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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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Chromosome reorganization after pachytene exit. See text for description. (A) Immunolocalization of REC-8 and SYP-1 at the pachytene–diplotene transition; late pachytene nuclei are at the left, diplotene at the right. Bar, 5 μm. (B) Projection halfway through a late pachytene nucleus showing unevenness in intensity of SYP-1 signal along bivalent (arrow). Bar, 2 μm. (C) Position of nuclei showing SYP-1 asymmetry (right side of a dashed line) relative to disappearance of RAD-51 foci. Bar, 10 μm. (D) Volume renderings of individual diplotene bivalents. Red, α-REC-8; green, α-SYP-1; blue, DAPI. i, X-shaped bivalent; ii-a–c, Y-shaped bivalent shown from two different angles. Bar, 5 μm. Videos 1 and 2 (available at http://www.jcb.org/cgi/content/full/jcb200410144/DC1) show rotating images of these bivalents. (E) Complete complement of bivalents from a single oocyte nucleus at early/mid-diakinesis. Bar, 5 μm.
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fig2: Chromosome reorganization after pachytene exit. See text for description. (A) Immunolocalization of REC-8 and SYP-1 at the pachytene–diplotene transition; late pachytene nuclei are at the left, diplotene at the right. Bar, 5 μm. (B) Projection halfway through a late pachytene nucleus showing unevenness in intensity of SYP-1 signal along bivalent (arrow). Bar, 2 μm. (C) Position of nuclei showing SYP-1 asymmetry (right side of a dashed line) relative to disappearance of RAD-51 foci. Bar, 10 μm. (D) Volume renderings of individual diplotene bivalents. Red, α-REC-8; green, α-SYP-1; blue, DAPI. i, X-shaped bivalent; ii-a–c, Y-shaped bivalent shown from two different angles. Bar, 5 μm. Videos 1 and 2 (available at http://www.jcb.org/cgi/content/full/jcb200410144/DC1) show rotating images of these bivalents. (E) Complete complement of bivalents from a single oocyte nucleus at early/mid-diakinesis. Bar, 5 μm.

Mentions: SC disassembly at the pachytene–diplotene transition is accompanied by a major transition in the organization of chromosome axes. REC-8 (Fig. 2) and HIM-3 (not depicted) continue to localize along the lengths of desynapsing chromosomes, but whereas REC-8 and HIM-3 signals appear as extended linear stretches in pachytene nuclei, this linear appearance gives way to a more convoluted appearance as nuclei enter diplonema. In a subset of diplotene nuclei, a coiled organization of chromosome axes can be clearly resolved (three-dimensional volume renderings in Fig. 2 D and Video 1, available at http://www.jcb.org/cgi/content/full/jcb200410144/DC1). Axis coiling coincides temporally with shortening of the end-to-end lengths of chromosomes that occurs at this stage, suggesting that coiling of preexisting axial structures may either contribute to or be a consequence of the chromosome shortening mechanism. Axis coiling during late meiotic prophase was observed previously in silver-stained preparations of rye and lily chromosomes (Fedotova et al., 1989; Stack, 1991); however, this is the first report of coiled axial structures during meiotic prophase visualized by imaging of specific molecular components.


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)

Chromosome reorganization after pachytene exit. See text for description. (A) Immunolocalization of REC-8 and SYP-1 at the pachytene–diplotene transition; late pachytene nuclei are at the left, diplotene at the right. Bar, 5 μm. (B) Projection halfway through a late pachytene nucleus showing unevenness in intensity of SYP-1 signal along bivalent (arrow). Bar, 2 μm. (C) Position of nuclei showing SYP-1 asymmetry (right side of a dashed line) relative to disappearance of RAD-51 foci. Bar, 10 μm. (D) Volume renderings of individual diplotene bivalents. Red, α-REC-8; green, α-SYP-1; blue, DAPI. i, X-shaped bivalent; ii-a–c, Y-shaped bivalent shown from two different angles. Bar, 5 μm. Videos 1 and 2 (available at http://www.jcb.org/cgi/content/full/jcb200410144/DC1) show rotating images of these bivalents. (E) Complete complement of bivalents from a single oocyte nucleus at early/mid-diakinesis. Bar, 5 μm.
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Related In: Results  -  Collection

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fig2: Chromosome reorganization after pachytene exit. See text for description. (A) Immunolocalization of REC-8 and SYP-1 at the pachytene–diplotene transition; late pachytene nuclei are at the left, diplotene at the right. Bar, 5 μm. (B) Projection halfway through a late pachytene nucleus showing unevenness in intensity of SYP-1 signal along bivalent (arrow). Bar, 2 μm. (C) Position of nuclei showing SYP-1 asymmetry (right side of a dashed line) relative to disappearance of RAD-51 foci. Bar, 10 μm. (D) Volume renderings of individual diplotene bivalents. Red, α-REC-8; green, α-SYP-1; blue, DAPI. i, X-shaped bivalent; ii-a–c, Y-shaped bivalent shown from two different angles. Bar, 5 μm. Videos 1 and 2 (available at http://www.jcb.org/cgi/content/full/jcb200410144/DC1) show rotating images of these bivalents. (E) Complete complement of bivalents from a single oocyte nucleus at early/mid-diakinesis. Bar, 5 μm.
Mentions: SC disassembly at the pachytene–diplotene transition is accompanied by a major transition in the organization of chromosome axes. REC-8 (Fig. 2) and HIM-3 (not depicted) continue to localize along the lengths of desynapsing chromosomes, but whereas REC-8 and HIM-3 signals appear as extended linear stretches in pachytene nuclei, this linear appearance gives way to a more convoluted appearance as nuclei enter diplonema. In a subset of diplotene nuclei, a coiled organization of chromosome axes can be clearly resolved (three-dimensional volume renderings in Fig. 2 D and Video 1, available at http://www.jcb.org/cgi/content/full/jcb200410144/DC1). Axis coiling coincides temporally with shortening of the end-to-end lengths of chromosomes that occurs at this stage, suggesting that coiling of preexisting axial structures may either contribute to or be a consequence of the chromosome shortening mechanism. Axis coiling during late meiotic prophase was observed previously in silver-stained preparations of rye and lily chromosomes (Fedotova et al., 1989; Stack, 1991); however, this is the first report of coiled axial structures during meiotic prophase visualized by imaging of specific molecular components.

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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