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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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Meiotic behavior of a ring chromosome. (a) The origin of the ring chromosome used in this study. Firstly, a B chromosome underwent reciprocal translocation with chromosome 9 to give rise to translocation chromosome TB-9Sb. This chromosome then circularized to form the ring chromosome B9 ring. The resulting configuration places a B centromere (containing blocks of B repeat sequences) adjacent to a canonical telomere sequence, making possible its detection by FISH. (b) A schematic of possible ring chromosome behaviors during the bouquet. A ring chromosome may localize randomly within the cell (double arrows) or near the bouquet site (single arrow). (c) Box-whisker plots of distances from the bouquet center to the ring signals and to all telomere signals. RND, distances of randomly placed points in modeled nuclei. By this measure the ring signals do not significantly differ in their localization from telomere signals.
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fig8: Meiotic behavior of a ring chromosome. (a) The origin of the ring chromosome used in this study. Firstly, a B chromosome underwent reciprocal translocation with chromosome 9 to give rise to translocation chromosome TB-9Sb. This chromosome then circularized to form the ring chromosome B9 ring. The resulting configuration places a B centromere (containing blocks of B repeat sequences) adjacent to a canonical telomere sequence, making possible its detection by FISH. (b) A schematic of possible ring chromosome behaviors during the bouquet. A ring chromosome may localize randomly within the cell (double arrows) or near the bouquet site (single arrow). (c) Box-whisker plots of distances from the bouquet center to the ring signals and to all telomere signals. RND, distances of randomly placed points in modeled nuclei. By this measure the ring signals do not significantly differ in their localization from telomere signals.

Mentions: We analyzed the behavior of ring chromosomes to assess whether participation in the meiotic bouquet requires chromosome termini. The ring chromosomes used in the study were derived from an A–B translocation of maize chromosome 9. The initial translocation chromosome spontaneously circularized after a centric misdivision to give rise to a ring chromosome (Fig. 8 a). The interstitial telomeric repeats of the ring chromosome are thus located near the centromere, which contains a highly repetitive DNA sequence of the B repeat family (Kaszás and Birchler, 1996). Because this block of telomeric repeats is the only occurence of this sequence in the genome that is closely linked to B repeats, we could determine its localization by using FISH probes against both repeats in the same samples. Because the ring chromosome contains wild-type alleles of the seed markers shrunken (Sh) and bronze (Bz), its segregation can be monitored phenotypically.


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

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

Meiotic behavior of a ring chromosome. (a) The origin of the ring chromosome used in this study. Firstly, a B chromosome underwent reciprocal translocation with chromosome 9 to give rise to translocation chromosome TB-9Sb. This chromosome then circularized to form the ring chromosome B9 ring. The resulting configuration places a B centromere (containing blocks of B repeat sequences) adjacent to a canonical telomere sequence, making possible its detection by FISH. (b) A schematic of possible ring chromosome behaviors during the bouquet. A ring chromosome may localize randomly within the cell (double arrows) or near the bouquet site (single arrow). (c) Box-whisker plots of distances from the bouquet center to the ring signals and to all telomere signals. RND, distances of randomly placed points in modeled nuclei. By this measure the ring signals do not significantly differ in their localization from telomere signals.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2199251&req=5

fig8: Meiotic behavior of a ring chromosome. (a) The origin of the ring chromosome used in this study. Firstly, a B chromosome underwent reciprocal translocation with chromosome 9 to give rise to translocation chromosome TB-9Sb. This chromosome then circularized to form the ring chromosome B9 ring. The resulting configuration places a B centromere (containing blocks of B repeat sequences) adjacent to a canonical telomere sequence, making possible its detection by FISH. (b) A schematic of possible ring chromosome behaviors during the bouquet. A ring chromosome may localize randomly within the cell (double arrows) or near the bouquet site (single arrow). (c) Box-whisker plots of distances from the bouquet center to the ring signals and to all telomere signals. RND, distances of randomly placed points in modeled nuclei. By this measure the ring signals do not significantly differ in their localization from telomere signals.
Mentions: We analyzed the behavior of ring chromosomes to assess whether participation in the meiotic bouquet requires chromosome termini. The ring chromosomes used in the study were derived from an A–B translocation of maize chromosome 9. The initial translocation chromosome spontaneously circularized after a centric misdivision to give rise to a ring chromosome (Fig. 8 a). The interstitial telomeric repeats of the ring chromosome are thus located near the centromere, which contains a highly repetitive DNA sequence of the B repeat family (Kaszás and Birchler, 1996). Because this block of telomeric repeats is the only occurence of this sequence in the genome that is closely linked to B repeats, we could determine its localization by using FISH probes against both repeats in the same samples. Because the ring chromosome contains wild-type alleles of the seed markers shrunken (Sh) and bronze (Bz), its segregation can be monitored phenotypically.

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