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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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Telomere distribution at pachytene and diakinesis. Sequential color overlay projections of four nuclei subjected to telomere  FISH are shown for the DAPI (DNA, red) and FITC (telomeres, green) images as described in Fig. 3. (A–C) Examples of pachytene nuclei identified as early pachytene (A), middle pachytene (B), and late pachytene (C) are shown. (D) The bivalents of a diakinesis have  widely separated homologous telomeres (double arrows), reflecting the desynapsis of homologues. In all cases the nucleolus is seen to  be peripherally located, but less common examples of an internal nucleolus at late pachytene and diakinesis have been observed (not  shown).
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Figure 6: Telomere distribution at pachytene and diakinesis. Sequential color overlay projections of four nuclei subjected to telomere FISH are shown for the DAPI (DNA, red) and FITC (telomeres, green) images as described in Fig. 3. (A–C) Examples of pachytene nuclei identified as early pachytene (A), middle pachytene (B), and late pachytene (C) are shown. (D) The bivalents of a diakinesis have widely separated homologous telomeres (double arrows), reflecting the desynapsis of homologues. In all cases the nucleolus is seen to be peripherally located, but less common examples of an internal nucleolus at late pachytene and diakinesis have been observed (not shown).

Mentions: The telomere cluster was found to disperse throughout pachytene as shown in Fig. 6. We used the progressive decrease in chromosome crowding to indicate the early, middle, and late substages of pachytene. Nuclei identified as early or middle pachytene (Fig. 6, A and B) were found to have a telomere distribution that was intermediate between the zygotene bouquet cluster and the dispersed, peripheral distribution found at late pachytene (Fig. 6 C). Pachytene nuclei, like those in zygotene, typically gave good hybridization signals resulting in detection of more than 80% of the expected telomeres. Most of these signals were found on or near the nuclear periphery as seen by stereo viewing of the models (Fig. 6 C). By the end of pachytene, the telomeres were fully dispersed (Fig. 6 C). By diakinesis the bivalent organization of the chromosomes was evident (Fig. 6 D). At this stage, the synaptonemal complex has presumably dissolved and the telomere pairs at the end of homologous chromosomes (double arrows Fig. 6 D) were connected only via the nearest chiasmata; thereby increasing the space between homologous telomeres.


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)

Telomere distribution at pachytene and diakinesis. Sequential color overlay projections of four nuclei subjected to telomere  FISH are shown for the DAPI (DNA, red) and FITC (telomeres, green) images as described in Fig. 3. (A–C) Examples of pachytene nuclei identified as early pachytene (A), middle pachytene (B), and late pachytene (C) are shown. (D) The bivalents of a diakinesis have  widely separated homologous telomeres (double arrows), reflecting the desynapsis of homologues. In all cases the nucleolus is seen to  be peripherally located, but less common examples of an internal nucleolus at late pachytene and diakinesis have been observed (not  shown).
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Related In: Results  -  Collection

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Figure 6: Telomere distribution at pachytene and diakinesis. Sequential color overlay projections of four nuclei subjected to telomere FISH are shown for the DAPI (DNA, red) and FITC (telomeres, green) images as described in Fig. 3. (A–C) Examples of pachytene nuclei identified as early pachytene (A), middle pachytene (B), and late pachytene (C) are shown. (D) The bivalents of a diakinesis have widely separated homologous telomeres (double arrows), reflecting the desynapsis of homologues. In all cases the nucleolus is seen to be peripherally located, but less common examples of an internal nucleolus at late pachytene and diakinesis have been observed (not shown).
Mentions: The telomere cluster was found to disperse throughout pachytene as shown in Fig. 6. We used the progressive decrease in chromosome crowding to indicate the early, middle, and late substages of pachytene. Nuclei identified as early or middle pachytene (Fig. 6, A and B) were found to have a telomere distribution that was intermediate between the zygotene bouquet cluster and the dispersed, peripheral distribution found at late pachytene (Fig. 6 C). Pachytene nuclei, like those in zygotene, typically gave good hybridization signals resulting in detection of more than 80% of the expected telomeres. Most of these signals were found on or near the nuclear periphery as seen by stereo viewing of the models (Fig. 6 C). By the end of pachytene, the telomeres were fully dispersed (Fig. 6 C). By diakinesis the bivalent organization of the chromosomes was evident (Fig. 6 D). At this stage, the synaptonemal complex has presumably dissolved and the telomere pairs at the end of homologous chromosomes (double arrows Fig. 6 D) were connected only via the nearest chiasmata; thereby increasing the space between homologous telomeres.

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