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Defective meiosis in telomere-silencing mutants of Schizosaccharomyces pombe

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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Figure 1: Identification and analysis of S.pombe mutants with defective silencing at telomeres.
Figure 2: Telomere mutants display defects in meiosis.
Figure 3: Telomeres fail to associate with the spindle pole body in telomere mutants.
Figure 4: lot2-s17 displays aberrant horsetail movement and reduced recombination during meiotic prophase.

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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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Correspondence to Robin C. Allshire.

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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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