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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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HCP-6 is required for chromosome segregation in meiosis I and II. In wild-type zygotes, GFP::H2B histone-tagged chromosomes align on the metaphase plate after breakdown of the oocyte nuclear envelope. Homologues separate in anaphase of meiosis I; one set is extruded into the first polar body (PB1). Sister chromatids separate in meiosis II; one set is extruded into the second polar body (PB2). The second set decondenses and forms the oocyte pronucleus (O). In hcp-6(mr17) and hcp-6(mr17, RNAi) mutants, DNA bridges connected separating chromosomes in anaphase I and II (arrows). Bars, 5 μm.
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fig3: HCP-6 is required for chromosome segregation in meiosis I and II. In wild-type zygotes, GFP::H2B histone-tagged chromosomes align on the metaphase plate after breakdown of the oocyte nuclear envelope. Homologues separate in anaphase of meiosis I; one set is extruded into the first polar body (PB1). Sister chromatids separate in meiosis II; one set is extruded into the second polar body (PB2). The second set decondenses and forms the oocyte pronucleus (O). In hcp-6(mr17) and hcp-6(mr17, RNAi) mutants, DNA bridges connected separating chromosomes in anaphase I and II (arrows). Bars, 5 μm.

Mentions: Chromosome condensation is essential for chromosome segregation in mitosis and is a conserved feature of chromosome segregation in meiosis, yet a conserved role for condensin in meiosis has not been established. Therefore, we assessed the requirement for condensin in meiosis I and II of C. elegans in animals with chromosomes tagged by a GFP::H2B histone (Praitis et al., 2001). Prominent DNA bridges formed between segregating chromosomes during anaphase I and anaphase II in all hcp-6(mr17, RNAi) zygotes observed (n = 15; Fig. 3). Chromatin bridges also formed in all hcp-6(mr17) zygotes, but were consistently less severe in anaphase I than in anaphase II (n = 9; Fig. 3). Chromosome segregation defects were detected during meiosis II (but not meiosis I) in animals treated with RNAi to deplete HCP-6 (unpublished data), consistent with the report that only anaphase II was affected by RNAi depletion of MIX-1 or SMC-4 (Hagstrom et al., 2002). Thus, condensin is essential for homologue segregation in meiosis I, but this segregation appears less sensitive to condensin depletion than sister chromatid segregation in meiosis II. The combined results from worms, yeast (Yu and Koshland, 2003), and plants (Siddiqui et al., 2003) indicate a conserved requirement for condensin activity in both meiotic divisions.


Condensin restructures chromosomes in preparation for meiotic divisions.

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

HCP-6 is required for chromosome segregation in meiosis I and II. In wild-type zygotes, GFP::H2B histone-tagged chromosomes align on the metaphase plate after breakdown of the oocyte nuclear envelope. Homologues separate in anaphase of meiosis I; one set is extruded into the first polar body (PB1). Sister chromatids separate in meiosis II; one set is extruded into the second polar body (PB2). The second set decondenses and forms the oocyte pronucleus (O). In hcp-6(mr17) and hcp-6(mr17, RNAi) mutants, DNA bridges connected separating chromosomes in anaphase I and II (arrows). Bars, 5 μm.
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Related In: Results  -  Collection

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fig3: HCP-6 is required for chromosome segregation in meiosis I and II. In wild-type zygotes, GFP::H2B histone-tagged chromosomes align on the metaphase plate after breakdown of the oocyte nuclear envelope. Homologues separate in anaphase of meiosis I; one set is extruded into the first polar body (PB1). Sister chromatids separate in meiosis II; one set is extruded into the second polar body (PB2). The second set decondenses and forms the oocyte pronucleus (O). In hcp-6(mr17) and hcp-6(mr17, RNAi) mutants, DNA bridges connected separating chromosomes in anaphase I and II (arrows). Bars, 5 μm.
Mentions: Chromosome condensation is essential for chromosome segregation in mitosis and is a conserved feature of chromosome segregation in meiosis, yet a conserved role for condensin in meiosis has not been established. Therefore, we assessed the requirement for condensin in meiosis I and II of C. elegans in animals with chromosomes tagged by a GFP::H2B histone (Praitis et al., 2001). Prominent DNA bridges formed between segregating chromosomes during anaphase I and anaphase II in all hcp-6(mr17, RNAi) zygotes observed (n = 15; Fig. 3). Chromatin bridges also formed in all hcp-6(mr17) zygotes, but were consistently less severe in anaphase I than in anaphase II (n = 9; Fig. 3). Chromosome segregation defects were detected during meiosis II (but not meiosis I) in animals treated with RNAi to deplete HCP-6 (unpublished data), consistent with the report that only anaphase II was affected by RNAi depletion of MIX-1 or SMC-4 (Hagstrom et al., 2002). Thus, condensin is essential for homologue segregation in meiosis I, but this segregation appears less sensitive to condensin depletion than sister chromatid segregation in meiosis II. The combined results from worms, yeast (Yu and Koshland, 2003), and plants (Siddiqui et al., 2003) indicate a conserved requirement for condensin activity in both meiotic divisions.

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