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Leptotene/zygotene chromosome movement via the SUN/KASH protein bridge in Caenorhabditis elegans.

Baudrimont A, Penkner A, Woglar A, Machacek T, Wegrostek C, Gloggnitzer J, Fridkin A, Klein F, Gruenbaum Y, Pasierbek P, Jantsch V - PLoS Genet. (2010)

Bottom Line: Abrogation of synapsis led to a deceleration of SUN-1 aggregate movement.Analysis of matefin/SUN-1 in a double-strand break deficient mutant revealed that repair intermediates influenced matefin/SUN-1 aggregate dynamics.Investigation of movement in meiotic regulator mutants substantiated that proper orchestration of the meiotic program and effective repair of DNA double-strand breaks were necessary for the wild-type behavior of matefin/SUN-1 aggregates.

View Article: PubMed Central - PubMed

Affiliation: Department of Chromosome Biology, Max F. Perutz Laboratories, University of Vienna, Vienna, Austria.

ABSTRACT
The Caenorhabditis elegans inner nuclear envelope protein matefin/SUN-1 plays a conserved, pivotal role in the process of genome haploidization. CHK-2-dependent phosphorylation of SUN-1 regulates homologous chromosome pairing and interhomolog recombination in Caenorhabditis elegans. Using time-lapse microscopy, we characterized the movement of matefin/SUN-1::GFP aggregates (the equivalent of chromosomal attachment plaques) and showed that the dynamics of matefin/SUN-1 aggregates remained unchanged throughout leptonene/zygotene, despite the progression of pairing. Movement of SUN-1 aggregates correlated with chromatin polarization. We also analyzed the requirements for the formation of movement-competent matefin/SUN-1 aggregates in the context of chromosome structure and found that chromosome axes were required to produce wild-type numbers of attachment plaques. Abrogation of synapsis led to a deceleration of SUN-1 aggregate movement. Analysis of matefin/SUN-1 in a double-strand break deficient mutant revealed that repair intermediates influenced matefin/SUN-1 aggregate dynamics. Investigation of movement in meiotic regulator mutants substantiated that proper orchestration of the meiotic program and effective repair of DNA double-strand breaks were necessary for the wild-type behavior of matefin/SUN-1 aggregates.

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Establishment of synapsis and formation of high speed via shuffling of chromosome ends through SUN-1 patches.Chromosome axes (green lines) support binding of PC proteins (red or violet shapes) that connect chromosome ends (red, blue, and violet loops) to SUN-1 (brown ellipses), directly or indirectly, (unknown factor, blue circle). ZYG-12 (pink ellipses) and SUN-1 bridge chromosomes to cytoplasmic forces (orange arrow) to move chromosome ends. (A) SUN-1 patch containing two nonhomologous chromosome ends (red and blue loops) fuses with SUN-1 focus carrying a single chromosome end, a homolog (red loops). After fusion, chromosome ends will be shuffled inside the newly formed SUN-1 patch. When the homologous chromosome is found, synapsis overcomes the cytoplasmic forces and synapsis can be established. (B) The same scenario is depicted, except that ends of nonhomologous chromosomes are in the SUN-1 aggregate (violet loops). After fusion, chromosome ends will be shuffled. However, as the cytoplasmic forces overcome the attempt to synapse, one SUN-1 focus will be driven out of the patch. This tension-generated splitting event is one of the factors leading to the formation of high speed in the distribution of SUN-1 aggregates. Our data support other factors as sources for the high speed aggregates: recombination intermediates (C) and chromosomes entanglements (D).
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pgen-1001219-g008: Establishment of synapsis and formation of high speed via shuffling of chromosome ends through SUN-1 patches.Chromosome axes (green lines) support binding of PC proteins (red or violet shapes) that connect chromosome ends (red, blue, and violet loops) to SUN-1 (brown ellipses), directly or indirectly, (unknown factor, blue circle). ZYG-12 (pink ellipses) and SUN-1 bridge chromosomes to cytoplasmic forces (orange arrow) to move chromosome ends. (A) SUN-1 patch containing two nonhomologous chromosome ends (red and blue loops) fuses with SUN-1 focus carrying a single chromosome end, a homolog (red loops). After fusion, chromosome ends will be shuffled inside the newly formed SUN-1 patch. When the homologous chromosome is found, synapsis overcomes the cytoplasmic forces and synapsis can be established. (B) The same scenario is depicted, except that ends of nonhomologous chromosomes are in the SUN-1 aggregate (violet loops). After fusion, chromosome ends will be shuffled. However, as the cytoplasmic forces overcome the attempt to synapse, one SUN-1 focus will be driven out of the patch. This tension-generated splitting event is one of the factors leading to the formation of high speed in the distribution of SUN-1 aggregates. Our data support other factors as sources for the high speed aggregates: recombination intermediates (C) and chromosomes entanglements (D).

Mentions: We propose that duplets/multiplets of chromosome ends are linked to SUN-1 patches. These duplets/multiplets of chromosome ends attached to SUN-1 patches continue to move and meet other SUN-1 patches or foci. While the newly met SUN-1 aggregates coalesce, homology is assessed; how homology is assessed is still an open question. Chromosome ends are then shuffled through patches of SUN-1, and when the right partner is met, synapsis can take place. The shuffling of chromosome ends through the patches continues until all of the chromosomes have found their homolog. This process is dynamic, as most SUN-1 aggregates coalesce for less than 1 min. The shuffling of the chromosome ends during SUN-1 aggregate coalescence is, thus, one of the driving forces for homology search (Figure 8A and 8B). This allows homologous chromosome ends to meet and nonhomologous chromosomes to separate.


Leptotene/zygotene chromosome movement via the SUN/KASH protein bridge in Caenorhabditis elegans.

Baudrimont A, Penkner A, Woglar A, Machacek T, Wegrostek C, Gloggnitzer J, Fridkin A, Klein F, Gruenbaum Y, Pasierbek P, Jantsch V - PLoS Genet. (2010)

Establishment of synapsis and formation of high speed via shuffling of chromosome ends through SUN-1 patches.Chromosome axes (green lines) support binding of PC proteins (red or violet shapes) that connect chromosome ends (red, blue, and violet loops) to SUN-1 (brown ellipses), directly or indirectly, (unknown factor, blue circle). ZYG-12 (pink ellipses) and SUN-1 bridge chromosomes to cytoplasmic forces (orange arrow) to move chromosome ends. (A) SUN-1 patch containing two nonhomologous chromosome ends (red and blue loops) fuses with SUN-1 focus carrying a single chromosome end, a homolog (red loops). After fusion, chromosome ends will be shuffled inside the newly formed SUN-1 patch. When the homologous chromosome is found, synapsis overcomes the cytoplasmic forces and synapsis can be established. (B) The same scenario is depicted, except that ends of nonhomologous chromosomes are in the SUN-1 aggregate (violet loops). After fusion, chromosome ends will be shuffled. However, as the cytoplasmic forces overcome the attempt to synapse, one SUN-1 focus will be driven out of the patch. This tension-generated splitting event is one of the factors leading to the formation of high speed in the distribution of SUN-1 aggregates. Our data support other factors as sources for the high speed aggregates: recombination intermediates (C) and chromosomes entanglements (D).
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2991264&req=5

pgen-1001219-g008: Establishment of synapsis and formation of high speed via shuffling of chromosome ends through SUN-1 patches.Chromosome axes (green lines) support binding of PC proteins (red or violet shapes) that connect chromosome ends (red, blue, and violet loops) to SUN-1 (brown ellipses), directly or indirectly, (unknown factor, blue circle). ZYG-12 (pink ellipses) and SUN-1 bridge chromosomes to cytoplasmic forces (orange arrow) to move chromosome ends. (A) SUN-1 patch containing two nonhomologous chromosome ends (red and blue loops) fuses with SUN-1 focus carrying a single chromosome end, a homolog (red loops). After fusion, chromosome ends will be shuffled inside the newly formed SUN-1 patch. When the homologous chromosome is found, synapsis overcomes the cytoplasmic forces and synapsis can be established. (B) The same scenario is depicted, except that ends of nonhomologous chromosomes are in the SUN-1 aggregate (violet loops). After fusion, chromosome ends will be shuffled. However, as the cytoplasmic forces overcome the attempt to synapse, one SUN-1 focus will be driven out of the patch. This tension-generated splitting event is one of the factors leading to the formation of high speed in the distribution of SUN-1 aggregates. Our data support other factors as sources for the high speed aggregates: recombination intermediates (C) and chromosomes entanglements (D).
Mentions: We propose that duplets/multiplets of chromosome ends are linked to SUN-1 patches. These duplets/multiplets of chromosome ends attached to SUN-1 patches continue to move and meet other SUN-1 patches or foci. While the newly met SUN-1 aggregates coalesce, homology is assessed; how homology is assessed is still an open question. Chromosome ends are then shuffled through patches of SUN-1, and when the right partner is met, synapsis can take place. The shuffling of chromosome ends through the patches continues until all of the chromosomes have found their homolog. This process is dynamic, as most SUN-1 aggregates coalesce for less than 1 min. The shuffling of the chromosome ends during SUN-1 aggregate coalescence is, thus, one of the driving forces for homology search (Figure 8A and 8B). This allows homologous chromosome ends to meet and nonhomologous chromosomes to separate.

Bottom Line: Abrogation of synapsis led to a deceleration of SUN-1 aggregate movement.Analysis of matefin/SUN-1 in a double-strand break deficient mutant revealed that repair intermediates influenced matefin/SUN-1 aggregate dynamics.Investigation of movement in meiotic regulator mutants substantiated that proper orchestration of the meiotic program and effective repair of DNA double-strand breaks were necessary for the wild-type behavior of matefin/SUN-1 aggregates.

View Article: PubMed Central - PubMed

Affiliation: Department of Chromosome Biology, Max F. Perutz Laboratories, University of Vienna, Vienna, Austria.

ABSTRACT
The Caenorhabditis elegans inner nuclear envelope protein matefin/SUN-1 plays a conserved, pivotal role in the process of genome haploidization. CHK-2-dependent phosphorylation of SUN-1 regulates homologous chromosome pairing and interhomolog recombination in Caenorhabditis elegans. Using time-lapse microscopy, we characterized the movement of matefin/SUN-1::GFP aggregates (the equivalent of chromosomal attachment plaques) and showed that the dynamics of matefin/SUN-1 aggregates remained unchanged throughout leptonene/zygotene, despite the progression of pairing. Movement of SUN-1 aggregates correlated with chromatin polarization. We also analyzed the requirements for the formation of movement-competent matefin/SUN-1 aggregates in the context of chromosome structure and found that chromosome axes were required to produce wild-type numbers of attachment plaques. Abrogation of synapsis led to a deceleration of SUN-1 aggregate movement. Analysis of matefin/SUN-1 in a double-strand break deficient mutant revealed that repair intermediates influenced matefin/SUN-1 aggregate dynamics. Investigation of movement in meiotic regulator mutants substantiated that proper orchestration of the meiotic program and effective repair of DNA double-strand breaks were necessary for the wild-type behavior of matefin/SUN-1 aggregates.

Show MeSH
Related in: MedlinePlus