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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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FISH analysis of homologue pairing during meiotic time courses of wild-type and ndj1Δ SK1 strains. Cosmid probe combinations m/p and f/l were hybridized to spread preparations obtained at the respective time points (minutes). Pairing values were obtained by determining the fraction of nuclei containing cosmid signals of the same color that touched each other or showed an enlarged coalesced signal. More than 200 FISH signal pairs were scored per time point, probe combination, and strain. Values were corrected for accidental heterologous contacts by subtracting 5% for cosmid combination m/p and 4% for probe combination l/f (see text). (A) Frequencies of nuclei with paired cos f signals (XI internal; Fig. 1) in wild-type (WT) and ndj1Δ (ndj1) time courses. (B) Frequencies (%) of paired cos l (XI, right telo) in wild-type and ndj1Δ time courses. (D) Frequencies of nuclei with paired cos p signals (IX, right arm) in wild-type and ndj1Δ time courses. (C) Frequencies of nuclei with paired cos m signals (III, HML) in wild-type and ndj1Δ time course. At all loci probed, the frequencies of nuclei with paired signals increase more gradually in the absence of Ndj1p, reaching nearly wild-type frequencies with a 2–3-h delay. In the wild type, signal patterns are displayed only until 320 min, since meiotic divisions (anaphases) appeared after 300 min and complicated the signal analysis.
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Figure 11: FISH analysis of homologue pairing during meiotic time courses of wild-type and ndj1Δ SK1 strains. Cosmid probe combinations m/p and f/l were hybridized to spread preparations obtained at the respective time points (minutes). Pairing values were obtained by determining the fraction of nuclei containing cosmid signals of the same color that touched each other or showed an enlarged coalesced signal. More than 200 FISH signal pairs were scored per time point, probe combination, and strain. Values were corrected for accidental heterologous contacts by subtracting 5% for cosmid combination m/p and 4% for probe combination l/f (see text). (A) Frequencies of nuclei with paired cos f signals (XI internal; Fig. 1) in wild-type (WT) and ndj1Δ (ndj1) time courses. (B) Frequencies (%) of paired cos l (XI, right telo) in wild-type and ndj1Δ time courses. (D) Frequencies of nuclei with paired cos p signals (IX, right arm) in wild-type and ndj1Δ time courses. (C) Frequencies of nuclei with paired cos m signals (III, HML) in wild-type and ndj1Δ time course. At all loci probed, the frequencies of nuclei with paired signals increase more gradually in the absence of Ndj1p, reaching nearly wild-type frequencies with a 2–3-h delay. In the wild type, signal patterns are displayed only until 320 min, since meiotic divisions (anaphases) appeared after 300 min and complicated the signal analysis.

Mentions: In wild-type and ndj1Δ time courses, the fraction of nucleoids with FISH signals homologously paired increased well above premeiotic values (Fig. 11). In ndj1Δ meiosis, all homologous regions investigated reached nearly wild-type levels of homologous signal pairing, but with a 2–3-h delay (Fig. 11). This slowed progression of homologous pairing is mirrored by a 2-h delay in the appearance of anaphases I and II in ndj1Δ meiosis as compared with the wild type, where these first appeared at 300 and 320 min, respectively (not shown, consistent with earlier reports). In wild-type meiosis, the homologous region near the left telomere of the small chromosomes III paired most rapidly (Table ). However, in the absence of Ndj1p and bouquet formation, the telomeric region of chromosomes III showed the most prominent retardation of homologous pairing, expressed as the difference in time required in wild-type and ndj1Δ meiosis to reach peak values in signal pairing (Δt = 160 min, Fig. 11). Pairing of the telomeric region of the right arm of the large chromosomes XI (cos l), in contrast, showed only a delay of 100 min in ndj1Δ meiosis. Pairing of large chromosomes may thus be less dependent on a catalytic action of telomere clustering on homologue pairing, since these may span the entire nucleus and therefore have a higher probability for chance encounters with their homologues in the absence of bouquet formation.


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 homologue pairing during meiotic time courses of wild-type and ndj1Δ SK1 strains. Cosmid probe combinations m/p and f/l were hybridized to spread preparations obtained at the respective time points (minutes). Pairing values were obtained by determining the fraction of nuclei containing cosmid signals of the same color that touched each other or showed an enlarged coalesced signal. More than 200 FISH signal pairs were scored per time point, probe combination, and strain. Values were corrected for accidental heterologous contacts by subtracting 5% for cosmid combination m/p and 4% for probe combination l/f (see text). (A) Frequencies of nuclei with paired cos f signals (XI internal; Fig. 1) in wild-type (WT) and ndj1Δ (ndj1) time courses. (B) Frequencies (%) of paired cos l (XI, right telo) in wild-type and ndj1Δ time courses. (D) Frequencies of nuclei with paired cos p signals (IX, right arm) in wild-type and ndj1Δ time courses. (C) Frequencies of nuclei with paired cos m signals (III, HML) in wild-type and ndj1Δ time course. At all loci probed, the frequencies of nuclei with paired signals increase more gradually in the absence of Ndj1p, reaching nearly wild-type frequencies with a 2–3-h delay. In the wild type, signal patterns are displayed only until 320 min, since meiotic divisions (anaphases) appeared after 300 min and complicated the signal analysis.
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Related In: Results  -  Collection

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Figure 11: FISH analysis of homologue pairing during meiotic time courses of wild-type and ndj1Δ SK1 strains. Cosmid probe combinations m/p and f/l were hybridized to spread preparations obtained at the respective time points (minutes). Pairing values were obtained by determining the fraction of nuclei containing cosmid signals of the same color that touched each other or showed an enlarged coalesced signal. More than 200 FISH signal pairs were scored per time point, probe combination, and strain. Values were corrected for accidental heterologous contacts by subtracting 5% for cosmid combination m/p and 4% for probe combination l/f (see text). (A) Frequencies of nuclei with paired cos f signals (XI internal; Fig. 1) in wild-type (WT) and ndj1Δ (ndj1) time courses. (B) Frequencies (%) of paired cos l (XI, right telo) in wild-type and ndj1Δ time courses. (D) Frequencies of nuclei with paired cos p signals (IX, right arm) in wild-type and ndj1Δ time courses. (C) Frequencies of nuclei with paired cos m signals (III, HML) in wild-type and ndj1Δ time course. At all loci probed, the frequencies of nuclei with paired signals increase more gradually in the absence of Ndj1p, reaching nearly wild-type frequencies with a 2–3-h delay. In the wild type, signal patterns are displayed only until 320 min, since meiotic divisions (anaphases) appeared after 300 min and complicated the signal analysis.
Mentions: In wild-type and ndj1Δ time courses, the fraction of nucleoids with FISH signals homologously paired increased well above premeiotic values (Fig. 11). In ndj1Δ meiosis, all homologous regions investigated reached nearly wild-type levels of homologous signal pairing, but with a 2–3-h delay (Fig. 11). This slowed progression of homologous pairing is mirrored by a 2-h delay in the appearance of anaphases I and II in ndj1Δ meiosis as compared with the wild type, where these first appeared at 300 and 320 min, respectively (not shown, consistent with earlier reports). In wild-type meiosis, the homologous region near the left telomere of the small chromosomes III paired most rapidly (Table ). However, in the absence of Ndj1p and bouquet formation, the telomeric region of chromosomes III showed the most prominent retardation of homologous pairing, expressed as the difference in time required in wild-type and ndj1Δ meiosis to reach peak values in signal pairing (Δt = 160 min, Fig. 11). Pairing of the telomeric region of the right arm of the large chromosomes XI (cos l), in contrast, showed only a delay of 100 min in ndj1Δ meiosis. Pairing of large chromosomes may thus be less dependent on a catalytic action of telomere clustering on homologue pairing, since these may span the entire nucleus and therefore have a higher probability for chance encounters with their homologues in the absence of bouquet formation.

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