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Telomeres act autonomously in maize to organize the meiotic bouquet from a semipolarized chromosome orientation.

Carlton PM, Cande WZ - J. Cell Biol. (2002)

Bottom Line: Our results demonstrate that meiotic centromeres are polarized prior to the bouquet stage, but that this polarization does not contribute to bouquet formation.We find that: (a) the healed ends of broken chromosomes, which contain telomere repeats, can enter the bouquet; (b) ring chromosomes enter the bouquet, indicating that terminal position on a chromosome is not necessary for telomere sequences to localize to the bouquet; and (c) beginning at zygotene, the behavior of telomeres is dominant over any centromere-mediated chromosome behavior.The results of this study indicate that specific chromosome regions are acted upon to determine the organization of meiotic chromosomes, enabling the bouquet to form despite large-scale changes in chromosome architecture.

View Article: PubMed Central - PubMed

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

ABSTRACT
During meiosis, chromosomes undergo large-scale reorganization to allow pairing between homologues, which is necessary for recombination and segregation. In many organisms, pairing of homologous chromosomes is accompanied, and possibly facilitated, by the bouquet, the clustering of telomeres in a small region of the nuclear periphery. Taking advantage of the cytological accessibility of meiosis in maize, we have characterized the organization of centromeres and telomeres throughout meiotic prophase. Our results demonstrate that meiotic centromeres are polarized prior to the bouquet stage, but that this polarization does not contribute to bouquet formation. By examining telocentric and ring chromosomes, we have tested the cis-acting requirements for participation in the bouquet. We find that: (a) the healed ends of broken chromosomes, which contain telomere repeats, can enter the bouquet; (b) ring chromosomes enter the bouquet, indicating that terminal position on a chromosome is not necessary for telomere sequences to localize to the bouquet; and (c) beginning at zygotene, the behavior of telomeres is dominant over any centromere-mediated chromosome behavior. The results of this study indicate that specific chromosome regions are acted upon to determine the organization of meiotic chromosomes, enabling the bouquet to form despite large-scale changes in chromosome architecture.

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Centromere and telomere positions during the stages of maize meiosis used in this study are shown. Representative nuclei from each of the five stages observed are displayed as a series of semioverlapping quarter-volume projections. Cells were subjected to FISH using oligonucleotide probes to the telomere repeat (green) and the CentC repeat (red), and imaged in three dimensions. Chromosomes are counterstained with DAPI (blue). (a) The last prophase before meiosis. (b) Premeiotic interphase. (c) Leptotene. (d) Zygotene. (e) Tapetal cell prophase. Each stage is shown as a maximum-intensity projection of one quarter of the entire image stack. Arrowheads and insets in d indicate elongated centromere signals. Large fields of view containing several (5–20) cells were acquired and later cropped, resulting in three-dimensional datasets containing one nucleus each. The number of centromere signals detected ranged from 15 to 20 in nuclei before zygotene, and 9 to 16 in nuclei at zygotene. Bars, 5 μm.
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fig1: Centromere and telomere positions during the stages of maize meiosis used in this study are shown. Representative nuclei from each of the five stages observed are displayed as a series of semioverlapping quarter-volume projections. Cells were subjected to FISH using oligonucleotide probes to the telomere repeat (green) and the CentC repeat (red), and imaged in three dimensions. Chromosomes are counterstained with DAPI (blue). (a) The last prophase before meiosis. (b) Premeiotic interphase. (c) Leptotene. (d) Zygotene. (e) Tapetal cell prophase. Each stage is shown as a maximum-intensity projection of one quarter of the entire image stack. Arrowheads and insets in d indicate elongated centromere signals. Large fields of view containing several (5–20) cells were acquired and later cropped, resulting in three-dimensional datasets containing one nucleus each. The number of centromere signals detected ranged from 15 to 20 in nuclei before zygotene, and 9 to 16 in nuclei at zygotene. Bars, 5 μm.

Mentions: The earliest cells examined were in prophase of the final premeiotic mitosis (Fig. 1 a). Chromosomes in these early cells were both longer and straighter than those of somatic prophase cells. Centromere and telomere FISH signals were evident as doublets, one signal per sister chromatid. The centromere signals appeared to be restricted to roughly one half of the nucleus, whereas the telomeres were concentrated in the opposite half. However, a subset of telomere signals was found in the centromere hemisphere of the nucleus, indicating freedom of movement of the chromosome arms, and an incomplete or degenerate Rabl organization.


Telomeres act autonomously in maize to organize the meiotic bouquet from a semipolarized chromosome orientation.

Carlton PM, Cande WZ - J. Cell Biol. (2002)

Centromere and telomere positions during the stages of maize meiosis used in this study are shown. Representative nuclei from each of the five stages observed are displayed as a series of semioverlapping quarter-volume projections. Cells were subjected to FISH using oligonucleotide probes to the telomere repeat (green) and the CentC repeat (red), and imaged in three dimensions. Chromosomes are counterstained with DAPI (blue). (a) The last prophase before meiosis. (b) Premeiotic interphase. (c) Leptotene. (d) Zygotene. (e) Tapetal cell prophase. Each stage is shown as a maximum-intensity projection of one quarter of the entire image stack. Arrowheads and insets in d indicate elongated centromere signals. Large fields of view containing several (5–20) cells were acquired and later cropped, resulting in three-dimensional datasets containing one nucleus each. The number of centromere signals detected ranged from 15 to 20 in nuclei before zygotene, and 9 to 16 in nuclei at zygotene. Bars, 5 μm.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2199251&req=5

fig1: Centromere and telomere positions during the stages of maize meiosis used in this study are shown. Representative nuclei from each of the five stages observed are displayed as a series of semioverlapping quarter-volume projections. Cells were subjected to FISH using oligonucleotide probes to the telomere repeat (green) and the CentC repeat (red), and imaged in three dimensions. Chromosomes are counterstained with DAPI (blue). (a) The last prophase before meiosis. (b) Premeiotic interphase. (c) Leptotene. (d) Zygotene. (e) Tapetal cell prophase. Each stage is shown as a maximum-intensity projection of one quarter of the entire image stack. Arrowheads and insets in d indicate elongated centromere signals. Large fields of view containing several (5–20) cells were acquired and later cropped, resulting in three-dimensional datasets containing one nucleus each. The number of centromere signals detected ranged from 15 to 20 in nuclei before zygotene, and 9 to 16 in nuclei at zygotene. Bars, 5 μm.
Mentions: The earliest cells examined were in prophase of the final premeiotic mitosis (Fig. 1 a). Chromosomes in these early cells were both longer and straighter than those of somatic prophase cells. Centromere and telomere FISH signals were evident as doublets, one signal per sister chromatid. The centromere signals appeared to be restricted to roughly one half of the nucleus, whereas the telomeres were concentrated in the opposite half. However, a subset of telomere signals was found in the centromere hemisphere of the nucleus, indicating freedom of movement of the chromosome arms, and an incomplete or degenerate Rabl organization.

Bottom Line: Our results demonstrate that meiotic centromeres are polarized prior to the bouquet stage, but that this polarization does not contribute to bouquet formation.We find that: (a) the healed ends of broken chromosomes, which contain telomere repeats, can enter the bouquet; (b) ring chromosomes enter the bouquet, indicating that terminal position on a chromosome is not necessary for telomere sequences to localize to the bouquet; and (c) beginning at zygotene, the behavior of telomeres is dominant over any centromere-mediated chromosome behavior.The results of this study indicate that specific chromosome regions are acted upon to determine the organization of meiotic chromosomes, enabling the bouquet to form despite large-scale changes in chromosome architecture.

View Article: PubMed Central - PubMed

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

ABSTRACT
During meiosis, chromosomes undergo large-scale reorganization to allow pairing between homologues, which is necessary for recombination and segregation. In many organisms, pairing of homologous chromosomes is accompanied, and possibly facilitated, by the bouquet, the clustering of telomeres in a small region of the nuclear periphery. Taking advantage of the cytological accessibility of meiosis in maize, we have characterized the organization of centromeres and telomeres throughout meiotic prophase. Our results demonstrate that meiotic centromeres are polarized prior to the bouquet stage, but that this polarization does not contribute to bouquet formation. By examining telocentric and ring chromosomes, we have tested the cis-acting requirements for participation in the bouquet. We find that: (a) the healed ends of broken chromosomes, which contain telomere repeats, can enter the bouquet; (b) ring chromosomes enter the bouquet, indicating that terminal position on a chromosome is not necessary for telomere sequences to localize to the bouquet; and (c) beginning at zygotene, the behavior of telomeres is dominant over any centromere-mediated chromosome behavior. The results of this study indicate that specific chromosome regions are acted upon to determine the organization of meiotic chromosomes, enabling the bouquet to form despite large-scale changes in chromosome architecture.

Show MeSH