Limits...
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.

Show MeSH

Related in: MedlinePlus

The centromeric ends of telocentric chromosomes behave as centromeres before the bouquet, and as telomeres during the bouquet. (a) Steps in the formation of the telocentric chromosome. A normal chromosome 3 (left) undergoes rare centric misdivision, leading to a broken centromere (middle). Telomere sequence is then added to the centric ends by an unknown mechanism to form telocentric chromosomes (right). (b) A schematic of possible telocentric behaviors. In leptotene (left), the centromeric end can potentially either be polarized with the other centromeres (top, single arrow) or localize randomly like other telomeres (double arrow), whereas in zygotene, centromeric ends can either localize randomly like the other centromeres (top, double arrow) or participate in the bouquet with the other telomeres (bottom, single arrow). (c) Box-whisker plot of mean angular separation of the centromeric ends from the centromere midpoint at leptotene. The lower mean angle for the ditelocentric signals demonstrates that centromeric ends are significantly constrained compared with randomly placed points, and thus they are polarized with the other centromeres in the nucleus.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2199251&req=5

fig6: The centromeric ends of telocentric chromosomes behave as centromeres before the bouquet, and as telomeres during the bouquet. (a) Steps in the formation of the telocentric chromosome. A normal chromosome 3 (left) undergoes rare centric misdivision, leading to a broken centromere (middle). Telomere sequence is then added to the centric ends by an unknown mechanism to form telocentric chromosomes (right). (b) A schematic of possible telocentric behaviors. In leptotene (left), the centromeric end can potentially either be polarized with the other centromeres (top, single arrow) or localize randomly like other telomeres (double arrow), whereas in zygotene, centromeric ends can either localize randomly like the other centromeres (top, double arrow) or participate in the bouquet with the other telomeres (bottom, single arrow). (c) Box-whisker plot of mean angular separation of the centromeric ends from the centromere midpoint at leptotene. The lower mean angle for the ditelocentric signals demonstrates that centromeric ends are significantly constrained compared with randomly placed points, and thus they are polarized with the other centromeres in the nucleus.

Mentions: The quantitatively measured stage-specific behavior of centromeres and telomeres in wild-type maize nuclei provided a baseline to ask further questions about chromosome organization, using chromosome derivatives. The mechanisms of Rabl maintenance and bouquet formation were addressed through the use of lines containing either one copy (heterozygous) or two copies (homozygous) of telocentric chromosome 3 (Fig. 6). Heterozygous lines contain one copy of an unbroken chromosome 3. In principle, the behavior of a centromeric terminus before or after the bouquet could be centromere- (Fig. 6 b, top, single arrows) or telomere-like (Fig. 6 b, bottom, double arrows). To determine which mode of behavior was dominant, we performed FISH with telomere and centromere probes in both homozygous and heterozygous ditelocentric maize lines at all stages, and quantitatively analyzed their positions with respect to the normal centromeres and telomeres. The intensity and size of telomere signals was 2–5× greater at the centromeric ends of the telocentric chromosomes than at all other chromosome ends. Fortuitously, this larger size combined with the directly adjacent localization of CentC signal provided a convenient way of marking these ends without the need for a specific chromosome 3 centromere marker.


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

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

The centromeric ends of telocentric chromosomes behave as centromeres before the bouquet, and as telomeres during the bouquet. (a) Steps in the formation of the telocentric chromosome. A normal chromosome 3 (left) undergoes rare centric misdivision, leading to a broken centromere (middle). Telomere sequence is then added to the centric ends by an unknown mechanism to form telocentric chromosomes (right). (b) A schematic of possible telocentric behaviors. In leptotene (left), the centromeric end can potentially either be polarized with the other centromeres (top, single arrow) or localize randomly like other telomeres (double arrow), whereas in zygotene, centromeric ends can either localize randomly like the other centromeres (top, double arrow) or participate in the bouquet with the other telomeres (bottom, single arrow). (c) Box-whisker plot of mean angular separation of the centromeric ends from the centromere midpoint at leptotene. The lower mean angle for the ditelocentric signals demonstrates that centromeric ends are significantly constrained compared with randomly placed points, and thus they are polarized with the other centromeres in the nucleus.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2199251&req=5

fig6: The centromeric ends of telocentric chromosomes behave as centromeres before the bouquet, and as telomeres during the bouquet. (a) Steps in the formation of the telocentric chromosome. A normal chromosome 3 (left) undergoes rare centric misdivision, leading to a broken centromere (middle). Telomere sequence is then added to the centric ends by an unknown mechanism to form telocentric chromosomes (right). (b) A schematic of possible telocentric behaviors. In leptotene (left), the centromeric end can potentially either be polarized with the other centromeres (top, single arrow) or localize randomly like other telomeres (double arrow), whereas in zygotene, centromeric ends can either localize randomly like the other centromeres (top, double arrow) or participate in the bouquet with the other telomeres (bottom, single arrow). (c) Box-whisker plot of mean angular separation of the centromeric ends from the centromere midpoint at leptotene. The lower mean angle for the ditelocentric signals demonstrates that centromeric ends are significantly constrained compared with randomly placed points, and thus they are polarized with the other centromeres in the nucleus.
Mentions: The quantitatively measured stage-specific behavior of centromeres and telomeres in wild-type maize nuclei provided a baseline to ask further questions about chromosome organization, using chromosome derivatives. The mechanisms of Rabl maintenance and bouquet formation were addressed through the use of lines containing either one copy (heterozygous) or two copies (homozygous) of telocentric chromosome 3 (Fig. 6). Heterozygous lines contain one copy of an unbroken chromosome 3. In principle, the behavior of a centromeric terminus before or after the bouquet could be centromere- (Fig. 6 b, top, single arrows) or telomere-like (Fig. 6 b, bottom, double arrows). To determine which mode of behavior was dominant, we performed FISH with telomere and centromere probes in both homozygous and heterozygous ditelocentric maize lines at all stages, and quantitatively analyzed their positions with respect to the normal centromeres and telomeres. The intensity and size of telomere signals was 2–5× greater at the centromeric ends of the telocentric chromosomes than at all other chromosome ends. Fortuitously, this larger size combined with the directly adjacent localization of CentC signal provided a convenient way of marking these ends without the need for a specific chromosome 3 centromere marker.

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
Related in: MedlinePlus