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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

Analysis of occurrence of meiosis-specific telomere distribution patterns during meiotic time courses (minutes) of wild-type (solid symbols) and ndj1Δ (open symbols, dotted lines) SK1 strains. Frequency of diploid nuclei (%) with telomeric FISH signals showing a rim-like distribution along the nuclear periphery (telos rim-like; Fig. 4 e) and of bouquet nuclei with a telomere cluster (bouquet; Fig. 4f and Fig. g). The frequency of nuclei with rim-like telomere distribution and with a bouquet arrangement is significantly reduced in ndj1Δ meiosis. Wild-type signal patterns are displayed until 360 min only, since meiotic divisions (anaphases) appeared after 300 min in the wild-type culture and complicated the signal analysis.
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Figure 5: Analysis of occurrence of meiosis-specific telomere distribution patterns during meiotic time courses (minutes) of wild-type (solid symbols) and ndj1Δ (open symbols, dotted lines) SK1 strains. Frequency of diploid nuclei (%) with telomeric FISH signals showing a rim-like distribution along the nuclear periphery (telos rim-like; Fig. 4 e) and of bouquet nuclei with a telomere cluster (bouquet; Fig. 4f and Fig. g). The frequency of nuclei with rim-like telomere distribution and with a bouquet arrangement is significantly reduced in ndj1Δ meiosis. Wild-type signal patterns are displayed until 360 min only, since meiotic divisions (anaphases) appeared after 300 min in the wild-type culture and complicated the signal analysis.

Mentions: Nuclei with a rim-like peripheral telomere signal distribution (Fig. 4 a) are rarely encountered at the induction of sporulation, but increase early after induction of meiosis in the wild type (Fig. 5). In contrast, the frequency of spread ndj1Δ meiocytes with such a preleptotene-like perinuclear telomere distribution (see Scherthan et al. 1996) essentially remained at a vegetative background level during sporulation, well below the level seen in the wild type (Fig. 5). Similar observations were obtained in time courses of undisrupted ndj1Δ nuclei (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 occurrence of meiosis-specific telomere distribution patterns during meiotic time courses (minutes) of wild-type (solid symbols) and ndj1Δ (open symbols, dotted lines) SK1 strains. Frequency of diploid nuclei (%) with telomeric FISH signals showing a rim-like distribution along the nuclear periphery (telos rim-like; Fig. 4 e) and of bouquet nuclei with a telomere cluster (bouquet; Fig. 4f and Fig. g). The frequency of nuclei with rim-like telomere distribution and with a bouquet arrangement is significantly reduced in ndj1Δ meiosis. Wild-type signal patterns are displayed until 360 min only, since meiotic divisions (anaphases) appeared after 300 min in the wild-type culture and complicated the signal analysis.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 5: Analysis of occurrence of meiosis-specific telomere distribution patterns during meiotic time courses (minutes) of wild-type (solid symbols) and ndj1Δ (open symbols, dotted lines) SK1 strains. Frequency of diploid nuclei (%) with telomeric FISH signals showing a rim-like distribution along the nuclear periphery (telos rim-like; Fig. 4 e) and of bouquet nuclei with a telomere cluster (bouquet; Fig. 4f and Fig. g). The frequency of nuclei with rim-like telomere distribution and with a bouquet arrangement is significantly reduced in ndj1Δ meiosis. Wild-type signal patterns are displayed until 360 min only, since meiotic divisions (anaphases) appeared after 300 min in the wild-type culture and complicated the signal analysis.
Mentions: Nuclei with a rim-like peripheral telomere signal distribution (Fig. 4 a) are rarely encountered at the induction of sporulation, but increase early after induction of meiosis in the wild type (Fig. 5). In contrast, the frequency of spread ndj1Δ meiocytes with such a preleptotene-like perinuclear telomere distribution (see Scherthan et al. 1996) essentially remained at a vegetative background level during sporulation, well below the level seen in the wild type (Fig. 5). Similar observations were obtained in time courses of undisrupted ndj1Δ nuclei (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