Excess crossovers impede faithful meiotic chromosome segregation in C. elegans


Autoři: Jeremy A. Hollis aff001;  Marissa L. Glover aff002;  Aleesa J. Schlientz aff002;  Cori K. Cahoon aff002;  Bruce Bowerman aff002;  Sarah M. Wignall aff001;  Diana E. Libuda aff002
Působiště autorů: Department of Molecular Biosciences, Northwestern University, Evanston, IL, United States of America aff001;  Institute of Molecular Biology, Department of Biology, University of Oregon, Eugene, OR, United States of America aff002
Vyšlo v časopise: Excess crossovers impede faithful meiotic chromosome segregation in C. elegans. PLoS Genet 16(9): e32767. doi:10.1371/journal.pgen.1009001
Kategorie: Research Article
doi: 10.1371/journal.pgen.1009001

Souhrn

During meiosis, diploid organisms reduce their chromosome number by half to generate haploid gametes. This process depends on the repair of double strand DNA breaks as crossover recombination events between homologous chromosomes, which hold homologs together to ensure their proper segregation to opposite spindle poles during the first meiotic division. Although most organisms are limited in the number of crossovers between homologs by a phenomenon called crossover interference, the consequences of excess interfering crossovers on meiotic chromosome segregation are not well known. Here we show that extra interfering crossovers lead to a range of meiotic defects and we uncover mechanisms that counteract these errors. Using chromosomes that exhibit a high frequency of supernumerary crossovers in Caenorhabditis elegans, we find that essential chromosomal structures are mispatterned in the presence of multiple crossovers, subjecting chromosomes to improper spindle forces and leading to defects in metaphase alignment. Additionally, the chromosomes with extra interfering crossovers often exhibited segregation defects in anaphase I, with a high incidence of chromatin bridges that sometimes created a tether between the chromosome and the first polar body. However, these anaphase I bridges were often able to resolve in a LEM-3 nuclease dependent manner, and chromosome tethers that persisted were frequently resolved during Meiosis II by a second mechanism that preferentially segregates the tethered sister chromatid into the polar body. Altogether these findings demonstrate that excess interfering crossovers can severely impact chromosome patterning and segregation, highlighting the importance of limiting the number of recombination events between homologous chromosomes for the proper execution of meiosis.

Klíčová slova:

Anaphase – Crossover interference – Homologous chromosomes – Chromatin – Chromosome structure and function – Meiosis – Metaphase – Oocytes


Zdroje

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