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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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Localization of telocentric ends in meiotic prophase. In each row, the first four images are quarter projections of a single nucleus; the fifth image is the full projection. Telomeres are labeled in green; centromeres are labeled in red; chromosomes (counterstained with DAPI) are blue. Telocentric ends, characterized by brighter than normal telomere staining with adjacent centromere staining, are highlighted in the full projections with arrows. In premeiotic interphase and leptotene (top two rows), the telocentric ends localize in the same hemisphere as the bulk of the centromeres (yellow line) and appear close to the NE. In zygotene, all the telocentric ends localize to the bouquet. The premeiotic nucleus has one wild-type copy of chromosome 3, and one telocentric (long and short arms separate) copy yielding two signals; the leptotene and zygotene nuclei have two telocentric copies which yield four signals.
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fig7: Localization of telocentric ends in meiotic prophase. In each row, the first four images are quarter projections of a single nucleus; the fifth image is the full projection. Telomeres are labeled in green; centromeres are labeled in red; chromosomes (counterstained with DAPI) are blue. Telocentric ends, characterized by brighter than normal telomere staining with adjacent centromere staining, are highlighted in the full projections with arrows. In premeiotic interphase and leptotene (top two rows), the telocentric ends localize in the same hemisphere as the bulk of the centromeres (yellow line) and appear close to the NE. In zygotene, all the telocentric ends localize to the bouquet. The premeiotic nucleus has one wild-type copy of chromosome 3, and one telocentric (long and short arms separate) copy yielding two signals; the leptotene and zygotene nuclei have two telocentric copies which yield four signals.

Mentions: In premeiotic interphase (preceding leptotene but after the last premeiotic cell division) and leptotene nuclei, the centromeric ends of telocentric chromosomes were consistently found to lie in the same hemisphere with the majority of centromere signals (Fig. 7, top). Telocentric ends were analyzed for their polarization relative to the midpoint of the centromeres at leptotene. Their angular displacement from the axis formed by the nuclear midpoint and the centromere signal midpoint was measured, and compared to normal centromeres and to randomly placed points. For random points, two points were placed at random in the models and their angular separation from the centromere polarization axis was measured. The centromeric ends were found to be significantly constrained to one end of the axis (Figs. 6 c and 7, middle; Table III). The centromeric ends show no difference in polarity from the other centromeres, whereas they do significantly differ from random points. Although normal chromosome ends are randomly localized at leptotene, centromeric ends were constrained to one pole.


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

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

Localization of telocentric ends in meiotic prophase. In each row, the first four images are quarter projections of a single nucleus; the fifth image is the full projection. Telomeres are labeled in green; centromeres are labeled in red; chromosomes (counterstained with DAPI) are blue. Telocentric ends, characterized by brighter than normal telomere staining with adjacent centromere staining, are highlighted in the full projections with arrows. In premeiotic interphase and leptotene (top two rows), the telocentric ends localize in the same hemisphere as the bulk of the centromeres (yellow line) and appear close to the NE. In zygotene, all the telocentric ends localize to the bouquet. The premeiotic nucleus has one wild-type copy of chromosome 3, and one telocentric (long and short arms separate) copy yielding two signals; the leptotene and zygotene nuclei have two telocentric copies which yield four signals.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2199251&req=5

fig7: Localization of telocentric ends in meiotic prophase. In each row, the first four images are quarter projections of a single nucleus; the fifth image is the full projection. Telomeres are labeled in green; centromeres are labeled in red; chromosomes (counterstained with DAPI) are blue. Telocentric ends, characterized by brighter than normal telomere staining with adjacent centromere staining, are highlighted in the full projections with arrows. In premeiotic interphase and leptotene (top two rows), the telocentric ends localize in the same hemisphere as the bulk of the centromeres (yellow line) and appear close to the NE. In zygotene, all the telocentric ends localize to the bouquet. The premeiotic nucleus has one wild-type copy of chromosome 3, and one telocentric (long and short arms separate) copy yielding two signals; the leptotene and zygotene nuclei have two telocentric copies which yield four signals.
Mentions: In premeiotic interphase (preceding leptotene but after the last premeiotic cell division) and leptotene nuclei, the centromeric ends of telocentric chromosomes were consistently found to lie in the same hemisphere with the majority of centromere signals (Fig. 7, top). Telocentric ends were analyzed for their polarization relative to the midpoint of the centromeres at leptotene. Their angular displacement from the axis formed by the nuclear midpoint and the centromere signal midpoint was measured, and compared to normal centromeres and to randomly placed points. For random points, two points were placed at random in the models and their angular separation from the centromere polarization axis was measured. The centromeric ends were found to be significantly constrained to one end of the axis (Figs. 6 c and 7, middle; Table III). The centromeric ends show no difference in polarity from the other centromeres, whereas they do significantly differ from random points. Although normal chromosome ends are randomly localized at leptotene, centromeric ends were constrained to one pole.

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