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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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Localization of SYP-1 and HIM-3 after pachytene exit in untreated and γ-irradiated spo-11 mutants. (A) Portions of germ lines extend from late pachynema (left) through mid/late diplonema (right). Closed arrowheads indicate diplotene nuclei in which SYP-1 is retained along the lengths of coiled axes; open arrowheads indicate nuclei in which SYP-1 has been lost from the majority of the chromosomes but is retained on some chromosomes; arrows indicate nuclei in which each desynapsing bivalent retains a single robust stretch of SYP-1, reflecting restoration of orderly asymmetric departure of SYP-1 by γ-irradiation. (B, top) Mid-diakinesis oocyte from an untreated spo-11 worm showing lack of chiasmata and SYP-1 distributed along the lengths of the axes. (bottom) Late diplotene oocyte from a γ-irradiated spo-11 worm showing SYP-1 concentrated on a region of each bivalent in the vicinity of and/or distal to the emerging chiasma. (C) Late diakinesis oocyte from a γ-irradiated spo-11 worm showing restoration of chiasmata. Bars, 5 μm.
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fig4: Localization of SYP-1 and HIM-3 after pachytene exit in untreated and γ-irradiated spo-11 mutants. (A) Portions of germ lines extend from late pachynema (left) through mid/late diplonema (right). Closed arrowheads indicate diplotene nuclei in which SYP-1 is retained along the lengths of coiled axes; open arrowheads indicate nuclei in which SYP-1 has been lost from the majority of the chromosomes but is retained on some chromosomes; arrows indicate nuclei in which each desynapsing bivalent retains a single robust stretch of SYP-1, reflecting restoration of orderly asymmetric departure of SYP-1 by γ-irradiation. (B, top) Mid-diakinesis oocyte from an untreated spo-11 worm showing lack of chiasmata and SYP-1 distributed along the lengths of the axes. (bottom) Late diplotene oocyte from a γ-irradiated spo-11 worm showing SYP-1 concentrated on a region of each bivalent in the vicinity of and/or distal to the emerging chiasma. (C) Late diakinesis oocyte from a γ-irradiated spo-11 worm showing restoration of chiasmata. Bars, 5 μm.

Mentions: The spo-11 mutant is severely impaired in achieving orderly asymmetric departure of SYP-1,2 from meiotic prophase chromosomes (Figs. 3 and 4 A). This is particularly evident at diplonema, when SYP-1,2 fail to become concentrated to a single short stretch per homologue pair. Instead, spo-11 diplotene nuclei exhibit several types of anomalies. In some nuclei, SYP-1 is retained along the full lengths of coiled axes, and DAPI-staining shows that the homologues are still largely synapsed; this differs from wild-type meiosis, where axis coiling is usually seen only in nuclei exhibiting extensive desynapsis. In other nuclei, SYP-1,2 have been lost from the entire lengths of most of the chromosomes within the nucleus, but a few bright chromosome-associated SYP-1,2 signals are present; the appearance of the HIM-3 signals and DAPI-stained chromatin in such nuclei indicates that homologues are largely desynapsed. Finally, some nuclei exhibit a mixture of these two phenotypes. In summary, meiotic chromosomes in the spo-11 mutant have not lost either the ability to retain or to eject SYP-1,2; rather, they have lost the capacity to coordinate retention and loss in a manner that results in reliable asymmetric differentiation of chromosomal subdomains.


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)

Localization of SYP-1 and HIM-3 after pachytene exit in untreated and γ-irradiated spo-11 mutants. (A) Portions of germ lines extend from late pachynema (left) through mid/late diplonema (right). Closed arrowheads indicate diplotene nuclei in which SYP-1 is retained along the lengths of coiled axes; open arrowheads indicate nuclei in which SYP-1 has been lost from the majority of the chromosomes but is retained on some chromosomes; arrows indicate nuclei in which each desynapsing bivalent retains a single robust stretch of SYP-1, reflecting restoration of orderly asymmetric departure of SYP-1 by γ-irradiation. (B, top) Mid-diakinesis oocyte from an untreated spo-11 worm showing lack of chiasmata and SYP-1 distributed along the lengths of the axes. (bottom) Late diplotene oocyte from a γ-irradiated spo-11 worm showing SYP-1 concentrated on a region of each bivalent in the vicinity of and/or distal to the emerging chiasma. (C) Late diakinesis oocyte from a γ-irradiated spo-11 worm showing restoration of chiasmata. Bars, 5 μm.
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Related In: Results  -  Collection

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fig4: Localization of SYP-1 and HIM-3 after pachytene exit in untreated and γ-irradiated spo-11 mutants. (A) Portions of germ lines extend from late pachynema (left) through mid/late diplonema (right). Closed arrowheads indicate diplotene nuclei in which SYP-1 is retained along the lengths of coiled axes; open arrowheads indicate nuclei in which SYP-1 has been lost from the majority of the chromosomes but is retained on some chromosomes; arrows indicate nuclei in which each desynapsing bivalent retains a single robust stretch of SYP-1, reflecting restoration of orderly asymmetric departure of SYP-1 by γ-irradiation. (B, top) Mid-diakinesis oocyte from an untreated spo-11 worm showing lack of chiasmata and SYP-1 distributed along the lengths of the axes. (bottom) Late diplotene oocyte from a γ-irradiated spo-11 worm showing SYP-1 concentrated on a region of each bivalent in the vicinity of and/or distal to the emerging chiasma. (C) Late diakinesis oocyte from a γ-irradiated spo-11 worm showing restoration of chiasmata. Bars, 5 μm.
Mentions: The spo-11 mutant is severely impaired in achieving orderly asymmetric departure of SYP-1,2 from meiotic prophase chromosomes (Figs. 3 and 4 A). This is particularly evident at diplonema, when SYP-1,2 fail to become concentrated to a single short stretch per homologue pair. Instead, spo-11 diplotene nuclei exhibit several types of anomalies. In some nuclei, SYP-1 is retained along the full lengths of coiled axes, and DAPI-staining shows that the homologues are still largely synapsed; this differs from wild-type meiosis, where axis coiling is usually seen only in nuclei exhibiting extensive desynapsis. In other nuclei, SYP-1,2 have been lost from the entire lengths of most of the chromosomes within the nucleus, but a few bright chromosome-associated SYP-1,2 signals are present; the appearance of the HIM-3 signals and DAPI-stained chromatin in such nuclei indicates that homologues are largely desynapsed. Finally, some nuclei exhibit a mixture of these two phenotypes. In summary, meiotic chromosomes in the spo-11 mutant have not lost either the ability to retain or to eject SYP-1,2; rather, they have lost the capacity to coordinate retention and loss in a manner that results in reliable asymmetric differentiation of chromosomal subdomains.

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
Related in: MedlinePlus