Skip to main content
NCBI home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1993 Aug;13(8):4578–4587. doi: 10.1128/mcb.13.8.4578

Centromeres of the fission yeast Schizosaccharomyces pombe are highly variable genetic loci.

N C Steiner 1, K M Hahnenberger 1, L Clarke 1
PMCID: PMC360078  PMID: 8336703

Abstract

Gross variations in the structure of the centromere of Schizosaccharomyces pombe chromosome III (cen3) were apparent following characterization of this centromeric DNA in strain Sp223 and comparison of the structure with that of cen3 in three other commonly used laboratory strains. Further differences in centromere structure were revealed when the structure of the centromere of S. pombe chromosome II (cen2) was compared among common laboratory strains and when the structures of cen2 and cen3 from our laboratory strains were compared with those reported from other laboratories. Differences observed in cen3 structure include variations in the arrangement of the centromeric K repeats and an inverted orientation of the conserved centromeric central core. In addition, we have identified two laboratory strains that contain a minimal cen2 repeat structure that lacks the tandem copies of the cen2-specific block of K-L-B-J repeats characteristic of Sp223 cen2. We have also determined that certain centromeric DNA structural motifs are relatively conserved among the four laboratory strains and eight additional wild-type S. pombe strains isolated from various food and beverage sources. We conclude that in S. pombe, as in higher eukaryotes, the centromere of a particular chromosome is not a defined genetic locus but can contain significant variability. However, the basic DNA structural motif of a central core immediately flanked by inverted repeats is a common parameter of the S. pombe centromere.

Full text

PDF
4578

Images in this article

4581Image
on p.4581
4582Image
on p.4582
4583Image
on p.4583
4583Image
on p.4583
4584Image
on p.4584
4585Image
on p.4585

Selected References

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

  1. Beach D. H., Klar A. J. Rearrangements of the transposable mating-type cassettes of fission yeast. EMBO J. 1984 Mar;3(3):603–610. doi: 10.1002/j.1460-2075.1984.tb01855.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brutlag D. L. Molecular arrangement and evolution of heterochromatic DNA. Annu Rev Genet. 1980;14:121–144. doi: 10.1146/annurev.ge.14.120180.001005. [DOI] [PubMed] [Google Scholar]
  3. Carle G. F., Frank M., Olson M. V. Electrophoretic separations of large DNA molecules by periodic inversion of the electric field. Science. 1986 Apr 4;232(4746):65–68. doi: 10.1126/science.3952500. [DOI] [PubMed] [Google Scholar]
  4. Chikashige Y., Kinoshita N., Nakaseko Y., Matsumoto T., Murakami S., Niwa O., Yanagida M. Composite motifs and repeat symmetry in S. pombe centromeres: direct analysis by integration of NotI restriction sites. Cell. 1989 Jun 2;57(5):739–751. doi: 10.1016/0092-8674(89)90789-7. [DOI] [PubMed] [Google Scholar]
  5. Clarke L., Amstutz H., Fishel B., Carbon J. Analysis of centromeric DNA in the fission yeast Schizosaccharomyces pombe. Proc Natl Acad Sci U S A. 1986 Nov;83(21):8253–8257. doi: 10.1073/pnas.83.21.8253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Clarke L., Baum M. P. Functional analysis of a centromere from fission yeast: a role for centromere-specific repeated DNA sequences. Mol Cell Biol. 1990 May;10(5):1863–1872. doi: 10.1128/mcb.10.5.1863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Clarke L. Centromeres of budding and fission yeasts. Trends Genet. 1990 May;6(5):150–154. doi: 10.1016/0168-9525(90)90149-z. [DOI] [PubMed] [Google Scholar]
  8. Cottarel G., Shero J. H., Hieter P., Hegemann J. H. A 125-base-pair CEN6 DNA fragment is sufficient for complete meiotic and mitotic centromere functions in Saccharomyces cerevisiae. Mol Cell Biol. 1989 Aug;9(8):3342–3349. doi: 10.1128/mcb.9.8.3342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fishel B., Amstutz H., Baum M., Carbon J., Clarke L. Structural organization and functional analysis of centromeric DNA in the fission yeast Schizosaccharomyces pombe. Mol Cell Biol. 1988 Feb;8(2):754–763. doi: 10.1128/mcb.8.2.754. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hahnenberger K. M., Baum M. P., Polizzi C. M., Carbon J., Clarke L. Construction of functional artificial minichromosomes in the fission yeast Schizosaccharomyces pombe. Proc Natl Acad Sci U S A. 1989 Jan;86(2):577–581. doi: 10.1073/pnas.86.2.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hahnenberger K. M., Carbon J., Clarke L. Identification of DNA regions required for mitotic and meiotic functions within the centromere of Schizosaccharomyces pombe chromosome I. Mol Cell Biol. 1991 Apr;11(4):2206–2215. doi: 10.1128/mcb.11.4.2206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. doi: 10.1128/jb.153.1.163-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jabs E. W., Goble C. A., Cutting G. R. Macromolecular organization of human centromeric regions reveals high-frequency, polymorphic macro DNA repeats. Proc Natl Acad Sci U S A. 1989 Jan;86(1):202–206. doi: 10.1073/pnas.86.1.202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kuhn R. M., Clarke L., Carbon J. Clustered tRNA genes in Schizosaccharomyces pombe centromeric DNA sequence repeats. Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1306–1310. doi: 10.1073/pnas.88.4.1306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Murakami S., Matsumoto T., Niwa O., Yanagida M. Structure of the fission yeast centromere cen3: direct analysis of the reiterated inverted region. Chromosoma. 1991 Dec;101(4):214–221. doi: 10.1007/BF00365153. [DOI] [PubMed] [Google Scholar]
  16. Nakaseko Y., Adachi Y., Funahashi S., Niwa O., Yanagida M. Chromosome walking shows a highly homologous repetitive sequence present in all the centromere regions of fission yeast. EMBO J. 1986 May;5(5):1011–1021. doi: 10.1002/j.1460-2075.1986.tb04316.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Nakaseko Y., Kinoshita N., Yanagida M. A novel sequence common to the centromere regions of Schizosaccharomyces pombe chromosomes. Nucleic Acids Res. 1987 Jun 25;15(12):4705–4715. doi: 10.1093/nar/15.12.4705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Niwa O., Matsumoto T., Chikashige Y., Yanagida M. Characterization of Schizosaccharomyces pombe minichromosome deletion derivatives and a functional allocation of their centromere. EMBO J. 1989 Oct;8(10):3045–3052. doi: 10.1002/j.1460-2075.1989.tb08455.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Orr-Weaver T. L., Szostak J. W., Rothstein R. J. Yeast transformation: a model system for the study of recombination. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6354–6358. doi: 10.1073/pnas.78.10.6354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Peacock W. J., Lohe A. R., Gerlach W. L., Dunsmuir P., Dennis E. S., Appels R. Fine structure and evolution of DNA in heterochromatin. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 2):1121–1135. doi: 10.1101/sqb.1978.042.01.113. [DOI] [PubMed] [Google Scholar]
  21. Polizzi C., Clarke L. The chromatin structure of centromeres from fission yeast: differentiation of the central core that correlates with function. J Cell Biol. 1991 Jan;112(2):191–201. doi: 10.1083/jcb.112.2.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Takahashi K., Murakami S., Chikashige Y., Funabiki H., Niwa O., Yanagida M. A low copy number central sequence with strict symmetry and unusual chromatin structure in fission yeast centromere. Mol Biol Cell. 1992 Jul;3(7):819–835. doi: 10.1091/mbc.3.7.819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Takahashi K., Murakami S., Chikashige Y., Niwa O., Yanagida M. A large number of tRNA genes are symmetrically located in fission yeast centromeres. J Mol Biol. 1991 Mar 5;218(1):13–17. doi: 10.1016/0022-2836(91)90867-6. [DOI] [PubMed] [Google Scholar]
  24. Wevrick R., Earnshaw W. C., Howard-Peebles P. N., Willard H. F. Partial deletion of alpha satellite DNA associated with reduced amounts of the centromere protein CENP-B in a mitotically stable human chromosome rearrangement. Mol Cell Biol. 1990 Dec;10(12):6374–6380. doi: 10.1128/mcb.10.12.6374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wevrick R., Willard H. F. Long-range organization of tandem arrays of alpha satellite DNA at the centromeres of human chromosomes: high-frequency array-length polymorphism and meiotic stability. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9394–9398. doi: 10.1073/pnas.86.23.9394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Zimmer M., Welser F., Oraler G., Wolf K. Distribution of mitochondrial introns in the species Schizosaccharomyces pombe and the origin of the group II intron in the gene encoding apocytochrome b. Curr Genet. 1987;12(5):329–336. doi: 10.1007/BF00405755. [DOI] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES