651–658.

    CAS  PubMed  Google Scholar 

  • Tsukamoto, Y., Kato, J., & Ikeda, H. (1997). Silencing factors participate in DNA repair and recombination in Saccharomyces cerevisiae. Nature, 388, 900–903.

    CAS  PubMed  Google Scholar 

  • Van Mulders, S. E., Ghequire, M., Daenen, L., Verbelen, P. J., Verstrepen, K. J., & Delvaux, F. R. (2010). Flocculation gene variability in industrial brewer’s yeast strains. Applied Microbiology and Biotechnology, 88, 1321–1331.

    PubMed  Google Scholar 

  • Verstrepen, K. J., & Fink, G. R. (2009). Genetic and epigenetic mechanisms underlying cell-surface variability in protozoa and fungi. Annual Review of Genetics, 43, 1–24.

    CAS  PubMed  Google Scholar 

  • Verstrepen, K. J., Jansen, A., Lewitter, F., & Fink, G. R. (2005). Intragenic tandem repeats generate functional variability. Nature Genetics, 37, 986–990.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Verstrepen, K. J., & Klis, F. M. (2006). Flocculation, adhesion and biofilm formation in yeasts. Molecular Microbiology, 60, 5–15.

    CAS  PubMed  Google Scholar 

  • Verstrepen, K. J., Reynolds, T. B., & Fink, G. R. (2004). Origins of variation in the fungal cell surface. Nature Reviews Microbiology, 2, 533–540.

    CAS  PubMed  Google Scholar 

  • Vinces, M. D., Legendre, M., Caldara, M., Hagihara, M., & Verstrepen, K. J. (2009). Unstable tandem repeats in promoters confer transcriptional evolvability. Science, 324, 1213–1216.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Voordeckers, K., Brown, C. A., Vanneste, K., van der Zande, E., Voet, A., Maere, S., & Verstrepen, K. J. (2012). Reconstruction of Ancestral Metabolic Enzymes Reveals Molecular Mechanisms Underlying Evolutionary Innovation through Gene Duplication. PLoS biology, 10(12), e1001446.

    Google Scholar 

  • Voytas, D. F., & Boeke, J. D. (1992). Yeast retrotransposon revealed. Nature, 358, 717.

    CAS  PubMed  Google Scholar 

  • Walmsley, R. M., & Petes, T. D. (1985). Genetic control of chromosome length in yeast. Proceedings of the National Academy of Sciences United States of America, 82, 506–510.

    CAS  Google Scholar 

  • Wapinski, I., Pfeffer, A., Friedman, N., & Regev, A. (2007). Natural history and evolutionary principles of gene duplication in fungi. Nature, 449, 54–61.

    CAS  PubMed  Google Scholar 

  • Wolf, D. M., Vazirani, V. V., & Arkin, A. P. (2005). Diversity in times of adversity: Probabilistic strategies in microbial survival games. Journal of Theoretical Biology, 234, 227–253.

    PubMed  Google Scholar 

  • Wolfe, K. H., & Shields, D. C. (1997). Molecular evidence for an ancient duplication of the entire yeast genome. Nature, 387, 708–713.

    CAS  PubMed  Google Scholar 

  • Wotton, D., & Shore, D. (1997). A novel Rap1p-interacting factor, Rif2p, cooperates with Rif1p to regulate telomere length in Saccharomyces cerevisiae. Genes and Development, 11, 748–760.

    CAS  PubMed  Google Scholar 

  • Wyrick, J. J., Holstege, F. C., Jennings, E. G., Causton, H. C., Shore, D., Grunstein, M., et al. (1999). Chromosomal landscape of nucleosome-dependent gene expression and silencing in yeast. Nature, 402, 418–421.

    CAS  PubMed  Google Scholar 

  • Yamada, M., Hayatsu, N., Matsuura, A., & Ishikawa, F. (1998). Y′-Help1, a DNA helicase encoded by the yeast subtelomeric Y′ element, is induced in survivors defective for telomerase. Journal of Biological Chemistry, 273, 33360–33366.

    CAS  PubMed  Google Scholar 

  • Yamashita, I., Maemura, T., Hatano, T., & Fukui, S. (1985). Polymorphic extracellular glucoamylase genes and their evolutionary origin in the yeast Saccharomyces diastaticus. Journal of Bacteriology, 161, 574–582.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zakian, V. A. (1996). Structure, function, and replication of Saccharomyces cerevisiae telomeres. Annual Review of Genetics, 30, 141–172.

    CAS  PubMed  Google Scholar 

  • Zhou, B. O., Wang, S. S., Zhang, Y., Fu, X. H., Dang, W., Lenzmeier, B. A., et al. (2011). Histone H4 lysine 12 acetylation regulates telomeric heterochromatin plasticity in Saccharomyces cerevisiae. PLoS Genetics, 7, e1001272.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu, X., & Gustafsson, C. M. (2009). Distinct differences in chromatin structure at subtelomeric X and Y′ elements in budding yeast. PLoS ONE, 4, e6363.

    PubMed Central  PubMed  Google Scholar 

  • Zhu, Y., Dai, J., Fuerst, P. G., & Voytas, D. F. (2003). Controlling integration specificity of a yeast retrotransposon. Proceedings of the National Academy of Sciences of the United States of America, 100, 5891–5895.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zou, S., Wright, D. A., & Voytas, D. F. (1995). The Saccharomyces Ty5 retrotransposon family is associated with origins of DNA replication at the telomeres and the silent mating locus HMR. Proceedings of the National Academy of Sciences of the United States of America, 92, 920–924.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zou, S., Ke, N., Kim, J. M., & Voytas, D. F. (1996a). The Saccharomyces retrotransposon Ty5 integrates preferentially into regions of silent chromatin at the telomeres and mating loci. Genes and Development, 10, 634–645.

    CAS  PubMed  Google Scholar 

  • Zou, S., Kim, J. M., & Voytas, D. F. (1996b). The Saccharomyces retrotransposon Ty5 influences the organization of chromosome ends. Nucleic Acids Research, 24, 4825–4831.

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Joaquin Christiaens for useful suggestions to improve this manuscript. We are grateful to Narendra Maheshri for providing the microscopy pictures used in Fig. 3.5. All Verstrepen Laboratory members are thanked for useful discussions. We apologize for the omission of several relevant studies we could not cite due to space limitations. Research in the laboratory of KJV is supported by NIH Grant P50GM068763, HumanFrontier Science ProgramHFSPRGY79/2007, ERC Young Investigator Grant 241426, VIB, KU Leuven, the FWO-Odysseus program, and the AB InBev Baillet-Latour. KV is a postdoctoral fellow of the Fonds voor Wetenschappelijk Onderzoek (FWO) Vlaanderen.

Author information

Authors and Affiliations

  1. VIB Laboratory for Systems Biology, Gaston Geenslaan 1, 3001, Leuven, Belgium

    Tim Snoek, Karin Voordeckers & Kevin J. Verstrepen

  2. CMPG Laboratory for Genetics and Genomics, Katholieke Universiteit Leuven, Gaston Geenslaan 1, 3001, Leuven, Belgium

    Tim Snoek, Karin Voordeckers & Kevin J. Verstrepen

Authors
  1. Tim Snoek
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karin Voordeckers
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kevin J. Verstrepen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kevin J. Verstrepen .

Editor information

Editors and Affiliations

  1. Department of Genetics, University of Leicester, Leicester, United Kingdom

    Edward J Louis

  2. Department of Genetics, University of Leicester, Leicester, United Kingdom

    Marion M Becker

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Snoek, T., Voordeckers, K., Verstrepen, K.J. (2014). Subtelomeric Regions Promote Evolutionary Innovation of Gene Families in Yeast. In: Louis, E., Becker, M. (eds) Subtelomeres. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-41566-1_3

Download citation

Publish with us

Policies and ethics

Search

Navigation