Abstract
Although end-on microtubule–kinetochore attachments typically drive chromosome alignment, Caenorhabditis elegans oocytes do not form these connections. Instead, microtubule bundles run laterally alongside chromosomes and a ring-shaped protein complex facilitates congression (the “ring complex”, RC). Here, we report new aspects of RC and chromosome structure that are required for congression and segregation. First, we found that in addition to encircling the outside of each homologous chromosome pair (bivalent), the RC also forms internal subloops that wrap around the domains where cohesion is lost during the first meiotic division; cohesin removal could therefore disengage these subloops in anaphase, enabling RC removal from chromosomes. Additionally, we discovered new features of chromosome organization that facilitate congression. Analysis of a mutant that forms bivalents with a fragile, unresolved homolog interface revealed that these bivalents are usually able to biorient on the spindle, with lateral microtubule bundles running alongside them and constraining the chromosome arms so that the two homologs are pointed to opposite spindle poles. This biorientation facilitates congression, as monooriented bivalents exhibited reduced polar ejection forces that resulted in congression defects. Thus, despite not forming end-on attachments, chromosome biorientation promotes congression in C. elegans oocytes. Our work therefore reveals novel features of chromosome organization in oocytes and highlights the importance of proper chromosome structure for faithful segregation during meiotic divisions.
| Original language | English (US) |
|---|---|
| Article number | br25 |
| Journal | Molecular biology of the cell |
| Volume | 33 |
| Issue number | 14 |
| DOIs | |
| State | Published - Dec 1 2022 |
Funding
We would like to thank Tom Hope’s lab at Northwestern University for providing training and access to the OMX superresolution microscope and Keila Torre-Santiago for help with acquisition of the image in Figure 1C. We would also like to thank members of the Wig-nall lab and the WiLa ICB for support and guidance, particularly Gabe Cavin-Meza, Emily Czajkowski, Jordy Martinez, and Juhi Na-rula for providing feedback on the manuscript. We are grateful to Arshad Desai, Andy Golden, Federico Pelisch, and Jill Schumacher for antibodies and the Caenorhabditis Genetics Center, funded by the NIH Office of Research Infrastructure Programs (P40 OD010440), for strains. This work was supported by Cellular and Molecular Basis of Disease (CMBD) Training Grant NIH T32 GM00806 (to H.E.H.) and NIH R01GM124354 (to S.M.W.). Microscopy was performed at the Biological Imaging Facility at Northwestern University, supported by the Chemistry for Life Processes Institute, the NU Office for Research, and the Department of Molecular Biosciences. We would like to thank Tom Hope’s lab at Northwestern University for providing training and access to the OMX superresolution microscope and Keila Torre-Santiago for help with acquisition of the image in Figure 1C. We would also like to thank members of the Wignall lab and the WiLa ICB for support and guidance, particularly Gabe Cavin-Meza, Emily Czajkowski, Jordy Martinez, and Juhi Narula for providing feedback on the manuscript. We are grateful to Arshad Desai, Andy Golden, Federico Pelisch, and Jill Schumacher for antibodies and the Caenorhabditis Genetics Center, funded by the NIH Office of Research Infrastructure Programs (P40 OD010440), for strains. This work was supported by Cellular and Molecular Basis of Disease (CMBD) Training Grant NIH T32 GM00806 (to H.E.H.) and NIH R01GM124354 (to S.M.W.). Microscopy was performed at the Biological Imaging Facility at Northwestern University, supported by the Chemistry for Life Processes Institute, the NU Office for Research, and the Department of Molecular Biosciences.
ASJC Scopus subject areas
- Molecular Biology
- Cell Biology