Abstract
Interactions between homologous chromosomes (pairing, recombination) are of central importance for meiosis. We studied entire chromosomes and defined chromosomal subregions in synchronous meiotic cultures of Schizosaccharomyces pombe by fluorescence in situ hybridization. Probes of different complexity were applied to spread nuclei, to delineate whole chromosomes, to visualize repeated sequences of centromeres, telomeres, and ribosomal DNA, and to study unique sequences of different chromosomal regions. In diploid nuclei, homologous chromosomes share a joint territory even before entry into meiosis. The centromeres of all chromosomes are clustered in vegetative and meiotic prophase cells, whereas the telomeres cluster near the nucleolus early in meiosis and maintain this configuration throughout meiotic prophase. Telomeres and centromeres appear to play crucial roles for chromosome organization and pairing, both in vegetative cells and during meiosis. Homologous pairing of unique sequences shows regional differences and is most frequent near centromeres and telomeres. Multiple homologous interactions are formed independently of each other. Pairing increases during meiosis, but not all chromosomal regions become closely paired in every meiosis. There is no detectable axial compaction of chromosomes in meiotic prophase. S. pombe does not form mature synaptonemal complexes, but axial element-like structures (linear elements), which were analyzed in parallel. Their appearance coincides with pairing of interstitial chromosomal regions. Axial elements may define minimal structures required for efficient pairing and recombination of meiotic chromosomes.
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- Allshire R. C., Gosden J. R., Cross S. H., Cranston G., Rout D., Sugawara N., Szostak J. W., Fantes P. A., Hastie N. D. Telomeric repeat from T. thermophila cross hybridizes with human telomeres. Nature. 1988 Apr 14;332(6165):656–659. doi: 10.1038/332656a0. [DOI] [PubMed] [Google Scholar]
- Amstutz H., Munz P., Heyer W. D., Leupoid U., Kohli J. Concerted evolution of tRNA genes: intergenic conversion among three unlinked serine tRNA genes in S. pombe. Cell. 1985 Apr;40(4):879–886. doi: 10.1016/0092-8674(85)90347-2. [DOI] [PubMed] [Google Scholar]
- Baker B. S., Carpenter A. T., Esposito M. S., Esposito R. E., Sandler L. The genetic control of meiosis. Annu Rev Genet. 1976;10:53–134. doi: 10.1146/annurev.ge.10.120176.000413. [DOI] [PubMed] [Google Scholar]
- Blackburn E. H. Telomeres: no end in sight. Cell. 1994 Jun 3;77(5):621–623. doi: 10.1016/0092-8674(94)90046-9. [DOI] [PubMed] [Google Scholar]
- Blackburn E. H. The molecular structure of centromeres and telomeres. Annu Rev Biochem. 1984;53:163–194. doi: 10.1146/annurev.bi.53.070184.001115. [DOI] [PubMed] [Google Scholar]
- Bresch C., Müller G., Egel R. Genes involved in meiosis and sporulation of a yeast. Mol Gen Genet. 1968;102(4):301–306. doi: 10.1007/BF00433721. [DOI] [PubMed] [Google Scholar]
- Bähler J., Hagens G., Holzinger G., Scherthan H., Heyer W. D. Saccharomyces cerevisiae cells lacking the homologous pairing protein p175SEP1 arrest at pachytene during meiotic prophase. Chromosoma. 1994 Apr;103(2):129–141. doi: 10.1007/BF00352322. [DOI] [PubMed] [Google Scholar]
- Bähler J., Schuchert P., Grimm C., Kohli J. Synchronized meiosis and recombination in fission yeast: observations with pat1-114 diploid cells. Curr Genet. 1991 Jun;19(6):445–451. doi: 10.1007/BF00312735. [DOI] [PubMed] [Google Scholar]
- Bähler J., Wyler T., Loidl J., Kohli J. Unusual nuclear structures in meiotic prophase of fission yeast: a cytological analysis. J Cell Biol. 1993 Apr;121(2):241–256. doi: 10.1083/jcb.121.2.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Camerini-Otero R. D., Hsieh P. Parallel DNA triplexes, homologous recombination, and other homology-dependent DNA interactions. Cell. 1993 Apr 23;73(2):217–223. doi: 10.1016/0092-8674(93)90224-e. [DOI] [PubMed] [Google Scholar]
- Chikashige Y., Ding D. Q., Funabiki H., Haraguchi T., Mashiko S., Yanagida M., Hiraoka Y. Telomere-led premeiotic chromosome movement in fission yeast. Science. 1994 Apr 8;264(5156):270–273. doi: 10.1126/science.8146661. [DOI] [PubMed] [Google Scholar]
- 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]
- Collins I., Newlon C. S. Meiosis-specific formation of joint DNA molecules containing sequences from homologous chromosomes. Cell. 1994 Jan 14;76(1):65–75. doi: 10.1016/0092-8674(94)90173-2. [DOI] [PubMed] [Google Scholar]
- Cremer T., Kurz A., Zirbel R., Dietzel S., Rinke B., Schröck E., Speicher M. R., Mathieu U., Jauch A., Emmerich P. Role of chromosome territories in the functional compartmentalization of the cell nucleus. Cold Spring Harb Symp Quant Biol. 1993;58:777–792. doi: 10.1101/sqb.1993.058.01.085. [DOI] [PubMed] [Google Scholar]
- Dawe R. K., Sedat J. W., Agard D. A., Cande W. Z. Meiotic chromosome pairing in maize is associated with a novel chromatin organization. Cell. 1994 Mar 11;76(5):901–912. doi: 10.1016/0092-8674(94)90364-6. [DOI] [PubMed] [Google Scholar]
- De Veaux L. C., Hoagland N. A., Smith G. R. Seventeen complementation groups of mutations decreasing meiotic recombination in Schizosaccharomyces pombe. Genetics. 1992 Feb;130(2):251–262. doi: 10.1093/genetics/130.2.251. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DeVeaux L. C., Smith G. R. Region-specific activators of meiotic recombination in Schizosaccharomyces pombe. Genes Dev. 1994 Jan;8(2):203–210. doi: 10.1101/gad.8.2.203. [DOI] [PubMed] [Google Scholar]
- Egel-Mitani M., Olson L. W., Egel R. Meiosis in Aspergillus nidulans: another example for lacking synaptonemal complexes in the absence of crossover interference. Hereditas. 1982;97(2):179–187. doi: 10.1111/j.1601-5223.1982.tb00761.x. [DOI] [PubMed] [Google Scholar]
- Egel R., Egel-Mitani M. Premeiotic DNA synthesis in fission yeast. Exp Cell Res. 1974 Sep;88(1):127–134. doi: 10.1016/0014-4827(74)90626-0. [DOI] [PubMed] [Google Scholar]
- Fan J. B., Chikashige Y., Smith C. L., Niwa O., Yanagida M., Cantor C. R. Construction of a Not I restriction map of the fission yeast Schizosaccharomyces pombe genome. Nucleic Acids Res. 1989 Apr 11;17(7):2801–2818. doi: 10.1093/nar/17.7.2801. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fan J. B., Grothues D., Smith C. L. Alignment of Sfi I sites with the Not I restriction map of Schizosaccharomyces pombe genome. Nucleic Acids Res. 1991 Nov 25;19(22):6289–6294. doi: 10.1093/nar/19.22.6289. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Funabiki H., Hagan I., Uzawa S., Yanagida M. Cell cycle-dependent specific positioning and clustering of centromeres and telomeres in fission yeast. J Cell Biol. 1993 Jun;121(5):961–976. doi: 10.1083/jcb.121.5.961. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gilson E., Laroche T., Gasser S. M. Telomeres and the functional architecture of the nucleus. Trends Cell Biol. 1993 Apr;3(4):128–134. doi: 10.1016/0962-8924(93)90175-z. [DOI] [PubMed] [Google Scholar]
- Guacci V., Hogan E., Koshland D. Chromosome condensation and sister chromatid pairing in budding yeast. J Cell Biol. 1994 May;125(3):517–530. doi: 10.1083/jcb.125.3.517. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Haaf T., Schmid M. Chromosome topology in mammalian interphase nuclei. Exp Cell Res. 1991 Feb;192(2):325–332. doi: 10.1016/0014-4827(91)90048-y. [DOI] [PubMed] [Google Scholar]
- Haber J. E., Leung W. Y., Borts R. H., Lichten M. The frequency of meiotic recombination in yeast is independent of the number and position of homologous donor sequences: implications for chromosome pairing. Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1120–1124. doi: 10.1073/pnas.88.4.1120. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hawley R. S., Arbel T. Yeast genetics and the fall of the classical view of meiosis. Cell. 1993 Feb 12;72(3):301–303. doi: 10.1016/0092-8674(93)90108-3. [DOI] [PubMed] [Google Scholar]
- Henikoff S., Dreesen T. D. Trans-inactivation of the Drosophila brown gene: evidence for transcriptional repression and somatic pairing dependence. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6704–6708. doi: 10.1073/pnas.86.17.6704. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hilliker A. J., Appels R. The arrangement of interphase chromosomes: structural and functional aspects. Exp Cell Res. 1989 Dec;185(2):267–318. doi: 10.1016/0014-4827(89)90301-7. [DOI] [PubMed] [Google Scholar]
- Hiraoka Y., Dernburg A. F., Parmelee S. J., Rykowski M. C., Agard D. A., Sedat J. W. The onset of homologous chromosome pairing during Drosophila melanogaster embryogenesis. J Cell Biol. 1993 Feb;120(3):591–600. doi: 10.1083/jcb.120.3.591. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hoheisel J. D., Maier E., Mott R., McCarthy L., Grigoriev A. V., Schalkwyk L. C., Nizetic D., Francis F., Lehrach H. High resolution cosmid and P1 maps spanning the 14 Mb genome of the fission yeast S. pombe. Cell. 1993 Apr 9;73(1):109–120. doi: 10.1016/0092-8674(93)90164-l. [DOI] [PubMed] [Google Scholar]
- Hubert J., Bourgeois C. A. The nuclear skeleton and the spatial arrangement of chromosomes in the interphase nucleus of vertebrate somatic cells. Hum Genet. 1986 Sep;74(1):1–15. doi: 10.1007/BF00278778. [DOI] [PubMed] [Google Scholar]
- Iino Y., Yamamoto M. Negative control for the initiation of meiosis in Schizosaccharomyces pombe. Proc Natl Acad Sci U S A. 1985 Apr;82(8):2447–2451. doi: 10.1073/pnas.82.8.2447. [DOI] [PMC free article] [PubMed] [Google Scholar]
- King J. S., Mortimer R. K. A polymerization model of chiasma interference and corresponding computer simulation. Genetics. 1990 Dec;126(4):1127–1138. doi: 10.1093/genetics/126.4.1127. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kleckner N., Weiner B. M. Potential advantages of unstable interactions for pairing of chromosomes in meiotic, somatic, and premeiotic cells. Cold Spring Harb Symp Quant Biol. 1993;58:553–565. doi: 10.1101/sqb.1993.058.01.062. [DOI] [PubMed] [Google Scholar]
- Kohli J., Bähler J. Homologous recombination in fission yeast: absence of crossover interference and synaptonemal complex. Experientia. 1994 Mar 15;50(3):295–306. doi: 10.1007/BF01924013. [DOI] [PubMed] [Google Scholar]
- Kohli J., Hottinger H., Munz P., Strauss A., Thuriaux P. Genetic Mapping in SCHIZOSACCHAROMYCES POMBE by Mitotic and Meiotic Analysis and Induced Haploidization. Genetics. 1977 Nov;87(3):471–489. doi: 10.1093/genetics/87.3.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lichter P., Cremer T., Borden J., Manuelidis L., Ward D. C. Delineation of individual human chromosomes in metaphase and interphase cells by in situ suppression hybridization using recombinant DNA libraries. Hum Genet. 1988 Nov;80(3):224–234. doi: 10.1007/BF01790090. [DOI] [PubMed] [Google Scholar]
- Loidl J., Klein F., Scherthan H. Homologous pairing is reduced but not abolished in asynaptic mutants of yeast. J Cell Biol. 1994 Jun;125(6):1191–1200. doi: 10.1083/jcb.125.6.1191. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Loidl J., Nairz K., Klein F. Meiotic chromosome synapsis in a haploid yeast. Chromosoma. 1991 May;100(4):221–228. doi: 10.1007/BF00344155. [DOI] [PubMed] [Google Scholar]
- Loidl J. The initiation of meiotic chromosome pairing: the cytological view. Genome. 1990 Dec;33(6):759–778. doi: 10.1139/g90-115. [DOI] [PubMed] [Google Scholar]
- Maier E., Hoheisel J. D., McCarthy L., Mott R., Grigoriev A. V., Monaco A. P., Larin Z., Lehrach H. Complete coverage of the Schizosaccharomyces pombe genome in yeast artificial chromosomes. Nat Genet. 1992 Jul;1(4):273–277. doi: 10.1038/ng0792-273. [DOI] [PubMed] [Google Scholar]
- Matsumoto T., Fukui K., Niwa O., Sugawara N., Szostak J. W., Yanagida M. Identification of healed terminal DNA fragments in linear minichromosomes of Schizosaccharomyces pombe. Mol Cell Biol. 1987 Dec;7(12):4424–4430. doi: 10.1128/mcb.7.12.4424. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moens P. B. Molecular perspectives of chromosome pairing at meiosis. Bioessays. 1994 Feb;16(2):101–106. doi: 10.1002/bies.950160206. [DOI] [PubMed] [Google Scholar]
- Munz P., Amstutz H., Kohli J., Leupold U. Recombination between dispersed serine tRNA genes in Schizosaccharomyces pombe. Nature. 1982 Nov 18;300(5889):225–231. doi: 10.1038/300225a0. [DOI] [PubMed] [Google Scholar]
- Munz P. An analysis of interference in the fission yeast Schizosaccharomyces pombe. Genetics. 1994 Jul;137(3):701–707. doi: 10.1093/genetics/137.3.701. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Padmore R., Cao L., Kleckner N. Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell. 1991 Sep 20;66(6):1239–1256. doi: 10.1016/0092-8674(91)90046-2. [DOI] [PubMed] [Google Scholar]
- Palladino F., Laroche T., Gilson E., Axelrod A., Pillus L., Gasser S. M. SIR3 and SIR4 proteins are required for the positioning and integrity of yeast telomeres. Cell. 1993 Nov 5;75(3):543–555. doi: 10.1016/0092-8674(93)90388-7. [DOI] [PubMed] [Google Scholar]
- Pinkel D., Landegent J., Collins C., Fuscoe J., Segraves R., Lucas J., Gray J. Fluorescence in situ hybridization with human chromosome-specific libraries: detection of trisomy 21 and translocations of chromosome 4. Proc Natl Acad Sci U S A. 1988 Dec;85(23):9138–9142. doi: 10.1073/pnas.85.23.9138. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pinkel D., Straume T., Gray J. W. Cytogenetic analysis using quantitative, high-sensitivity, fluorescence hybridization. Proc Natl Acad Sci U S A. 1986 May;83(9):2934–2938. doi: 10.1073/pnas.83.9.2934. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pirrotta V. Transvection and long-distance gene regulation. Bioessays. 1990 Sep;12(9):409–414. doi: 10.1002/bies.950120903. [DOI] [PubMed] [Google Scholar]
- Ponticelli A. S., Smith G. R. Meiotic recombination-deficient mutants of Schizosaccharomyces pombe. Genetics. 1989 Sep;123(1):45–54. doi: 10.1093/genetics/123.1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roeder G. S. Chromosome synapsis and genetic recombination: their roles in meiotic chromosome segregation. Trends Genet. 1990 Dec;6(12):385–389. doi: 10.1016/0168-9525(90)90297-j. [DOI] [PubMed] [Google Scholar]
- Scherthan H., Loidl J., Schuster T., Schweizer D. Meiotic chromosome condensation and pairing in Saccharomyces cerevisiae studied by chromosome painting. Chromosoma. 1992 Oct;101(10):590–595. doi: 10.1007/BF00360535. [DOI] [PubMed] [Google Scholar]
- Scherthan H., Schweizer D., Loidl J. Delineation of individual chromosomes of Saccharomyces cerevisiae by two-colour in situ hybridization. Trends Genet. 1993 Feb;9(2):41–41. doi: 10.1016/0168-9525(93)90176-i. [DOI] [PubMed] [Google Scholar]
- Schwacha A., Kleckner N. Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell. 1994 Jan 14;76(1):51–63. doi: 10.1016/0092-8674(94)90172-4. [DOI] [PubMed] [Google Scholar]
- Steiner N. C., Hahnenberger K. M., Clarke L. Centromeres of the fission yeast Schizosaccharomyces pombe are highly variable genetic loci. Mol Cell Biol. 1993 Aug;13(8):4578–4587. doi: 10.1128/mcb.13.8.4578. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sym M., Engebrecht J. A., Roeder G. S. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell. 1993 Feb 12;72(3):365–378. doi: 10.1016/0092-8674(93)90114-6. [DOI] [PubMed] [Google Scholar]
- 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]
- Tartof K. D., Henikoff S. Trans-sensing effects from Drosophila to humans. Cell. 1991 Apr 19;65(2):201–203. doi: 10.1016/0092-8674(91)90153-p. [DOI] [PubMed] [Google Scholar]
- Uzawa S., Yanagida M. Visualization of centromeric and nucleolar DNA in fission yeast by fluorescence in situ hybridization. J Cell Sci. 1992 Feb;101(Pt 2):267–275. doi: 10.1242/jcs.101.2.267. [DOI] [PubMed] [Google Scholar]
- Weiner B. M., Kleckner N. Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell. 1994 Jul 1;77(7):977–991. doi: 10.1016/0092-8674(94)90438-3. [DOI] [PubMed] [Google Scholar]
- von Wettstein D., Rasmussen S. W., Holm P. B. The synaptonemal complex in genetic segregation. Annu Rev Genet. 1984;18:331–413. doi: 10.1146/annurev.ge.18.120184.001555. [DOI] [PubMed] [Google Scholar]