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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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Costaining of telomeres by FISH (rhodamine, red) and Zip1p by IF (FITC, green) in mildly spread ndj1Δ meiocyte nuclei (DAPI, blue). (a and b) Spread nuclei (obtained at 210 min after induction of meiosis) display Zip1-signal stretches and a Zip1 polycomplex (bright green oblong, arrow), while telomere FISH signals are dispersed. (c) Nucleus with dispersed telomeres but without Zip1 polycomplex from a later time point (330 min). Bar, 5 μm.
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Figure 9: Costaining of telomeres by FISH (rhodamine, red) and Zip1p by IF (FITC, green) in mildly spread ndj1Δ meiocyte nuclei (DAPI, blue). (a and b) Spread nuclei (obtained at 210 min after induction of meiosis) display Zip1-signal stretches and a Zip1 polycomplex (bright green oblong, arrow), while telomere FISH signals are dispersed. (c) Nucleus with dispersed telomeres but without Zip1 polycomplex from a later time point (330 min). Bar, 5 μm.

Mentions: Since formation of a true bouquet involves telomere clustering at the SPB during the leptotene/zygotene transition stage (Trelles-Sticken et al. 1999), we determined whether SPB/telomere cluster association is absent in ndj1Δ meiocytes. To this end, we simultaneously immunostained for spindle pole body and telomeres by FISH in intact nuclei at 240 min in wild-type and mutant meiosis. We failed to detect a physical association of the SPB signal and XY′ telomeric signal accumulations seen in a few ndj1Δ nuclei (not shown). This and the constant and negligible frequency of nuclei with a single telomere-FISH signal cluster over mutant time courses corroborates that bouquet formation is impaired in ndj1Δ meiosis. To further investigate whether telomere clustering is defective during the leptotene/zygotene transition stage, we immunostained spread meiocytes with antibodies to Zip1p, a component of transverse filaments of the synaptonemal complex (Sym et al. 1993) and determined the telomere distribution by FISH in SK1 meiocytes, obtained at t = 200 min with an incomplete speckled Zip1p distribution, which represent nuclei with synapsis in progress. It was found that telomere signals were scattered throughout mildly spread ndj1Δ nuclei (n = 168; obtained at 300 min) with a fragmented Zip1p distribution (zygotene-equivalent stage; Fig. 9, a–c), while in the wild type 20% of zygotene cells (n = 166) contained a single telomere cluster (see also Trelles-Sticken et al. 1999). These data suggest that true bouquet formation is disrupted in ndj1Δ meiosis.


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)

Costaining of telomeres by FISH (rhodamine, red) and Zip1p by IF (FITC, green) in mildly spread ndj1Δ meiocyte nuclei (DAPI, blue). (a and b) Spread nuclei (obtained at 210 min after induction of meiosis) display Zip1-signal stretches and a Zip1 polycomplex (bright green oblong, arrow), while telomere FISH signals are dispersed. (c) Nucleus with dispersed telomeres but without Zip1 polycomplex from a later time point (330 min). Bar, 5 μm.
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Related In: Results  -  Collection

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Figure 9: Costaining of telomeres by FISH (rhodamine, red) and Zip1p by IF (FITC, green) in mildly spread ndj1Δ meiocyte nuclei (DAPI, blue). (a and b) Spread nuclei (obtained at 210 min after induction of meiosis) display Zip1-signal stretches and a Zip1 polycomplex (bright green oblong, arrow), while telomere FISH signals are dispersed. (c) Nucleus with dispersed telomeres but without Zip1 polycomplex from a later time point (330 min). Bar, 5 μm.
Mentions: Since formation of a true bouquet involves telomere clustering at the SPB during the leptotene/zygotene transition stage (Trelles-Sticken et al. 1999), we determined whether SPB/telomere cluster association is absent in ndj1Δ meiocytes. To this end, we simultaneously immunostained for spindle pole body and telomeres by FISH in intact nuclei at 240 min in wild-type and mutant meiosis. We failed to detect a physical association of the SPB signal and XY′ telomeric signal accumulations seen in a few ndj1Δ nuclei (not shown). This and the constant and negligible frequency of nuclei with a single telomere-FISH signal cluster over mutant time courses corroborates that bouquet formation is impaired in ndj1Δ meiosis. To further investigate whether telomere clustering is defective during the leptotene/zygotene transition stage, we immunostained spread meiocytes with antibodies to Zip1p, a component of transverse filaments of the synaptonemal complex (Sym et al. 1993) and determined the telomere distribution by FISH in SK1 meiocytes, obtained at t = 200 min with an incomplete speckled Zip1p distribution, which represent nuclei with synapsis in progress. It was found that telomere signals were scattered throughout mildly spread ndj1Δ nuclei (n = 168; obtained at 300 min) with a fragmented Zip1p distribution (zygotene-equivalent stage; Fig. 9, a–c), while in the wild type 20% of zygotene cells (n = 166) contained a single telomere cluster (see also Trelles-Sticken et al. 1999). These data suggest that true bouquet formation is disrupted in ndj1Δ meiosis.

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