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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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Scheme showing the sequential steps of centromere and telomere redistribution that occur during earliest meiotic prophase of yeast. It is based on the observations made in this and earlier reports (see text). (a) In the premeiotic nucleus, telomeres (black) and centromeres (gray) form several telomere and one centromere cluster at the nuclear periphery. (b) In the wild type, induction of meiosis leads to dissolution of the centromere cluster and perinuclear telomere clusters. Centromeres become dispersed throughout the nuclear lumen, while telomeres disperse over the nuclear periphery. (c) Bouquet stage: telomeres tightly cluster at the spindle pole body, while centromeres are dispersed. (d) While premeiotic telomere topology is not affected, the early steps of meiotic telomere redistribution appear defective in the absence of Ndj1p, which leads to scattering of both telomeres and centromeres throughout the ndj1Δ meiocyte nucleus.
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Figure 14: Scheme showing the sequential steps of centromere and telomere redistribution that occur during earliest meiotic prophase of yeast. It is based on the observations made in this and earlier reports (see text). (a) In the premeiotic nucleus, telomeres (black) and centromeres (gray) form several telomere and one centromere cluster at the nuclear periphery. (b) In the wild type, induction of meiosis leads to dissolution of the centromere cluster and perinuclear telomere clusters. Centromeres become dispersed throughout the nuclear lumen, while telomeres disperse over the nuclear periphery. (c) Bouquet stage: telomeres tightly cluster at the spindle pole body, while centromeres are dispersed. (d) While premeiotic telomere topology is not affected, the early steps of meiotic telomere redistribution appear defective in the absence of Ndj1p, which leads to scattering of both telomeres and centromeres throughout the ndj1Δ meiocyte nucleus.

Mentions: Two of the early steps in the meiotic nuclear reorganization, dispersion of centromeres and telomeres, apparently are unaffected by deletion of NDJ1. However, this close proximity of dispersed telomeres to the nuclear periphery, which is evident in wild-type cells (Hayashi et al. 1998, and this report) does appear defective in ndj1Δ. During earliest meiotic prophase, telomeres dissociate from the vegetative aggregates and line the nuclear periphery (Fig. 14), giving raise to a rim-like staining in ∼20% of wild-type nuclei, which resembles the telomere distribution seen in the late preleptotene/leptotene stage of mammalian prophase I (Scherthan et al. 1996). In mammals, the switch from premeiotic to meiotic telomere distribution is a two-step process, with telomeres first attaching at scattered points over the nuclear envelope, and then congregating in the bouquet to a limited sector of the nuclear envelope (Rasmussen and Holm 1978; Boiko 1983; Scherthan et al. 1996). In ndj1Δ meiosis of yeast, FISH and IF analyses of telomere distribution in undisrupted and mildly spread nuclei revealed a paucity of nuclei with telomeres lining the nuclear periphery and a concomitant increase in the frequency of nuclei with telomeres scattered throughout the nuclear lumen, as inferred from three-dimensional Rap1p analysis. These observations indicate that the absence of Ndj1p impairs the assembly of a meiosis-specific perinuclear telomere topology (Fig. 14) after dissolution of the few vegetative telomere clusters (see Gilson et al. 1993). Furthermore, these observations indicate that localization of telomeres to the nuclear periphery requires Ndj1p, in accord with speculation based on an earlier genetic analysis of NDJ1/TAM1-deficient cells (Chua and Roeder 1997). Localization of the ends of yeast synaptonemal complexes to the nuclear envelope has been demonstrated by electron microscopy (Byers and Goetsch 1975; Zickler and Olson 1975; Moens and Ashton 1985) and a similar analysis of ndj1Δ is underway (Z. Zhang, M.N. Conrad, and M.E. Dresser).


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)

Scheme showing the sequential steps of centromere and telomere redistribution that occur during earliest meiotic prophase of yeast. It is based on the observations made in this and earlier reports (see text). (a) In the premeiotic nucleus, telomeres (black) and centromeres (gray) form several telomere and one centromere cluster at the nuclear periphery. (b) In the wild type, induction of meiosis leads to dissolution of the centromere cluster and perinuclear telomere clusters. Centromeres become dispersed throughout the nuclear lumen, while telomeres disperse over the nuclear periphery. (c) Bouquet stage: telomeres tightly cluster at the spindle pole body, while centromeres are dispersed. (d) While premeiotic telomere topology is not affected, the early steps of meiotic telomere redistribution appear defective in the absence of Ndj1p, which leads to scattering of both telomeres and centromeres throughout the ndj1Δ meiocyte nucleus.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 14: Scheme showing the sequential steps of centromere and telomere redistribution that occur during earliest meiotic prophase of yeast. It is based on the observations made in this and earlier reports (see text). (a) In the premeiotic nucleus, telomeres (black) and centromeres (gray) form several telomere and one centromere cluster at the nuclear periphery. (b) In the wild type, induction of meiosis leads to dissolution of the centromere cluster and perinuclear telomere clusters. Centromeres become dispersed throughout the nuclear lumen, while telomeres disperse over the nuclear periphery. (c) Bouquet stage: telomeres tightly cluster at the spindle pole body, while centromeres are dispersed. (d) While premeiotic telomere topology is not affected, the early steps of meiotic telomere redistribution appear defective in the absence of Ndj1p, which leads to scattering of both telomeres and centromeres throughout the ndj1Δ meiocyte nucleus.
Mentions: Two of the early steps in the meiotic nuclear reorganization, dispersion of centromeres and telomeres, apparently are unaffected by deletion of NDJ1. However, this close proximity of dispersed telomeres to the nuclear periphery, which is evident in wild-type cells (Hayashi et al. 1998, and this report) does appear defective in ndj1Δ. During earliest meiotic prophase, telomeres dissociate from the vegetative aggregates and line the nuclear periphery (Fig. 14), giving raise to a rim-like staining in ∼20% of wild-type nuclei, which resembles the telomere distribution seen in the late preleptotene/leptotene stage of mammalian prophase I (Scherthan et al. 1996). In mammals, the switch from premeiotic to meiotic telomere distribution is a two-step process, with telomeres first attaching at scattered points over the nuclear envelope, and then congregating in the bouquet to a limited sector of the nuclear envelope (Rasmussen and Holm 1978; Boiko 1983; Scherthan et al. 1996). In ndj1Δ meiosis of yeast, FISH and IF analyses of telomere distribution in undisrupted and mildly spread nuclei revealed a paucity of nuclei with telomeres lining the nuclear periphery and a concomitant increase in the frequency of nuclei with telomeres scattered throughout the nuclear lumen, as inferred from three-dimensional Rap1p analysis. These observations indicate that the absence of Ndj1p impairs the assembly of a meiosis-specific perinuclear telomere topology (Fig. 14) after dissolution of the few vegetative telomere clusters (see Gilson et al. 1993). Furthermore, these observations indicate that localization of telomeres to the nuclear periphery requires Ndj1p, in accord with speculation based on an earlier genetic analysis of NDJ1/TAM1-deficient cells (Chua and Roeder 1997). Localization of the ends of yeast synaptonemal complexes to the nuclear envelope has been demonstrated by electron microscopy (Byers and Goetsch 1975; Zickler and Olson 1975; Moens and Ashton 1985) and a similar analysis of ndj1Δ is underway (Z. Zhang, M.N. Conrad, and M.E. Dresser).

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