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Crossing over is coupled to late meiotic prophase bivalent differentiation through asymmetric disassembly of the SC.

Nabeshima K, Villeneuve AM, Colaiácovo MP - J. Cell Biol. (2005)

Bottom Line: This and other manifestations of asymmetry along chromosomes are lost in synapsis-proficient crossover-defective mutants, which often retain SYP-1,2 along the full lengths of coiled diplotene axes.Moreover, a gamma-irradiation treatment that restores crossovers in the spo-11 mutant also restores asymmetry of SYP-1 localization.We propose that crossovers or crossover precursors serve as symmetry-breaking events that promote differentiation of subregions of the bivalent by triggering asymmetric disassembly of the SC.

View Article: PubMed Central - PubMed

Affiliation: Department of Developmental Biology, Stanford University School of Medicine, Stanford, CA 94305, USA.

ABSTRACT
Homologous chromosome pairs (bivalents) undergo restructuring during meiotic prophase to convert a configuration that promotes crossover recombination into one that promotes bipolar spindle attachment and localized cohesion loss. We have imaged remodeling of meiotic chromosome structures after pachytene exit in Caenorhabditis elegans. Chromosome shortening during diplonema is accompanied by coiling of chromosome axes and highly asymmetric departure of synaptonemal complex (SC) central region proteins SYP-1 and SYP-2, which diminish over most of the length of each desynapsing bivalent while becoming concentrated on axis segments distal to the single emerging chiasma. This and other manifestations of asymmetry along chromosomes are lost in synapsis-proficient crossover-defective mutants, which often retain SYP-1,2 along the full lengths of coiled diplotene axes. Moreover, a gamma-irradiation treatment that restores crossovers in the spo-11 mutant also restores asymmetry of SYP-1 localization. We propose that crossovers or crossover precursors serve as symmetry-breaking events that promote differentiation of subregions of the bivalent by triggering asymmetric disassembly of the SC.

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Dynamic localization of SYP-1 and AIR-2. (A) Immunolocalization of SYP-1 and AIR-2 in wild-type and spo-11 nuclei at the indicated stages. For diakinesis nuclei, −3, −2, and −1 indicate position relative to the spermatheca, with the oocyte in the −1 position (closest to the spermatheca) being the most mature. In A and B, detection thresholds for α-AIR-2 signals were lower for the pachytene and diplotene panels than for the diakinesis panels to permit imaging of both the lower levels of chromosome-associated AIR-2 at the earlier stages and the subchromosomal localization of the higher levels of AIR-2 in late diakinesis. DAPI-stained chromatin is shown in blue in the merged images. (B) SYP-1 and AIR-2 localization after γ-irradiation. Bars, 5 μm.
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fig5: Dynamic localization of SYP-1 and AIR-2. (A) Immunolocalization of SYP-1 and AIR-2 in wild-type and spo-11 nuclei at the indicated stages. For diakinesis nuclei, −3, −2, and −1 indicate position relative to the spermatheca, with the oocyte in the −1 position (closest to the spermatheca) being the most mature. In A and B, detection thresholds for α-AIR-2 signals were lower for the pachytene and diplotene panels than for the diakinesis panels to permit imaging of both the lower levels of chromosome-associated AIR-2 at the earlier stages and the subchromosomal localization of the higher levels of AIR-2 in late diakinesis. DAPI-stained chromatin is shown in blue in the merged images. (B) SYP-1 and AIR-2 localization after γ-irradiation. Bars, 5 μm.

Mentions: As DNA breaks induced by γ-irradiation can bypass the requirement for SPO-11, rescuing the crossover and chiasma formation defects in a spo-11 mutant (Dernburg et al., 1998), we tested whether or not γ-irradiation could also restore asymmetry of SYP-1 departure. Fig. 4 (A and B) and Fig. 5 B show that asymmetry is indeed substantially restored in the spo-11 mutant after γ-irradiation. In irradiated spo-11 worms, we observed diplotene nuclei with six robust SYP-1 stretches, each concentrated over a limited subset of axis staining corresponding to the still-synapsed regions of the desynapsing bivalents. Restoration of localized SYP-1 retention by γ-irradiation indicates that some aspect of the recombination event by itself, rather than the SPO-11 protein, is responsible for eliciting asymmetry in SC disassembly.


Crossing over is coupled to late meiotic prophase bivalent differentiation through asymmetric disassembly of the SC.

Nabeshima K, Villeneuve AM, Colaiácovo MP - J. Cell Biol. (2005)

Dynamic localization of SYP-1 and AIR-2. (A) Immunolocalization of SYP-1 and AIR-2 in wild-type and spo-11 nuclei at the indicated stages. For diakinesis nuclei, −3, −2, and −1 indicate position relative to the spermatheca, with the oocyte in the −1 position (closest to the spermatheca) being the most mature. In A and B, detection thresholds for α-AIR-2 signals were lower for the pachytene and diplotene panels than for the diakinesis panels to permit imaging of both the lower levels of chromosome-associated AIR-2 at the earlier stages and the subchromosomal localization of the higher levels of AIR-2 in late diakinesis. DAPI-stained chromatin is shown in blue in the merged images. (B) SYP-1 and AIR-2 localization after γ-irradiation. Bars, 5 μm.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2171829&req=5

fig5: Dynamic localization of SYP-1 and AIR-2. (A) Immunolocalization of SYP-1 and AIR-2 in wild-type and spo-11 nuclei at the indicated stages. For diakinesis nuclei, −3, −2, and −1 indicate position relative to the spermatheca, with the oocyte in the −1 position (closest to the spermatheca) being the most mature. In A and B, detection thresholds for α-AIR-2 signals were lower for the pachytene and diplotene panels than for the diakinesis panels to permit imaging of both the lower levels of chromosome-associated AIR-2 at the earlier stages and the subchromosomal localization of the higher levels of AIR-2 in late diakinesis. DAPI-stained chromatin is shown in blue in the merged images. (B) SYP-1 and AIR-2 localization after γ-irradiation. Bars, 5 μm.
Mentions: As DNA breaks induced by γ-irradiation can bypass the requirement for SPO-11, rescuing the crossover and chiasma formation defects in a spo-11 mutant (Dernburg et al., 1998), we tested whether or not γ-irradiation could also restore asymmetry of SYP-1 departure. Fig. 4 (A and B) and Fig. 5 B show that asymmetry is indeed substantially restored in the spo-11 mutant after γ-irradiation. In irradiated spo-11 worms, we observed diplotene nuclei with six robust SYP-1 stretches, each concentrated over a limited subset of axis staining corresponding to the still-synapsed regions of the desynapsing bivalents. Restoration of localized SYP-1 retention by γ-irradiation indicates that some aspect of the recombination event by itself, rather than the SPO-11 protein, is responsible for eliciting asymmetry in SC disassembly.

Bottom Line: This and other manifestations of asymmetry along chromosomes are lost in synapsis-proficient crossover-defective mutants, which often retain SYP-1,2 along the full lengths of coiled diplotene axes.Moreover, a gamma-irradiation treatment that restores crossovers in the spo-11 mutant also restores asymmetry of SYP-1 localization.We propose that crossovers or crossover precursors serve as symmetry-breaking events that promote differentiation of subregions of the bivalent by triggering asymmetric disassembly of the SC.

View Article: PubMed Central - PubMed

Affiliation: Department of Developmental Biology, Stanford University School of Medicine, Stanford, CA 94305, USA.

ABSTRACT
Homologous chromosome pairs (bivalents) undergo restructuring during meiotic prophase to convert a configuration that promotes crossover recombination into one that promotes bipolar spindle attachment and localized cohesion loss. We have imaged remodeling of meiotic chromosome structures after pachytene exit in Caenorhabditis elegans. Chromosome shortening during diplonema is accompanied by coiling of chromosome axes and highly asymmetric departure of synaptonemal complex (SC) central region proteins SYP-1 and SYP-2, which diminish over most of the length of each desynapsing bivalent while becoming concentrated on axis segments distal to the single emerging chiasma. This and other manifestations of asymmetry along chromosomes are lost in synapsis-proficient crossover-defective mutants, which often retain SYP-1,2 along the full lengths of coiled diplotene axes. Moreover, a gamma-irradiation treatment that restores crossovers in the spo-11 mutant also restores asymmetry of SYP-1 localization. We propose that crossovers or crossover precursors serve as symmetry-breaking events that promote differentiation of subregions of the bivalent by triggering asymmetric disassembly of the SC.

Show MeSH