Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1994 Mar;136(3):789–802. doi: 10.1093/genetics/136.3.789

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

E J Louis 1, E S Naumova 1, A Lee 1, G Naumov 1, J E Haber 1
PMCID: PMC1205885  PMID: 8005434

Abstract

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.

Full Text

The Full Text of this article is available as a PDF (5.3 MB).

Selected References

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

  1. Allshire R. C., Dempster M., Hastie N. D. Human telomeres contain at least three types of G-rich repeat distributed non-randomly. Nucleic Acids Res. 1989 Jun 26;17(12):4611–4627. doi: 10.1093/nar/17.12.4611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bedbrook J. R., Jones J., O'Dell M., Thompson R. D., Flavell R. B. A molecular description of telometic heterochromatin in secale species. Cell. 1980 Feb;19(2):545–560. doi: 10.1016/0092-8674(80)90529-2. [DOI] [PubMed] [Google Scholar]
  3. Biessmann H., Champion L. E., O'Hair M., Ikenaga K., Kasravi B., Mason J. M. Frequent transpositions of Drosophila melanogaster HeT-A transposable elements to receding chromosome ends. EMBO J. 1992 Dec;11(12):4459–4469. doi: 10.1002/j.1460-2075.1992.tb05547.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blackburn E. H. Telomeres. Trends Biochem Sci. 1991 Oct;16(10):378–381. doi: 10.1016/0968-0004(91)90155-o. [DOI] [PubMed] [Google Scholar]
  5. Brigati C., Kurtz S., Balderes D., Vidali G., Shore D. An essential yeast gene encoding a TTAGGG repeat-binding protein. Mol Cell Biol. 1993 Feb;13(2):1306–1314. doi: 10.1128/mcb.13.2.1306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Button L. L., Astell C. R. The Saccharomyces cerevisiae chromosome III left telomere has a type X, but not a type Y', ARS region. Mol Cell Biol. 1986 Apr;6(4):1352–1356. doi: 10.1128/mcb.6.4.1352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Carlson M., Celenza J. L., Eng F. J. Evolution of the dispersed SUC gene family of Saccharomyces by rearrangements of chromosome telomeres. Mol Cell Biol. 1985 Nov;5(11):2894–2902. doi: 10.1128/mcb.5.11.2894. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chan C. S., Tye B. K. A family of Saccharomyces cerevisiae repetitive autonomously replicating sequences that have very similar genomic environments. J Mol Biol. 1983 Aug 15;168(3):505–523. doi: 10.1016/s0022-2836(83)80299-x. [DOI] [PubMed] [Google Scholar]
  9. Chan C. S., Tye B. K. Organization of DNA sequences and replication origins at yeast telomeres. Cell. 1983 Jun;33(2):563–573. doi: 10.1016/0092-8674(83)90437-3. [DOI] [PubMed] [Google Scholar]
  10. Charron M. J., Michels C. A. The naturally occurring alleles of MAL1 in Saccharomyces species evolved by various mutagenic processes including chromosomal rearrangement. Genetics. 1988 Sep;120(1):83–93. doi: 10.1093/genetics/120.1.83. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Charron M. J., Read E., Haut S. R., Michels C. A. Molecular evolution of the telomere-associated MAL loci of Saccharomyces. Genetics. 1989 Jun;122(2):307–316. doi: 10.1093/genetics/122.2.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cheng J. F., Smith C. L., Cantor C. R. Structural and transcriptional analysis of a human subtelomeric repeat. Nucleic Acids Res. 1991 Jan 11;19(1):149–154. doi: 10.1093/nar/19.1.149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cooke H. J., Brown W. R., Rappold G. A. Hypervariable telomeric sequences from the human sex chromosomes are pseudoautosomal. Nature. 1985 Oct 24;317(6039):687–692. doi: 10.1038/317687a0. [DOI] [PubMed] [Google Scholar]
  14. Corcoran L. M., Thompson J. K., Walliker D., Kemp D. J. Homologous recombination within subtelomeric repeat sequences generates chromosome size polymorphisms in P. falciparum. Cell. 1988 Jun 3;53(5):807–813. doi: 10.1016/0092-8674(88)90097-9. [DOI] [PubMed] [Google Scholar]
  15. Cross S., Lindsey J., Fantes J., McKay S., McGill N., Cooke H. The structure of a subterminal repeated sequence present on many human chromosomes. Nucleic Acids Res. 1990 Nov 25;18(22):6649–6657. doi: 10.1093/nar/18.22.6649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Danilevskaya O., Lofsky A., Kurenova E. V., Pardue M. L. The Y chromosome of Drosophila melanogaster contains a distinctive subclass of Het-A-related repeats. Genetics. 1993 Jun;134(2):531–543. doi: 10.1093/genetics/134.2.531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Foote S. J., Kemp D. J. Chromosomes of malaria parasites. Trends Genet. 1989 Oct;5(10):337–342. doi: 10.1016/0168-9525(89)90139-x. [DOI] [PubMed] [Google Scholar]
  18. Gottschling D. E., Aparicio O. M., Billington B. L., Zakian V. A. Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell. 1990 Nov 16;63(4):751–762. doi: 10.1016/0092-8674(90)90141-z. [DOI] [PubMed] [Google Scholar]
  19. Horowitz H., Thorburn P., Haber J. E. Rearrangements of highly polymorphic regions near telomeres of Saccharomyces cerevisiae. Mol Cell Biol. 1984 Nov;4(11):2509–2517. doi: 10.1128/mcb.4.11.2509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kane S. M., Roth R. Carbohydrate metabolism during ascospore development in yeast. J Bacteriol. 1974 Apr;118(1):8–14. doi: 10.1128/jb.118.1.8-14.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Karpen G. H., Spradling A. C. Analysis of subtelomeric heterochromatin in the Drosophila minichromosome Dp1187 by single P element insertional mutagenesis. Genetics. 1992 Nov;132(3):737–753. doi: 10.1093/genetics/132.3.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kramer K. M., Haber J. E. New telomeres in yeast are initiated with a highly selected subset of TG1-3 repeats. Genes Dev. 1993 Dec;7(12A):2345–2356. doi: 10.1101/gad.7.12a.2345. [DOI] [PubMed] [Google Scholar]
  23. Link A. J., Olson M. V. Physical map of the Saccharomyces cerevisiae genome at 110-kilobase resolution. Genetics. 1991 Apr;127(4):681–698. doi: 10.1093/genetics/127.4.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Liu Z. P., Tye B. K. A yeast protein that binds to vertebrate telomeres and conserved yeast telomeric junctions. Genes Dev. 1991 Jan;5(1):49–59. doi: 10.1101/gad.5.1.49. [DOI] [PubMed] [Google Scholar]
  25. Louis E. J., Haber J. E. Evolutionarily recent transfer of a group I mitochondrial intron to telomere regions in Saccharomyces cerevisiae. Curr Genet. 1991 Nov;20(5):411–415. doi: 10.1007/BF00317070. [DOI] [PubMed] [Google Scholar]
  26. Louis E. J., Haber J. E. Mitotic recombination among subtelomeric Y' repeats in Saccharomyces cerevisiae. Genetics. 1990 Mar;124(3):547–559. doi: 10.1093/genetics/124.3.547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Louis E. J., Haber J. E. The subtelomeric Y' repeat family in Saccharomyces cerevisiae: an experimental system for repeated sequence evolution. Genetics. 1990 Mar;124(3):533–545. doi: 10.1093/genetics/124.3.533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. McCusker J. H., Haber J. E. Cycloheximide-resistant temperature-sensitive lethal mutations of Saccharomyces cerevisiae. Genetics. 1988 Jun;119(2):303–315. doi: 10.1093/genetics/119.2.303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Michels C. A., Read E., Nat K., Charron M. J. The telomere-associated MAL3 locus of Saccharomyces is a tandem array of repeated genes. Yeast. 1992 Aug;8(8):655–665. doi: 10.1002/yea.320080809. [DOI] [PubMed] [Google Scholar]
  30. Naumov G. I., Naumova E. S., Lantto R. A., Louis E. J., Korhola M. Genetic homology between Saccharomyces cerevisiae and its sibling species S. paradoxus and S. bayanus: electrophoretic karyotypes. Yeast. 1992 Aug;8(8):599–612. doi: 10.1002/yea.320080804. [DOI] [PubMed] [Google Scholar]
  31. Naumov G., Naumova E., Turakainen H., Suominen P., Korhola M. Polymeric genes MEL8, MEL9 and MEL10--new members of alpha-galactosidase gene family in Saccharomyces cerevisiae. Curr Genet. 1991 Sep;20(4):269–276. doi: 10.1007/BF00318514. [DOI] [PubMed] [Google Scholar]
  32. Oliver S. G., van der Aart Q. J., Agostoni-Carbone M. L., Aigle M., Alberghina L., Alexandraki D., Antoine G., Anwar R., Ballesta J. P., Benit P. The complete DNA sequence of yeast chromosome III. Nature. 1992 May 7;357(6373):38–46. doi: 10.1038/357038a0. [DOI] [PubMed] [Google Scholar]
  33. Riethman H. C., Moyzis R. K., Meyne J., Burke D. T., Olson M. V. Cloning human telomeric DNA fragments into Saccharomyces cerevisiae using a yeast-artificial-chromosome vector. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6240–6244. doi: 10.1073/pnas.86.16.6240. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Saiga H., Edström J. E. Long tandem arrays of complex repeat units in Chironomus telomeres. EMBO J. 1985 Mar;4(3):799–804. doi: 10.1002/j.1460-2075.1985.tb03700.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
  36. Shampay J., Szostak J. W., Blackburn E. H. DNA sequences of telomeres maintained in yeast. Nature. 1984 Jul 12;310(5973):154–157. doi: 10.1038/310154a0. [DOI] [PubMed] [Google Scholar]
  37. Szostak J. W., Blackburn E. H. Cloning yeast telomeres on linear plasmid vectors. Cell. 1982 May;29(1):245–255. doi: 10.1016/0092-8674(82)90109-x. [DOI] [PubMed] [Google Scholar]
  38. Voytas D. F., Boeke J. D. Yeast retrotransposon revealed. Nature. 1992 Aug 27;358(6389):717–717. doi: 10.1038/358717a0. [DOI] [PubMed] [Google Scholar]
  39. Walmsley R. W., Chan C. S., Tye B. K., Petes T. D. Unusual DNA sequences associated with the ends of yeast chromosomes. Nature. 1984 Jul 12;310(5973):157–160. doi: 10.1038/310157a0. [DOI] [PubMed] [Google Scholar]
  40. Zakian V. A., Blanton H. M. Distribution of telomere-associated sequences on natural chromosomes in Saccharomyces cerevisiae. Mol Cell Biol. 1988 May;8(5):2257–2260. doi: 10.1128/mcb.8.5.2257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. de Lange T., Shiue L., Myers R. M., Cox D. R., Naylor S. L., Killery A. M., Varmus H. E. Structure and variability of human chromosome ends. Mol Cell Biol. 1990 Feb;10(2):518–527. doi: 10.1128/mcb.10.2.518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. de Steensma H. Y., de Jonge P., Kaptein A., Kaback D. B. Molecular cloning of chromosome I DNA from Saccharomyces cerevisiae: localization of a repeated sequence containing an acid phosphatase gene near a telomere of chromosome I and chromosome VIII. Curr Genet. 1989 Sep;16(3):131–137. doi: 10.1007/BF00391468. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES