The Chromosome End in Yeast: Its Mosaic Nature and Influence on Recombinational Dynamics

INVESTIGATIONS

The Chromosome End in Yeast: Its Mosaic Nature and Influence on Recombinational Dynamics

E. J. Louis, E. S. Naumova, A. Lee, G. Naumov and J. E. Haber
Yeast Genetics, Institute of Molecular Medicine, John Radcliffe Hospital, Oxford OX3 9DU, England

Yeast chromosome ends are composed of several different repeated elements. Among six clones of chromosome ends from two strains of Saccharomyces cerevisiae, at least seven different repeated sequence families were found. These included the previously identified Y' and X elements. Some families are highly variable in copy number and location between strains of S. cerevisiae, while other elements appear constant in copy number and location. Three repeated sequence elements are specific to S. cerevisiae and are not found in its evolutionarily close relative, Saccharomyces paradoxus. Two other repeated sequences are found in both S. cerevisiae and S. paradoxus. None of those described here is found (by low stringency DNA hybridization) in the next closest species, Saccharomyces bayanus. The loosely characterized X element is now more precisely defined. X is a composite of at least four small (ca. 45-140 bp) sequences found at some, but not all, ends. There is also a potential ``core'' X element of approximately 560 bp which may be found at all ends. Distal to X, only one of six clones had (TG(1-3))(n) telomere sequence at the junction between X and Y'. The presence of these internal (TG(1-3))(n) sequences correlates with the ability of a single Y' to expand into a tandem array of Y's by unequal sister chromatid exchange. The presence of shared repeated elements proximal to the X region can override the strong preference of Y's to recombine ectopically with other Y's of the same size class. The chromosome ends in yeast are evolutionarily dynamic in terms of subtelomeric repeat structure and variability.

This article has been cited by other articles:

M. E. Marvin, C. D. Griffin, D. E. Eyre, D. B. H. Barton, and E. J. Louis
In Saccharomyces cerevisiae, yKu and Subtelomeric Core X Sequences Repress Homologous Recombination Near Telomeres as Part of the Same Pathway
Genetics, October 1, 2009; 183(2): 441 - 451.
[Abstract] [Full Text] [PDF]

G.-F. Richard, A. Kerrest, and B. Dujon
Comparative Genomics and Molecular Dynamics of DNA Repeats in Eukaryotes
Microbiol. Mol. Biol. Rev., December 1, 2008; 72(4): 686 - 727.
[Abstract] [Full Text] [PDF]

H. Schober, V. Kalck, M. A. Vega-Palas, G. Van Houwe, D. Sage, M. Unser, M. R. Gartenberg, and S. M. Gasser
Controlled exchange of chromosomal arms reveals principles driving telomere interactions in yeast
Genome Res., February 1, 2008; 18(2): 261 - 271.
[Abstract] [Full Text] [PDF]

C. Rehmeyer, W. Li, M. Kusaba, Y.-S. Kim, D. Brown, C. Staben, R. Dean, and M. Farman
Organization of chromosome ends in the rice blast fungus, Magnaporthe oryzae
Nucleic Acids Res., October 18, 2006; 34(17): 4685 - 4701.
[Abstract] [Full Text] [PDF]

G.-F. Richard and B. Dujon
Molecular Evolution of Minisatellites in Hemiascomycetous Yeasts
Mol. Biol. Evol., January 1, 2006; 23(1): 189 - 202.
[Abstract] [Full Text] [PDF]

E. Trelles-Sticken, S. Bonfils, J. Sollier, V. Geli, H. Scherthan, and C. de La Roche Saint-Andre
Set1- and Clb5-deficiencies disclose the differential regulation of centromere and telomere dynamics in Saccharomyces cerevisiae meiosis
J. Cell Sci., November 1, 2005; 118(21): 4985 - 4994.
[Abstract] [Full Text] [PDF]

H. B. Schlecht, M. Lichten, and A. S. H. Goldman
Compartmentalization of the Yeast Meiotic Nucleus Revealed by Analysis of Ectopic Recombination
Genetics, November 1, 2004; 168(3): 1189 - 1203.
[Abstract] [Full Text] [PDF]

M. K. Zubko, S. Guillard, and D. Lydall
Exo1 and Rad24 Differentially Regulate Generation of ssDNA at Telomeres of Saccharomyces cerevisiae cdc13-1 Mutants
Genetics, September 1, 2004; 168(1): 103 - 115.
[Abstract] [Full Text] [PDF]

D. Lydall
Hiding at the ends of yeast chromosomes: telomeres, nucleases and checkpoint pathways
J. Cell Sci., October 15, 2003; 116(20): 4057 - 4065.
[Abstract] [Full Text] [PDF]

J. E. Lowell, A. I. Roughton, V. Lundblad, and L. Pillus
Telomerase-Independent Proliferation Is Influenced by Cell Type in Saccharomyces cerevisiae
Genetics, July 1, 2003; 164(3): 909 - 921.
[Abstract] [Full Text] [PDF]

D. Carro, E. Bartra, and B. Pina
Karyotype Rearrangements in a Wine Yeast Strain by rad52-Dependent and rad52-Independent Mechanisms
Appl. Envir. Microbiol., April 1, 2003; 69(4): 2161 - 2165.
[Abstract] [Full Text] [PDF]

W. Gao, C. H. Khang, S.-Y. Park, Y.-H. Lee, and S. Kang
Evolution and Organization of a Highly Dynamic, Subtelomeric Helicase Gene Family in the Rice Blast Fungus Magnaporthe grisea
Genetics, September 1, 2002; 162(1): 103 - 112.
[Abstract] [Full Text] [PDF]

Y. Huang
Transcriptional silencing in Saccharomyces cerevisiae and Schizosaccharomyces pombe
Nucleic Acids Res., April 1, 2002; 30(7): 1465 - 1482.
[Abstract] [Full Text] [PDF]

A. Poloumienko, A. Dershowitz, J. De, and C. S. Newlon
Completion of Replication Map of Saccharomyces cerevisiae Chromosome III
Mol. Biol. Cell, November 1, 2001; 12(11): 3317 - 3327.
[Abstract] [Full Text] [PDF]

E. Lebrun, E. Revardel, C. Boscheron, R. Li, E. Gilson, and G. Fourel
Protosilencers in Saccharomyces cerevisiae Subtelomeric Regions
Genetics, May 1, 2001; 158(1): 167 - 176.
[Abstract] [Full Text]

P. Heun, T. Laroche, M.K. Raghuraman, and S. M. Gasser
The Positioning and Dynamics of Origins of Replication in the Budding Yeast Nucleus
J. Cell Biol., January 22, 2001; 152(2): 385 - 400.
[Abstract] [Full Text] [PDF]

H. Chibana, J. L. Beckerman, and P.T. Magee
Fine-Resolution Physical Mapping of Genomic Diversity in Candida albicans
Genome Res., December 1, 2000; 10(12): 1865 - 1877.
[Abstract] [Full Text]

E. Trelles-Sticken, M. E. Dresser, and H. Scherthan
Meiotic Telomere Protein Ndj1p Is Required for Meiosis-Specific Telomere Distribution, Bouquet Formation and Efficient Homologue Pairing
J. Cell Biol., October 2, 2000; 151(1): 95 - 106.
[Abstract] [Full Text] [PDF]

S.-C. Teng and V. A. Zakian
Telomere-Telomere Recombination Is an Efficient Bypass Pathway for Telomere Maintenance in Saccharomyces cerevisiae
Mol. Cell. Biol., December 1, 1999; 19(12): 8083 - 8093.
[Abstract] [Full Text] [PDF]

L. M. Larraya, G. Pérez, M. M. Peñas, J. J. P. Baars, T. S. P. Mikosch, A. G. Pisabarro, and L. Ramírez
Molecular Karyotype of the White Rot Fungus Pleurotus ostreatus
Appl. Envir. Microbiol., August 1, 1999; 65(8): 3413 - 3417.
[Abstract] [Full Text]

R. J. Craven and T. D. Petes
Dependence of the Regulation of Telomere Length on the Type of Subtelomeric Repeat in the Yeast Saccharomyces cerevisiae
Genetics, August 1, 1999; 152(4): 1531 - 1541.
[Abstract] [Full Text]

S. Venditti, M. A. Vega-Palas, and E. Di Mauro
Heterochromatin Organization of a Natural Yeast Telomere. RECRUITMENT OF Sir3p THROUGH INTERACTION WITH HISTONE H4 N TERMINUS IS REQUIRED FOR THE ESTABLISHMENT OF REPRESSIVE STRUCTURES
J. Biol. Chem., January 22, 1999; 274(4): 1928 - 1933.
[Abstract] [Full Text] [PDF]

E Trelles-Sticken, J Loidl, and H Scherthan
Bouquet formation in budding yeast: initiation of recombination is not required for meiotic telomere clustering
J. Cell Sci., January 3, 1999; 112(5): 651 - 658.
[Abstract] [PDF]

M. Yamada, N. Hayatsu, A. Matsuura, and F. Ishikawa
Y'-Help1, a DNA Helicase Encoded by the Yeast Subtelomeric Y' Element, Is Induced in Survivors Defective for Telomerase
J. Biol. Chem., December 11, 1998; 273(50): 33360 - 33366.
[Abstract] [Full Text] [PDF]

J. B. Stavenhagen and V. A. Zakian
Yeast telomeres exert a position effect on recombination between internal tracts of yeast telomeric DNA
Genes & Dev., October 1, 1998; 12(19): 3044 - 3058.
[Abstract] [Full Text]

B. D. Bourns, M. K. Alexander, A. M. Smith, and V. A. Zakian
Sir Proteins, Rif Proteins, and Cdc13p Bind Saccharomyces Telomeres In Vivo
Mol. Cell. Biol., September 1, 1998; 18(9): 5600 - 5608.
[Abstract] [Full Text]

H. Chibana, B. B. Magee, S. Grindle, Y. Ran, S. Scherer, and P. T. Magee
A Physical Map of Chromosome 7 of Candida albicans
Genetics, August 1, 1998; 149(4): 1739 - 1752.
[Abstract] [Full Text] [PDF]

R. J. Britten
Precise sequence complementarity between yeast chromosome ends and two classes of just-subtelomeric sequences
PNAS, May 26, 1998; 95(11): 5906 - 5912.
[Abstract] [Full Text] [PDF]

M. A. Vega-Palas, S. Venditti, and E. Di Mauro
Heterochromatin Organization of a Natural Yeast Telomere. CHANGES OF NUCLEOSOME DISTRIBUTION DRIVEN BY THE ABSENCE OF Sir3p
J. Biol. Chem., April 17, 1998; 273(16): 9388 - 9392.
[Abstract] [Full Text] [PDF]

Q.-w. Jin, E. Trelles-Sticken, H. Scherthan, and J. Loidl
Yeast Nuclei Display Prominent Centromere Clustering That Is Reduced in Nondividing Cells and in Meiotic Prophase
J. Cell Biol., April 6, 1998; 141(1): 21 - 29.
[Abstract] [Full Text] [PDF]

P. Sanchez-Alonso and P. Guzman
Organization of Chromosome Ends in Ustilago maydis. RecQ-like Helicase Motifs at Telomeric Regions
Genetics, March 1, 1998; 148(3): 1043 - 1054.
[Abstract] [Full Text] [PDF]

S. Bassham, A. Beam, and J. Shampay
Telomere Variation in Xenopus laevis
Mol. Cell. Biol., January 1, 1998; 18(1): 269 - 275.
[Abstract] [Full Text]

F. Baudat and A. Nicolas
Clustering of meiotic double-strand breaks on yeast chromosome III
PNAS, May 13, 1997; 94(10): 5213 - 5218.
[Abstract] [Full Text] [PDF]

L Maillet, C Boscheron, M Gotta, S Marcand, E Gilson, and S M Gasser
Evidence for silencing compartments within the yeast nucleus: a role for telomere proximity and Sir protein concentration in silencer-mediated repression.
Genes & Dev., July 15, 1996; 10(14): 1796 - 1811.
[Abstract] [PDF]

S Marcand, S W Buck, P Moretti, E Gilson, and D Shore
Silencing of genes at nontelomeric sites in yeast is controlled by sequestration of silencing factors at telomeres by Rap 1 protein.
Genes & Dev., June 1, 1996; 10(11): 1297 - 1309.
[Abstract] [PDF]

S Zou, N Ke, J M Kim, and D F Voytas
The Saccharomyces retrotransposon Ty5 integrates preferentially into regions of silent chromatin at the telomeres and mating loci.
Genes & Dev., March 1, 1996; 10(5): 634 - 645.
[Abstract] [PDF]

V. A. Zakian
Telomeres: Beginning to Understand the End
Science, December 8, 1995; 270(5242): 1601 - 1607.
[Abstract] [PDF]

				G.-F. Richard, A. Kerrest, and B. Dujon Comparative Genomics and Molecular Dynamics of DNA Repeats in Eukaryotes Microbiol. Mol. Biol. Rev., December 1, 2008; 72(4): 686 - 727. [Abstract] [Full Text] [PDF]

				H. Schober, V. Kalck, M. A. Vega-Palas, G. Van Houwe, D. Sage, M. Unser, M. R. Gartenberg, and S. M. Gasser Controlled exchange of chromosomal arms reveals principles driving telomere interactions in yeast Genome Res., February 1, 2008; 18(2): 261 - 271. [Abstract] [Full Text] [PDF]

				C. Rehmeyer, W. Li, M. Kusaba, Y.-S. Kim, D. Brown, C. Staben, R. Dean, and M. Farman Organization of chromosome ends in the rice blast fungus, Magnaporthe oryzae Nucleic Acids Res., October 18, 2006; 34(17): 4685 - 4701. [Abstract] [Full Text] [PDF]

				G.-F. Richard and B. Dujon Molecular Evolution of Minisatellites in Hemiascomycetous Yeasts Mol. Biol. Evol., January 1, 2006; 23(1): 189 - 202. [Abstract] [Full Text] [PDF]

				E. Trelles-Sticken, S. Bonfils, J. Sollier, V. Geli, H. Scherthan, and C. de La Roche Saint-Andre Set1- and Clb5-deficiencies disclose the differential regulation of centromere and telomere dynamics in Saccharomyces cerevisiae meiosis J. Cell Sci., November 1, 2005; 118(21): 4985 - 4994. [Abstract] [Full Text] [PDF]

				H. B. Schlecht, M. Lichten, and A. S. H. Goldman Compartmentalization of the Yeast Meiotic Nucleus Revealed by Analysis of Ectopic Recombination Genetics, November 1, 2004; 168(3): 1189 - 1203. [Abstract] [Full Text] [PDF]

				M. K. Zubko, S. Guillard, and D. Lydall Exo1 and Rad24 Differentially Regulate Generation of ssDNA at Telomeres of Saccharomyces cerevisiae cdc13-1 Mutants Genetics, September 1, 2004; 168(1): 103 - 115. [Abstract] [Full Text] [PDF]

				D. Lydall Hiding at the ends of yeast chromosomes: telomeres, nucleases and checkpoint pathways J. Cell Sci., October 15, 2003; 116(20): 4057 - 4065. [Abstract] [Full Text] [PDF]

				J. E. Lowell, A. I. Roughton, V. Lundblad, and L. Pillus Telomerase-Independent Proliferation Is Influenced by Cell Type in Saccharomyces cerevisiae Genetics, July 1, 2003; 164(3): 909 - 921. [Abstract] [Full Text] [PDF]

				D. Carro, E. Bartra, and B. Pina Karyotype Rearrangements in a Wine Yeast Strain by rad52-Dependent and rad52-Independent Mechanisms Appl. Envir. Microbiol., April 1, 2003; 69(4): 2161 - 2165. [Abstract] [Full Text] [PDF]

				W. Gao, C. H. Khang, S.-Y. Park, Y.-H. Lee, and S. Kang Evolution and Organization of a Highly Dynamic, Subtelomeric Helicase Gene Family in the Rice Blast Fungus Magnaporthe grisea Genetics, September 1, 2002; 162(1): 103 - 112. [Abstract] [Full Text] [PDF]

				Y. Huang Transcriptional silencing in Saccharomyces cerevisiae and Schizosaccharomyces pombe Nucleic Acids Res., April 1, 2002; 30(7): 1465 - 1482. [Abstract] [Full Text] [PDF]

				A. Poloumienko, A. Dershowitz, J. De, and C. S. Newlon Completion of Replication Map of Saccharomyces cerevisiae Chromosome III Mol. Biol. Cell, November 1, 2001; 12(11): 3317 - 3327. [Abstract] [Full Text] [PDF]

				E. Lebrun, E. Revardel, C. Boscheron, R. Li, E. Gilson, and G. Fourel Protosilencers in Saccharomyces cerevisiae Subtelomeric Regions Genetics, May 1, 2001; 158(1): 167 - 176. [Abstract] [Full Text]

				P. Heun, T. Laroche, M.K. Raghuraman, and S. M. Gasser The Positioning and Dynamics of Origins of Replication in the Budding Yeast Nucleus J. Cell Biol., January 22, 2001; 152(2): 385 - 400. [Abstract] [Full Text] [PDF]

				H. Chibana, J. L. Beckerman, and P.T. Magee Fine-Resolution Physical Mapping of Genomic Diversity in Candida albicans Genome Res., December 1, 2000; 10(12): 1865 - 1877. [Abstract] [Full Text]

				E. Trelles-Sticken, M. E. Dresser, and H. Scherthan Meiotic Telomere Protein Ndj1p Is Required for Meiosis-Specific Telomere Distribution, Bouquet Formation and Efficient Homologue Pairing J. Cell Biol., October 2, 2000; 151(1): 95 - 106. [Abstract] [Full Text] [PDF]

				S.-C. Teng and V. A. Zakian Telomere-Telomere Recombination Is an Efficient Bypass Pathway for Telomere Maintenance in Saccharomyces cerevisiae Mol. Cell. Biol., December 1, 1999; 19(12): 8083 - 8093. [Abstract] [Full Text] [PDF]

				L. M. Larraya, G. Pérez, M. M. Peñas, J. J. P. Baars, T. S. P. Mikosch, A. G. Pisabarro, and L. Ramírez Molecular Karyotype of the White Rot Fungus Pleurotus ostreatus Appl. Envir. Microbiol., August 1, 1999; 65(8): 3413 - 3417. [Abstract] [Full Text]

				R. J. Craven and T. D. Petes Dependence of the Regulation of Telomere Length on the Type of Subtelomeric Repeat in the Yeast Saccharomyces cerevisiae Genetics, August 1, 1999; 152(4): 1531 - 1541. [Abstract] [Full Text]

				S. Venditti, M. A. Vega-Palas, and E. Di Mauro Heterochromatin Organization of a Natural Yeast Telomere. RECRUITMENT OF Sir3p THROUGH INTERACTION WITH HISTONE H4 N TERMINUS IS REQUIRED FOR THE ESTABLISHMENT OF REPRESSIVE STRUCTURES J. Biol. Chem., January 22, 1999; 274(4): 1928 - 1933. [Abstract] [Full Text] [PDF]

				E Trelles-Sticken, J Loidl, and H Scherthan Bouquet formation in budding yeast: initiation of recombination is not required for meiotic telomere clustering J. Cell Sci., January 3, 1999; 112(5): 651 - 658. [Abstract] [PDF]

				M. Yamada, N. Hayatsu, A. Matsuura, and F. Ishikawa Y'-Help1, a DNA Helicase Encoded by the Yeast Subtelomeric Y' Element, Is Induced in Survivors Defective for Telomerase J. Biol. Chem., December 11, 1998; 273(50): 33360 - 33366. [Abstract] [Full Text] [PDF]

				J. B. Stavenhagen and V. A. Zakian Yeast telomeres exert a position effect on recombination between internal tracts of yeast telomeric DNA Genes & Dev., October 1, 1998; 12(19): 3044 - 3058. [Abstract] [Full Text]

				B. D. Bourns, M. K. Alexander, A. M. Smith, and V. A. Zakian Sir Proteins, Rif Proteins, and Cdc13p Bind Saccharomyces Telomeres In Vivo Mol. Cell. Biol., September 1, 1998; 18(9): 5600 - 5608. [Abstract] [Full Text]

				H. Chibana, B. B. Magee, S. Grindle, Y. Ran, S. Scherer, and P. T. Magee A Physical Map of Chromosome 7 of Candida albicans Genetics, August 1, 1998; 149(4): 1739 - 1752. [Abstract] [Full Text] [PDF]

				R. J. Britten Precise sequence complementarity between yeast chromosome ends and two classes of just-subtelomeric sequences PNAS, May 26, 1998; 95(11): 5906 - 5912. [Abstract] [Full Text] [PDF]

				M. A. Vega-Palas, S. Venditti, and E. Di Mauro Heterochromatin Organization of a Natural Yeast Telomere. CHANGES OF NUCLEOSOME DISTRIBUTION DRIVEN BY THE ABSENCE OF Sir3p J. Biol. Chem., April 17, 1998; 273(16): 9388 - 9392. [Abstract] [Full Text] [PDF]

				Q.-w. Jin, E. Trelles-Sticken, H. Scherthan, and J. Loidl Yeast Nuclei Display Prominent Centromere Clustering That Is Reduced in Nondividing Cells and in Meiotic Prophase J. Cell Biol., April 6, 1998; 141(1): 21 - 29. [Abstract] [Full Text] [PDF]

				P. Sanchez-Alonso and P. Guzman Organization of Chromosome Ends in Ustilago maydis. RecQ-like Helicase Motifs at Telomeric Regions Genetics, March 1, 1998; 148(3): 1043 - 1054. [Abstract] [Full Text] [PDF]