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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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Related in: MedlinePlus

FISH analysis of the frequencies of vegetative/premeiotic centromere and telomere distribution patterns; i.e., one centromere cluster (cen cluster) and two to eight telomere clusters (two to eight telo signals) (Fig. 2, a and b), in spread ndj1Δ and wild-type SK1 nuclei at transfer to sporulation medium (0 min) and subsequent time points (minutes) in sporulation. The frequency (%) of nuclei with this hallmark of vegetative/premeiotic nuclear architecture drops similarly in ndj1Δ (ndj1) and wild-type (WT) meiotic time courses. Since meiotic divisions appeared at t = 300 min in the wild-type culture and complicated analysis, FISH analysis in the wild type was only conducted until 320 min.
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Figure 3: FISH analysis of the frequencies of vegetative/premeiotic centromere and telomere distribution patterns; i.e., one centromere cluster (cen cluster) and two to eight telomere clusters (two to eight telo signals) (Fig. 2, a and b), in spread ndj1Δ and wild-type SK1 nuclei at transfer to sporulation medium (0 min) and subsequent time points (minutes) in sporulation. The frequency (%) of nuclei with this hallmark of vegetative/premeiotic nuclear architecture drops similarly in ndj1Δ (ndj1) and wild-type (WT) meiotic time courses. Since meiotic divisions appeared at t = 300 min in the wild-type culture and complicated analysis, FISH analysis in the wild type was only conducted until 320 min.

Mentions: It has been shown that the nuclear organization of vegetative/premeiotic yeast cells is dominated by centromere clustering at the SPB (Fig. 2, a and b), which resolves during the onset of meiotic prophase (Fig. 2c and Fig. d) (Hayashi et al. 1998; Jin et al. 1998). When we determined centromere distribution by FISH to nuclei of SK1 strains, it was found that the frequency of nuclei with one centromere cluster diminished at similar rates after induction of meiosis, both in wild-type and in ndj1Δ meiotic time courses (Fig. 3, and not shown). This suggests that dissolution of the centromere cluster is not affected by the absence of Ndj1p.


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)

FISH analysis of the frequencies of vegetative/premeiotic centromere and telomere distribution patterns; i.e., one centromere cluster (cen cluster) and two to eight telomere clusters (two to eight telo signals) (Fig. 2, a and b), in spread ndj1Δ and wild-type SK1 nuclei at transfer to sporulation medium (0 min) and subsequent time points (minutes) in sporulation. The frequency (%) of nuclei with this hallmark of vegetative/premeiotic nuclear architecture drops similarly in ndj1Δ (ndj1) and wild-type (WT) meiotic time courses. Since meiotic divisions appeared at t = 300 min in the wild-type culture and complicated analysis, FISH analysis in the wild type was only conducted until 320 min.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 3: FISH analysis of the frequencies of vegetative/premeiotic centromere and telomere distribution patterns; i.e., one centromere cluster (cen cluster) and two to eight telomere clusters (two to eight telo signals) (Fig. 2, a and b), in spread ndj1Δ and wild-type SK1 nuclei at transfer to sporulation medium (0 min) and subsequent time points (minutes) in sporulation. The frequency (%) of nuclei with this hallmark of vegetative/premeiotic nuclear architecture drops similarly in ndj1Δ (ndj1) and wild-type (WT) meiotic time courses. Since meiotic divisions appeared at t = 300 min in the wild-type culture and complicated analysis, FISH analysis in the wild type was only conducted until 320 min.
Mentions: It has been shown that the nuclear organization of vegetative/premeiotic yeast cells is dominated by centromere clustering at the SPB (Fig. 2, a and b), which resolves during the onset of meiotic prophase (Fig. 2c and Fig. d) (Hayashi et al. 1998; Jin et al. 1998). When we determined centromere distribution by FISH to nuclei of SK1 strains, it was found that the frequency of nuclei with one centromere cluster diminished at similar rates after induction of meiosis, both in wild-type and in ndj1Δ meiotic time courses (Fig. 3, and not shown). This suggests that dissolution of the centromere cluster is not affected by the absence of Ndj1p.

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