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Meiotic telomere protein Ndj1p is required for meiosis-specific telomere distribution, bouquet formation and efficient homologue pairing.

Trelles-Sticken E, Dresser ME, Scherthan H - J. Cell Biol. (2000)

Bottom Line: Since ndj1Delta 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.Under naturally occurring conditions, bouquet formation may allow for rapid sporulation and confer a selective advantage.

View Article: PubMed Central - PubMed

Affiliation: Department of Human Biology and Genetics, University of Kaiserslautern, D-67653 Kaiserslautern, Germany.

ABSTRACT
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 ndj1Delta 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 ndj1Delta 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 ndj1Delta 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.

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Analysis of telomere FISH signal numbers in 20 randomly selected, mildly spread nuclei of diploid SK1 wild-type and ndj1Δ meiocytes. Nuclei were obtained 200 and 300 min after induction of meiosis in the wild type and ndj1Δ, respectively, to allow for a compensation of the delay in mutant prophase I. Ranking according to increasing numbers of telomere FISH signals/nucleoid reveals that ndj1Δ meiocytes display significantly larger telomere signal numbers/nucleus.
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Figure 8: Analysis of telomere FISH signal numbers in 20 randomly selected, mildly spread nuclei of diploid SK1 wild-type and ndj1Δ meiocytes. Nuclei were obtained 200 and 300 min after induction of meiosis in the wild type and ndj1Δ, respectively, to allow for a compensation of the delay in mutant prophase I. Ranking according to increasing numbers of telomere FISH signals/nucleoid reveals that ndj1Δ meiocytes display significantly larger telomere signal numbers/nucleus.

Mentions: A severe deviation from the wild-type situation was observed in ndj1Δ meiosis. The frequency of nuclei with a single telomere cluster never exceeded premeiotic levels, even in time courses with prolonged duration and in time-course experiments where we performed FISH to intact meiocyte nuclei (Fig. 5, and not shown). The defect in telomere clustering was also evident when telomere FISH signal numbers were compared in 20 randomly selected wild-type and mutant nuclei. Spread ndj1Δ meiocytes (obtained 300 min after induction of meiosis) contained a significantly increased spot number/nucleus as compared with wild-type meiocytes that were sampled at 200 min to compensate for the delay in mutant prophase I (Fig. 8). Similar results were obtained using anti–Rap1p IF and confocal microscopy (data not shown).


Meiotic telomere protein Ndj1p is required for meiosis-specific telomere distribution, bouquet formation and efficient homologue pairing.

Trelles-Sticken E, Dresser ME, Scherthan H - J. Cell Biol. (2000)

Analysis of telomere FISH signal numbers in 20 randomly selected, mildly spread nuclei of diploid SK1 wild-type and ndj1Δ meiocytes. Nuclei were obtained 200 and 300 min after induction of meiosis in the wild type and ndj1Δ, respectively, to allow for a compensation of the delay in mutant prophase I. Ranking according to increasing numbers of telomere FISH signals/nucleoid reveals that ndj1Δ meiocytes display significantly larger telomere signal numbers/nucleus.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2189801&req=5

Figure 8: Analysis of telomere FISH signal numbers in 20 randomly selected, mildly spread nuclei of diploid SK1 wild-type and ndj1Δ meiocytes. Nuclei were obtained 200 and 300 min after induction of meiosis in the wild type and ndj1Δ, respectively, to allow for a compensation of the delay in mutant prophase I. Ranking according to increasing numbers of telomere FISH signals/nucleoid reveals that ndj1Δ meiocytes display significantly larger telomere signal numbers/nucleus.
Mentions: A severe deviation from the wild-type situation was observed in ndj1Δ meiosis. The frequency of nuclei with a single telomere cluster never exceeded premeiotic levels, even in time courses with prolonged duration and in time-course experiments where we performed FISH to intact meiocyte nuclei (Fig. 5, and not shown). The defect in telomere clustering was also evident when telomere FISH signal numbers were compared in 20 randomly selected wild-type and mutant nuclei. Spread ndj1Δ meiocytes (obtained 300 min after induction of meiosis) contained a significantly increased spot number/nucleus as compared with wild-type meiocytes that were sampled at 200 min to compensate for the delay in mutant prophase I (Fig. 8). Similar results were obtained using anti–Rap1p IF and confocal microscopy (data not shown).

Bottom Line: Since ndj1Delta 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.Under naturally occurring conditions, bouquet formation may allow for rapid sporulation and confer a selective advantage.

View Article: PubMed Central - PubMed

Affiliation: Department of Human Biology and Genetics, University of Kaiserslautern, D-67653 Kaiserslautern, Germany.

ABSTRACT
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 ndj1Delta 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 ndj1Delta 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 ndj1Delta 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.

Show MeSH
Related in: MedlinePlus