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Condensin restructures chromosomes in preparation for meiotic divisions.

Chan RC, Severson AF, Meyer BJ - J. Cell Biol. (2004)

Bottom Line: We showed that condensin, the protein complex needed for mitotic chromosome compaction, restructures chromosomes during meiosis in Caenorhabditis elegans.Condensin helps resolve cohesin-independent linkages between sister chromatids and alleviates recombination-independent linkages between homologues.The safeguarding of chromosome resolution by condensin permits chromosome segregation and is crucial for the formation of discrete, individualized bivalent chromosomes.

View Article: PubMed Central - PubMed

Affiliation: Howard Hughes Medical Institute, Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA.

ABSTRACT
The production of haploid gametes from diploid germ cells requires two rounds of meiotic chromosome segregation after one round of replication. Accurate meiotic chromosome segregation involves the remodeling of each pair of homologous chromosomes around the site of crossover into a highly condensed and ordered structure. We showed that condensin, the protein complex needed for mitotic chromosome compaction, restructures chromosomes during meiosis in Caenorhabditis elegans. In particular, condensin promotes both meiotic chromosome condensation after crossover recombination and the remodeling of sister chromatids. Condensin helps resolve cohesin-independent linkages between sister chromatids and alleviates recombination-independent linkages between homologues. The safeguarding of chromosome resolution by condensin permits chromosome segregation and is crucial for the formation of discrete, individualized bivalent chromosomes.

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Condensin is required for chromosome organization within diakinesis bivalents. (A) AIR-2 localized at the midbivalent in wild-type and hcp-6(mr17) animals. In contrast, SMC-1 adopted a cruciform pattern in wild-type bivalents, but was disorganized in hcp-6(mr17) and mix-1(b285) bivalents. Each panel shows a representative subset of bivalents in a single diakinesis nucleus. (B) AIR-2 and SMC-3 colocalized along the length of synapsed pachytene homologues in wild-type and hcp-6(mr17) animals. (C) During SC disassembly, AIR-2 diminished along the desynapsed region of each homologue pair. AIR-2 persisted along the synapsed region (solid arrowhead). SMC-3 staining persisted along the entire length of homologue pairs, revealing the separation of desynapsed regions (hollow arrowhead). Bars, 5 μm.
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fig7: Condensin is required for chromosome organization within diakinesis bivalents. (A) AIR-2 localized at the midbivalent in wild-type and hcp-6(mr17) animals. In contrast, SMC-1 adopted a cruciform pattern in wild-type bivalents, but was disorganized in hcp-6(mr17) and mix-1(b285) bivalents. Each panel shows a representative subset of bivalents in a single diakinesis nucleus. (B) AIR-2 and SMC-3 colocalized along the length of synapsed pachytene homologues in wild-type and hcp-6(mr17) animals. (C) During SC disassembly, AIR-2 diminished along the desynapsed region of each homologue pair. AIR-2 persisted along the synapsed region (solid arrowhead). SMC-3 staining persisted along the entire length of homologue pairs, revealing the separation of desynapsed regions (hollow arrowhead). Bars, 5 μm.

Mentions: Pachytene chromosome organization appeared normal in hcp-6 mutants (Fig. 6 A), consistent with the association of HCP-6 with chromosomes after pachytene exit. 5S rDNA FISH indicated that synapsis was unaffected by hcp-6 inactivation. Moreover, SC central element SYP-1 and cohesin subunits SMC-1 and SMC-3 localized between homologues, as in wild type (Fig. 6 A, Fig. 7 A). In hcp-6(mr17) and hcp-6(mr17, RNAi) animals, homologue pairs appeared normally compacted and had no obvious attachments to other homologue pairs in late pachytene nuclei (Fig. 6 A; unpublished data). Finally, linkages between homologues were resolved because rec-8(RNAi) caused similar levels of asynapsis in late pachytene nuclei of hcp-6(mr17) animals grown at 15 and 25°C (Fig. 8 A). Both the timing of condensin localization and the phenotypes of condensin mutants suggest that factors other than HCP-6 mediate the condensation, individualization, and resolution of chromosomes accompanying entry into pachytene. However, we cannot exclude the possibility that residual condensin function is sufficient for these processes.


Condensin restructures chromosomes in preparation for meiotic divisions.

Chan RC, Severson AF, Meyer BJ - J. Cell Biol. (2004)

Condensin is required for chromosome organization within diakinesis bivalents. (A) AIR-2 localized at the midbivalent in wild-type and hcp-6(mr17) animals. In contrast, SMC-1 adopted a cruciform pattern in wild-type bivalents, but was disorganized in hcp-6(mr17) and mix-1(b285) bivalents. Each panel shows a representative subset of bivalents in a single diakinesis nucleus. (B) AIR-2 and SMC-3 colocalized along the length of synapsed pachytene homologues in wild-type and hcp-6(mr17) animals. (C) During SC disassembly, AIR-2 diminished along the desynapsed region of each homologue pair. AIR-2 persisted along the synapsed region (solid arrowhead). SMC-3 staining persisted along the entire length of homologue pairs, revealing the separation of desynapsed regions (hollow arrowhead). Bars, 5 μm.
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Related In: Results  -  Collection

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fig7: Condensin is required for chromosome organization within diakinesis bivalents. (A) AIR-2 localized at the midbivalent in wild-type and hcp-6(mr17) animals. In contrast, SMC-1 adopted a cruciform pattern in wild-type bivalents, but was disorganized in hcp-6(mr17) and mix-1(b285) bivalents. Each panel shows a representative subset of bivalents in a single diakinesis nucleus. (B) AIR-2 and SMC-3 colocalized along the length of synapsed pachytene homologues in wild-type and hcp-6(mr17) animals. (C) During SC disassembly, AIR-2 diminished along the desynapsed region of each homologue pair. AIR-2 persisted along the synapsed region (solid arrowhead). SMC-3 staining persisted along the entire length of homologue pairs, revealing the separation of desynapsed regions (hollow arrowhead). Bars, 5 μm.
Mentions: Pachytene chromosome organization appeared normal in hcp-6 mutants (Fig. 6 A), consistent with the association of HCP-6 with chromosomes after pachytene exit. 5S rDNA FISH indicated that synapsis was unaffected by hcp-6 inactivation. Moreover, SC central element SYP-1 and cohesin subunits SMC-1 and SMC-3 localized between homologues, as in wild type (Fig. 6 A, Fig. 7 A). In hcp-6(mr17) and hcp-6(mr17, RNAi) animals, homologue pairs appeared normally compacted and had no obvious attachments to other homologue pairs in late pachytene nuclei (Fig. 6 A; unpublished data). Finally, linkages between homologues were resolved because rec-8(RNAi) caused similar levels of asynapsis in late pachytene nuclei of hcp-6(mr17) animals grown at 15 and 25°C (Fig. 8 A). Both the timing of condensin localization and the phenotypes of condensin mutants suggest that factors other than HCP-6 mediate the condensation, individualization, and resolution of chromosomes accompanying entry into pachytene. However, we cannot exclude the possibility that residual condensin function is sufficient for these processes.

Bottom Line: We showed that condensin, the protein complex needed for mitotic chromosome compaction, restructures chromosomes during meiosis in Caenorhabditis elegans.Condensin helps resolve cohesin-independent linkages between sister chromatids and alleviates recombination-independent linkages between homologues.The safeguarding of chromosome resolution by condensin permits chromosome segregation and is crucial for the formation of discrete, individualized bivalent chromosomes.

View Article: PubMed Central - PubMed

Affiliation: Howard Hughes Medical Institute, Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA.

ABSTRACT
The production of haploid gametes from diploid germ cells requires two rounds of meiotic chromosome segregation after one round of replication. Accurate meiotic chromosome segregation involves the remodeling of each pair of homologous chromosomes around the site of crossover into a highly condensed and ordered structure. We showed that condensin, the protein complex needed for mitotic chromosome compaction, restructures chromosomes during meiosis in Caenorhabditis elegans. In particular, condensin promotes both meiotic chromosome condensation after crossover recombination and the remodeling of sister chromatids. Condensin helps resolve cohesin-independent linkages between sister chromatids and alleviates recombination-independent linkages between homologues. The safeguarding of chromosome resolution by condensin permits chromosome segregation and is crucial for the formation of discrete, individualized bivalent chromosomes.

Show MeSH
Related in: MedlinePlus