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Telomeres cluster de novo before the initiation of synapsis: a three-dimensional spatial analysis of telomere positions before and during meiotic prophase.

Bass HW, Marshall WF, Sedat JW, Agard DA, Cande WZ - J. Cell Biol. (1997)

Bottom Line: We found that nuclei at the last somatic prophase before meiosis exhibit a nonrandom, polarized chromosome organization resulting in a loose grouping of telomeres.The stage-dependent changes in telomere arrangements are suggestive of specific, active telomere-associated motility processes with meiotic functions.Thus, the formation of the cluster itself is an early event in the nuclear reorganizations associated with meiosis and may reflect a control point in the initiation of synapsis or crossing over.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular and Cell Biology, University of California at Berkeley 94720, USA.

ABSTRACT
We have analyzed the progressive changes in the spatial distribution of telomeres during meiosis using three-dimensional, high resolution fluorescence microscopy. Fixed meiotic cells of maize (Zea mays L.) were subjected to in situ hybridization under conditions that preserved chromosome structure, allowing identification of stage-dependent changes in telomere arrangements. We found that nuclei at the last somatic prophase before meiosis exhibit a nonrandom, polarized chromosome organization resulting in a loose grouping of telomeres. Quantitative measurements on the spatial arrangements of telomeres revealed that, as cells passed through premeiotic interphase and into leptotene, there was an increase in the frequency of large telomere-to-telomere distances and a decrease in the bias toward peripheral localization of telomeres. By leptotene, there was no obvious evidence of telomere grouping, and the large, singular nucleolus was internally located, nearly concentric with the nucleus. At the end of leptotene, telomeres clustered de novo at the nuclear periphery, coincident with a displacement of the nucleolus to one side. The telomere cluster persisted throughout zygotene and into early pachytene. The nucleolus was adjacent to the cluster at zygotene. At the pachytene stage, telomeres rearranged again by dispersing throughout the nuclear periphery. The stage-dependent changes in telomere arrangements are suggestive of specific, active telomere-associated motility processes with meiotic functions. Thus, the formation of the cluster itself is an early event in the nuclear reorganizations associated with meiosis and may reflect a control point in the initiation of synapsis or crossing over.

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Diagram of the timing of meiotic telomere clustering. A  summary of the fine scale timing of events associated with the onset of synapsis is presented based on the observations from this  work and from Dawe et al. (1994). Leptotene telomeres (legend  at right) are shown as either NOR-associated (open circles) or  non-NOR (closed circles, representing the other 38 of 40 maize  telomeres) are scattered throughout the chromatin, and the nucleolus is fully internal and approximately concentric with the nucleus. The first signs of telomere rearrangements give rise to the  “early bouquet” (see text). The early bouquet nucleus (as in Fig.  5, A and B) is first seen at the end of leptotene, just preceding  prezygotene. Next, prezygotene occurs, comprising the major  transition between leptotene and zygotene as described (12). By  zygotene, all of the telomeres are at the cluster site resulting in  the eccentric nucleolus showing an obligatory colocalization with  the telomere cluster (as in Fig. 5, C and D). At pachytene the  telomere bouquet disperses and the paired homologous telomeres remain at the nuclear periphery.
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Figure 9: Diagram of the timing of meiotic telomere clustering. A summary of the fine scale timing of events associated with the onset of synapsis is presented based on the observations from this work and from Dawe et al. (1994). Leptotene telomeres (legend at right) are shown as either NOR-associated (open circles) or non-NOR (closed circles, representing the other 38 of 40 maize telomeres) are scattered throughout the chromatin, and the nucleolus is fully internal and approximately concentric with the nucleus. The first signs of telomere rearrangements give rise to the “early bouquet” (see text). The early bouquet nucleus (as in Fig. 5, A and B) is first seen at the end of leptotene, just preceding prezygotene. Next, prezygotene occurs, comprising the major transition between leptotene and zygotene as described (12). By zygotene, all of the telomeres are at the cluster site resulting in the eccentric nucleolus showing an obligatory colocalization with the telomere cluster (as in Fig. 5, C and D). At pachytene the telomere bouquet disperses and the paired homologous telomeres remain at the nuclear periphery.

Mentions: We have illustrated our results in Fig. 9 to summarize the temporal relationship between the bouquet stage, defined by the bouquet structure, and the canonical early stages of meiotic prophase, leptotene, zygotene, and pachytene. The initial telomere clustering is shown to occur at the end of leptotene just preceding prezygotene. The “early bouquet” nuclei are the first to exhibit telomere clustering where all but the NOR-linked telomeres have reached the cluster site. The NOR in maize is located near the end of the short arm of chromosome 6. The spatial separation of the NOR from the telomere cluster site may reflect a slower rate at which the NOR-linked telomeres can move to the cluster site. Alternatively, the nucleolus may be positioned in these early bouquet nuclei by a telomere-independent mechanism that overrides the telomere clustering mechanism (28). Prezygotene is then followed by zygotene, during which the most commonly encountered bouquet arrangement was observed (indicated by “bouquet,” Fig. 9, above zygotene). The dispersal of telomeres during pachytene is indicated by the predominantly peripheral localization of telomeres near the nuclear envelope (nucleus diagrammed above “pachytene,” Fig. 9). This summary illustrates that the de novo formation of the telomere cluster is among the very first steps in nuclear changes associated with synapsis.


Telomeres cluster de novo before the initiation of synapsis: a three-dimensional spatial analysis of telomere positions before and during meiotic prophase.

Bass HW, Marshall WF, Sedat JW, Agard DA, Cande WZ - J. Cell Biol. (1997)

Diagram of the timing of meiotic telomere clustering. A  summary of the fine scale timing of events associated with the onset of synapsis is presented based on the observations from this  work and from Dawe et al. (1994). Leptotene telomeres (legend  at right) are shown as either NOR-associated (open circles) or  non-NOR (closed circles, representing the other 38 of 40 maize  telomeres) are scattered throughout the chromatin, and the nucleolus is fully internal and approximately concentric with the nucleus. The first signs of telomere rearrangements give rise to the  “early bouquet” (see text). The early bouquet nucleus (as in Fig.  5, A and B) is first seen at the end of leptotene, just preceding  prezygotene. Next, prezygotene occurs, comprising the major  transition between leptotene and zygotene as described (12). By  zygotene, all of the telomeres are at the cluster site resulting in  the eccentric nucleolus showing an obligatory colocalization with  the telomere cluster (as in Fig. 5, C and D). At pachytene the  telomere bouquet disperses and the paired homologous telomeres remain at the nuclear periphery.
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Related In: Results  -  Collection

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Figure 9: Diagram of the timing of meiotic telomere clustering. A summary of the fine scale timing of events associated with the onset of synapsis is presented based on the observations from this work and from Dawe et al. (1994). Leptotene telomeres (legend at right) are shown as either NOR-associated (open circles) or non-NOR (closed circles, representing the other 38 of 40 maize telomeres) are scattered throughout the chromatin, and the nucleolus is fully internal and approximately concentric with the nucleus. The first signs of telomere rearrangements give rise to the “early bouquet” (see text). The early bouquet nucleus (as in Fig. 5, A and B) is first seen at the end of leptotene, just preceding prezygotene. Next, prezygotene occurs, comprising the major transition between leptotene and zygotene as described (12). By zygotene, all of the telomeres are at the cluster site resulting in the eccentric nucleolus showing an obligatory colocalization with the telomere cluster (as in Fig. 5, C and D). At pachytene the telomere bouquet disperses and the paired homologous telomeres remain at the nuclear periphery.
Mentions: We have illustrated our results in Fig. 9 to summarize the temporal relationship between the bouquet stage, defined by the bouquet structure, and the canonical early stages of meiotic prophase, leptotene, zygotene, and pachytene. The initial telomere clustering is shown to occur at the end of leptotene just preceding prezygotene. The “early bouquet” nuclei are the first to exhibit telomere clustering where all but the NOR-linked telomeres have reached the cluster site. The NOR in maize is located near the end of the short arm of chromosome 6. The spatial separation of the NOR from the telomere cluster site may reflect a slower rate at which the NOR-linked telomeres can move to the cluster site. Alternatively, the nucleolus may be positioned in these early bouquet nuclei by a telomere-independent mechanism that overrides the telomere clustering mechanism (28). Prezygotene is then followed by zygotene, during which the most commonly encountered bouquet arrangement was observed (indicated by “bouquet,” Fig. 9, above zygotene). The dispersal of telomeres during pachytene is indicated by the predominantly peripheral localization of telomeres near the nuclear envelope (nucleus diagrammed above “pachytene,” Fig. 9). This summary illustrates that the de novo formation of the telomere cluster is among the very first steps in nuclear changes associated with synapsis.

Bottom Line: We found that nuclei at the last somatic prophase before meiosis exhibit a nonrandom, polarized chromosome organization resulting in a loose grouping of telomeres.The stage-dependent changes in telomere arrangements are suggestive of specific, active telomere-associated motility processes with meiotic functions.Thus, the formation of the cluster itself is an early event in the nuclear reorganizations associated with meiosis and may reflect a control point in the initiation of synapsis or crossing over.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular and Cell Biology, University of California at Berkeley 94720, USA.

ABSTRACT
We have analyzed the progressive changes in the spatial distribution of telomeres during meiosis using three-dimensional, high resolution fluorescence microscopy. Fixed meiotic cells of maize (Zea mays L.) were subjected to in situ hybridization under conditions that preserved chromosome structure, allowing identification of stage-dependent changes in telomere arrangements. We found that nuclei at the last somatic prophase before meiosis exhibit a nonrandom, polarized chromosome organization resulting in a loose grouping of telomeres. Quantitative measurements on the spatial arrangements of telomeres revealed that, as cells passed through premeiotic interphase and into leptotene, there was an increase in the frequency of large telomere-to-telomere distances and a decrease in the bias toward peripheral localization of telomeres. By leptotene, there was no obvious evidence of telomere grouping, and the large, singular nucleolus was internally located, nearly concentric with the nucleus. At the end of leptotene, telomeres clustered de novo at the nuclear periphery, coincident with a displacement of the nucleolus to one side. The telomere cluster persisted throughout zygotene and into early pachytene. The nucleolus was adjacent to the cluster at zygotene. At the pachytene stage, telomeres rearranged again by dispersing throughout the nuclear periphery. The stage-dependent changes in telomere arrangements are suggestive of specific, active telomere-associated motility processes with meiotic functions. Thus, the formation of the cluster itself is an early event in the nuclear reorganizations associated with meiosis and may reflect a control point in the initiation of synapsis or crossing over.

Show MeSH