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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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Ray-traced three-dimensional models showing superimposition of all nuclei used in this study. Small blue spheres are centromere (a) or telomere (b) signals. Each nucleus is rotated so that the signal midpoint satisfies (x = 0, y = 0, z > 0). LEP, leptotene; PMI, premeiotic interphase; RND, random points placed in a modeled nucleus; SI, somatic interphase; ZYG, zygotene. The overall polarization of centromeres at premeiotic interphase and leptotene and clustering of telomeres at zygotene are readily apparent.
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fig5: Ray-traced three-dimensional models showing superimposition of all nuclei used in this study. Small blue spheres are centromere (a) or telomere (b) signals. Each nucleus is rotated so that the signal midpoint satisfies (x = 0, y = 0, z > 0). LEP, leptotene; PMI, premeiotic interphase; RND, random points placed in a modeled nucleus; SI, somatic interphase; ZYG, zygotene. The overall polarization of centromeres at premeiotic interphase and leptotene and clustering of telomeres at zygotene are readily apparent.

Mentions: Although centromeres do not cluster, visual inspection suggested that centromeres were organized in a polar fashion, i.e., confined to one half of the nucleus. In Fig. 3, four leptotene nuclei are shown with lines drawn demarcating two halves: one containing all the centromeres, the other containing no centromeres. To confirm these observations quantitatively, we analyzed the angular distributions of centromere and telomere signals in a larger sample of nuclei. It is important to note that pairwise distance analysis provides no information about polarization. In the course of analyzing random distributions of signals, we found that signals confined to one hemisphere did not significantly differ in their pairwise distance distribution from signals distributed throughout an entire sphere. We decided to quantify polarization by using the more sensitive measure of the angular displacement of individual signals from the axis formed by the signal midpoint and the nuclear center. For each nucleus, an axis was defined by the line connecting the midpoint of the signals (centromeres or telomeres) and the nuclear center; the angular displacement of each individual signal from this axis, measured from the origin (nuclear center), could then be calculated. Equivalent measurements were performed for simulated nuclei (see Materials and methods). Significant polarization of centromeres is seen in both premeiotic interphase and leptotene (Fig. 4; Table II). Telomeres are unpolarized until the bouquet, indicating that the clustering of telomeres is coincident with their polarization. The overall polarization of centromeres at premeiotic interphase and leptotene, and telomeres at zygotene, can be visualized by superimposing all models of a given stage, rotated appropriately (Fig. 5).


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

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

Ray-traced three-dimensional models showing superimposition of all nuclei used in this study. Small blue spheres are centromere (a) or telomere (b) signals. Each nucleus is rotated so that the signal midpoint satisfies (x = 0, y = 0, z > 0). LEP, leptotene; PMI, premeiotic interphase; RND, random points placed in a modeled nucleus; SI, somatic interphase; ZYG, zygotene. The overall polarization of centromeres at premeiotic interphase and leptotene and clustering of telomeres at zygotene are readily apparent.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2199251&req=5

fig5: Ray-traced three-dimensional models showing superimposition of all nuclei used in this study. Small blue spheres are centromere (a) or telomere (b) signals. Each nucleus is rotated so that the signal midpoint satisfies (x = 0, y = 0, z > 0). LEP, leptotene; PMI, premeiotic interphase; RND, random points placed in a modeled nucleus; SI, somatic interphase; ZYG, zygotene. The overall polarization of centromeres at premeiotic interphase and leptotene and clustering of telomeres at zygotene are readily apparent.
Mentions: Although centromeres do not cluster, visual inspection suggested that centromeres were organized in a polar fashion, i.e., confined to one half of the nucleus. In Fig. 3, four leptotene nuclei are shown with lines drawn demarcating two halves: one containing all the centromeres, the other containing no centromeres. To confirm these observations quantitatively, we analyzed the angular distributions of centromere and telomere signals in a larger sample of nuclei. It is important to note that pairwise distance analysis provides no information about polarization. In the course of analyzing random distributions of signals, we found that signals confined to one hemisphere did not significantly differ in their pairwise distance distribution from signals distributed throughout an entire sphere. We decided to quantify polarization by using the more sensitive measure of the angular displacement of individual signals from the axis formed by the signal midpoint and the nuclear center. For each nucleus, an axis was defined by the line connecting the midpoint of the signals (centromeres or telomeres) and the nuclear center; the angular displacement of each individual signal from this axis, measured from the origin (nuclear center), could then be calculated. Equivalent measurements were performed for simulated nuclei (see Materials and methods). Significant polarization of centromeres is seen in both premeiotic interphase and leptotene (Fig. 4; Table II). Telomeres are unpolarized until the bouquet, indicating that the clustering of telomeres is coincident with their polarization. The overall polarization of centromeres at premeiotic interphase and leptotene, and telomeres at zygotene, can be visualized by superimposing all models of a given stage, rotated appropriately (Fig. 5).

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