Abstract
During meiotic prophase, chromosomes frequently adopt a bouquet-like arrangement, with their telomeres clustered close to the nuclear periphery1,2,3. A dramatic example of this occurs in the fission yeast, Schizosaccharomyces pombe, where all telomeres aggregate adjacent to the spindle pole body (SPB)4,5,6,7. Nuclei then undergo rapid traverses of the cell, known as ‘horsetail’ movement, which is led by the SPB dragging telomeres and chromosomes behind4,6,7. This process may initiate or facilitate chromosome pairing before recombination and meiosis. With the aim of identifying components involved in telomere structure and function, we report here the isolation of S. pombe mutants defective in the ability to impose transcriptional silencing on genes placed near telomeres8. Two of these mutants, lot2-s17 and lot3-uv3, also display a dramatic lengthening of telomeric repeats. lot3-uv3 carries a mutation in Taz1 (ref. 9), a telomere-binding protein containing a Myb-like motif similar to two human telomere-binding proteins10,11. Meiosis is aberrant in these mutant yeast strains, and our analysis demonstrates a decreased association of telomeres with the SPB in meiotic prophase. This results in defective ‘horsetail’ movement, a significant reduction in recombination, low spore viability and chromosome missegregation through meiosis.
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References
Dernberg, A. F., Sedat, J. W., Cande, W. Z. & Bass, H. W. in Telomeres (eds Blackburn, E. H. & Grieder, C. W.) 295–338 (Cold Spring Harbor Laboratory Press, New York, 1995).
Scherthan, H. et al. Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J. Cell Biol. 134, 1109–1125 (1996).
Bass, H. W., Marshall, W. F., Sedat, J. W., Agard, D. A. & Cande, Z. W. Telomeres cluster de novo before the initiation of synapsis: a three-dimensional analysis of telomere positions before and during meiotic prophase. J. Cell Biol. 137, 5–18 (1997).
Chikashige, Y. et al. Telomere-led premeiotic chromosome movement in fission yeast. Science 264, 270–273 (1994).
Scherthan, H., Bahler, J. & Kohli, J. Dynamics of chromosome organisation and pairing during meiotic prophase in fission yeast. J. Cell Biol. 127, 273–285 (1994).
Kohli, J. Telomeres lead chromosome movement. Curr. Biol. 4, 724–727 (1994).
Chikashige, Y. et al. Meiotic nuclear reorganisation: switching the position of centromeres and telomeres in the fission yeast Schizosaccharomyces pombe. EMBO J. 16, 193–202 (1997).
Nimmo, E. R., Cranston, G. & Allshire, R. C. Telomere-associated chromosome breakage in fission yeast results in variegated expression of adjacent genes. EMBO J. 13, 3801–3811 (1994).
Cooper, J. P., Nimmo, E. R., Allshire, R. C. & Cech, T. R. Regulation of telomere length and function by a Myb-domain protein in fission yeast. Nature 385, 744–747 (1997).
Broccoli, D., Smogorzewska, A., Chong, L. & de Lange, T. Human telomeres contain two distinct Myb-related proteins TRF1 and TRF2. Nature Genet. 17, 231–235 (1997).
Bilaud, T. et al. Telomeric localization of TRF2, a novel human telobox protein. Nature Genet. 17, 236–239 (1997).
Karpen, G. H. Position-effect variegation and the new biology of heterochromatin. Curr. Opin. Genet. Dev. 4, 281–291 (1994).
Allshire, R. C., Javerzat, J.-P., Redhead, N. J. & Cranston, G. Position effect variegation at fission yeast centromeres. Cell 76, 157–160 (1994).
Allshire, R. C., Nimmo, E. R., Ekwall, K., Javerzat, J.-P. & Cranston, G. Mutations derepressing silent centromeric domains in fission yeast disrupt chromosome segregation. Genes Dev. 9, 218–2133 (1995).
Thon, G. & Klar, A. J. S. The clr1 locus regulates the expression of the cryptic mating-type loci in fission yeast. Genetics 131, 287–296 (1992).
Molnar, M., Bahler, J., Sipiczki, M. & Kohli, J. The rec8 gene of Schizosaccharomyces pombe is involved in linear element formation, chromosome pairing and sister-chromatid cohesion during meiosis. Genetics 141 61–73 (1995).
Niwa, O. & Yanagida, M. Triplod meiosis and aneuploidy in Schizosaccharomyces pombe: an unstable aneuploid disomic for chromosome III. Curr. Genet. 9, 463–470 (1985).
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. 121, 961–976 (1993).
Ekwall, K. et al. The chromodomain protein Swi6: a key component at fission yeast centromeres. Science 269, 1429–1431 (1995).
Ekwall, K. et al. Mutations in the fission yeast silencing factors clr4+ and rik1+ disrupt the localisation of the chromodomain protein Swi6p and impair centromere function. J. Cell Sci. 109, 2637–2648 (1996).
Hagan, I. M. & Yanagida, M. The product of the spindle formation gene sad1+ associates with the fission yeast spindle pole and is essential for viability. J. Cell Biol. 129, 1033–1047 (1995).
Heim, R., Cubitt, A. B. & Tsien, R. Y. Improved green fluorescence. Nature 373, 663–664 (1995).
Svoboda, A., Bahler, J. & Kohli, J. Microtubule-driven nuclear movements and linear elements as meiosis specific characteristics of the fission yeasts Schizosaccharomyces versatilis and Schizosaccharomyces pombe. Chromosoma 104, 203–214 (1995).
Munz, P. An analysis of interference in the fission yeast Schizosaccharomyces pombe. Genetics 137, 701–707 (1994).
Hoheisel, J. D. et al. High resolution cosmid and P1 maps spanning the 14 Mb genome of the fission yeast S. pombe. Cell 73, 109–120 (1993).
Mizukami, T. et al. A13 kb resolution cosmid map of the 14 Mb fission yeast genome by nonrandom sequence-tagged site mapping. Cell 73, 121–132 (1993).
Shimanuki, M. et al. Anovel fission yeast gene, kms1+, is required for the formation of meiotic prophase specific architecture. Mol. Gen. Genet. 254, 238–249 (1997).
Parvinen, M. & Sonderstrom, K.-E. Chromosome rotation and formation of synapsis. Nature 260, 534–535 (1976).
Lamb, N. E. et al. Characterization of susceptible chiasma configurations that increase the risk for maternal nondisjunction of chromosome 21. Hum. Mol. Genet. 6, 1391–1399 (1997).
Moreno, S., Klar, A. J. S. & Nurse, P. Molecular genetic analyses of fission yeast Schizosaccharomyces pombe. Meth. Enzymol. 194, 795–823 (1991).
Acknowledgements
We thank K. Ekwall, J. Partridge and B. Borgstrom for discussion and advice; H. Cooke and N. Hastie for comments on the manuscript; M. LeDizet for pREP3X-GFP; I. Hagan for anti-Sad1 sera; K. Gould for alerting us to the potential of his3+; J. Cooper for taz1Δ; N. Davidson, S. Bruce and D. Stewart for photography and artwork; and A. Brown for help with the Web Page. A.L.P. is a Caledonian Research Fellow of the Royal Society of Edinburgh; E.R.N. is supported by a project grant from the Cancer Research campaign to R.C.A.
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Nimmo, E., Pidoux, A., Perry, P. et al. Defective meiosis in telomere-silencing mutants of Schizosaccharomyces pombe. Nature 392, 825–828 (1998). https://doi.org/10.1038/33941
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DOI: https://doi.org/10.1038/33941
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