Published online 2 October 2000. doi:10.1083/jcb.151.1.95
© The Rockefeller University Press,
0021-9525/2000//95 $5.00
The Journal of Cell Biology, Volume 151, Number 1,
, 2000 95-106
Meiotic Telomere Protein Ndj1p Is Required for Meiosis-Specific Telomere Distribution, Bouquet Formation and Efficient Homologue Pairing
Edgar Trelles-Stickena,
Michael E. Dresserb, and
Harry Scherthana,c
a Department of Human Biology and Genetics, University of Kaiserslautern, D-67653 Kaiserslautern, Germany
b Program in Molecular and Cell Biology, Oklahoma Medical Research Foundation, Oklahoma City, Oklahoma 73104
c Department of Cell Biology, University of Kaiserslautern, D-67653 Kaiserslautern, Germany
Dept. of Cell Biology, University of Kaiserslautern, P.O. Box 3049, D-67653 Kaiserslautern, Germany.49 631 205 287849 631 205 3313
We have investigated the requirements for NDJ1 in meiotic telomere redistribution and clustering in synchronized cultures of Saccharomyces cerevisiae. On induction of wild-type meiosis, telomeres disperse from premeiotic aggregates over the nuclear periphery, and then cluster near the spindle pole body (bouquet arrangement) before dispersing again. In ndj1
meiocytes, telomeres are scattered throughout the nucleus and fail to form perinuclear meiosis-specific distribution patterns, suggesting that Ndj1p may function to tether meiotic telomeres to the nuclear periphery. Since ndj1
meiocytes fail to cluster their telomeres at any prophase stage, Ndj1p is the first protein shown to be required for bouquet formation in a synaptic organism. Analysis of homologue pairing by two-color fluorescence in situ hybridization with cosmid probes to regions on III, IX, and XI revealed that disruption of bouquet formation is associated with a significant delay (>2 h) of homologue pairing. An increased and persistent fraction of ndj1
meiocytes with Zip1p polycomplexes suggests that chromosome polarization is important for synapsis progression. Thus, our observations support the hypothesis that meiotic telomere clustering contributes to efficient homologue alignment and synaptic pairing. Under naturally occurring conditions, bouquet formation may allow for rapid sporulation and confer a selective advantage.
Key Words: bouquet fluorescence in situ hybridization ndj1 chromosome pairing meiosis telomeres
© 2000 The Rockefeller University Press
Abbreviations used in this paper: cos, cosmid; FISH, fluorescence in situ hybridization; HA, hemagglutinin; IF, immunofluorescence; SPB, spindle pole body.

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-
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-
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-
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-
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-
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-
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-
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-
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-
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-
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-
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-
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