Excess crossovers impede faithful meiotic chromosome segregation in C. elegans
| dc.contributor.author | Hollis, Jeremy A. | |
| dc.contributor.author | Glover, Marissa L. | |
| dc.contributor.author | Schlientz, Aleesa J. | |
| dc.contributor.author | Cahoon, Cori K. | |
| dc.contributor.author | Bowerman, Bruce | |
| dc.contributor.author | Wignall, Sarah M. | |
| dc.contributor.author | Libuda, Diana E. | |
| dc.date.accessioned | 2022-10-17T23:33:17Z | |
| dc.date.available | 2022-10-17T23:33:17Z | |
| dc.date.issued | 2020-09-04 | |
| dc.description | 31 pages | en_US |
| dc.description.abstract | 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. | en_US |
| dc.description.sponsorship | This work was supported by the National Institutes of Health (NIH) R01GM124354 to SMW, NIH R00HD076165 and NIH R35GM128890 to DEL, NIH R01GM049869 and NIH R35GM217221 to BB, NIH T32GM007413 to AJS, and a Jane Coffin Childs Postdoctoral Fellowship to CKC. DEL is also a Searle Scholar and recipient of a March of Dimes Basil O’Connor Starter Scholar award. Some strains were provided by the CGC which is funded by NIH P40 OD010440. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. | en_US |
| dc.identifier.citation | Hollis JA, Glover ML, Schlientz AJ, Cahoon CK, Bowerman B, Wignall SM, et al. (2020) Excess crossovers impede faithful meiotic chromosome segregation in C. elegans. PLoS Genet 16(9): e1009001. https://doi.org/10.1371/journal.pgen.1009001 | en_US |
| dc.identifier.uri | https://doi.org/10.1371/journal.pgen.1009001 | |
| dc.identifier.uri | https://hdl.handle.net/1794/27705 | |
| dc.language.iso | en | en_US |
| dc.publisher | Public Library of Science | en_US |
| dc.rights | Creative Commons BY-NC-ND 4.0-US | en_US |
| dc.subject | Oocytes | en_US |
| dc.subject | Anaphase | en_US |
| dc.subject | Meiosis | en_US |
| dc.subject | Chromosome structure and function | en_US |
| dc.subject | Crossover interference | en_US |
| dc.subject | Homologous chromosomes | en_US |
| dc.subject | Metaphase | en_US |
| dc.title | Excess crossovers impede faithful meiotic chromosome segregation in C. elegans | en_US |
| dc.type | Article | en_US |